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Medical Ultrasonography Journal 1/2023

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MEDICAL Volume 25, Number 1

March 2023

ULTRASONOGRAPHY
A N I N T E R N A T I O N A L J O U R N A L O F C L I N I C A L I M A G I N G

„ What happens under the flexor tendons of the fingers in dactylitis?


„ Can the Vesical Imaging Reporting and Data System (VI-RADS)
score be applied in conventional ultrasound and
contrast-enhanced ultrasound to differentiate muscle-invasive
bladder cancer?
„ Ultrasonography on the non-living. Current approaches.
Early Liver
13425

Diagnosis
The difference is in the details

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Ultrasound Derived Fat Fraction (UDFF)


UDFF, with a total exam time of less than 1 minute is the only
ultrasound technology to classify hepatic steatosis as an index value
greater that 5%, delivering a similar clinical utility as MR-PDFF1, 2.

Ultrasound Derived Fat Fraction (UDFF)


UDFF 2% UDFF 17% UDFF 26%

MR – Proton Derived Fat Fraction (PDFF)


PDFF 1.5% PDFF 17.6% PDFF 26.5%

Learn more
No Steatosis Moderate Steatosis Severe Steatosis

1
Labyed, Y, PhD. Milkowski, A, MSc. Novel Method for Ultrasound-Derived Fat
Fraction Using an Integrated Phantom.
2
Quantification of Hepatic Steatosis by Ultrasound: Prospective Comparison
with MRI PDFF as Reference Standard |ajronline.org/doi/10.2214/AJR.22.27878
Contents

Editorial
The vincula system - an anatomical and functional crossroad
M.C. Micu, C.M. García-de-Pereda-Notario ................................................................................................................................ 5

Original papers
Diagnostic performance of a novel ultrasound-based quantitative method to assess liver steatosis in histologically
identified nonalcoholic fatty liver disease
K.A. Kang, S.R. Lee, D.W. Jun, I-G. Do, M.S. Kim ....................................................................................................................... 7
Percutaneous transhepatic ultrasound-guided gallbladder aspiration: Still a safe option for gallbladder
decompression in patients at high surgical risk
K. Bock, B. Heidrich, S. Zender, H. Wedemeyer, A. Potthoff, H. Lenzen ..................................................................................... 14
Can the Vesical Imaging Reporting and Data System (VI-RADS) score be applied in conventional ultrasound and
contrast-enhanced ultrasound to differentiate muscle-invasive bladder cancer?
J. Zhu, X. Huang, L. Liu, N. Wang, F. Nie ................................................................................................................................... 22
Mammography and breast ultrasound analysis in male and female transgender persons using long-term gender
affirming hormone therapy: a cross-sectional study in Brazil
A.A. Bartolamei Ramos, C. Spadoni, P. Santander, B. dos Santos, R. Andrade, J. Kulak .......................................................... 29
Ultrasound-guided versus computed tomography-controlled periradicular injections of the first sacral nerve:
a prospective randomized clinical trial
M. Plaikner, N. Kögl, H. Gruber, R. Bale, W.M. Ho, E. Skalla-Oberherber, A. Loizides ............................................................ 35
What happens under the flexor tendons of the fingers in dactylitis?
E. Naredo, R. Largo, O. Olivas-Vergara, C. Herencia, M. Mateos-Fernández, C.M. García-de-Pereda-Notario,
J.R. Mérida-Velasco, G. Herrero-Beaumont, J. Murillo-González ............................................................................................. 42
The value of percutaneous ultrasound-guided subacromial bursography in the diagnosis of rotator cuff tears
R. Li, M. Li, Y. Cui, P. Yang, C. hang .......................................................................................................................................... 48

Reviews
Ultrasonography on the non-living. Current approaches.
T. Thomsen, M. Blaivas, P. Sadiva, O.D. Kripfgans, H-L. Chan, Y. Dong, M.C. Chammas, B. Hoffman, C.F. Dietrich ........... 56
Role of emergency chest ultrasound in traumatic pneumothorax. An updated meta-analysis
H. Tian, T. Zhang, Y. Zhou, S. Rastogi, R. Choudhury, J. Iqbal .................................................................................................. 66
Diagnostic accuracy of ultrasonography for the confirmation of endotracheal tube intubation:
a systematic review and meta-analysis
X. Li, J. Zhang, M. Karunakaran, V.S. Hariharan ...................................................................................................................... 72
Scoping Review: Ultrasonographic evidence of intraabdominal manifestations of COVID-19 infection
S. Dehmani, N. Penkalla, E.M. Jung, C. De Molo, C. Serra, B. Hoffmann, C. Fang, C.F. Dietrich .......................................... 82

Pictorial essay
Preoperative ultrasound study of differentiated thyroid cancer: relevant aspects for its optimal performance.
Pictorial essay.
M. Hirsch, J. Matus, C. Orellana, K Krauss ............................................................................................................................... 93
Medical Ultrasonography
Official Journal of the Romanian Society for Ultrasonography in Medicine and Biology
Medical Ultrasonography (formerly Revista Româna de Ultrasonografie from 1999 to 2008) is the official publication of the
Romanian Society for Ultrasonography in Medicine and Biology (SRUMB). Starting with 2008 the entire content of Medical
Ultrasonography is published in English, quarterly. The journal aims to promote ultrasound diagnosis by publishing papers in a
variety of categories, including Original papers, Review Articles, Pictorial Essays, Technical Innovations, Case Report, or Letters to
the Editor (fundamental as well as methodological and educational papers). The published papers cover a wide variety of discipline
of ultrasound. The journal also host information regarding the society’s activities, the scheduling of accredited training courses in
ultrasound diagnosis, as well as the agenda of national and international scientific events.
Medical Ultrasonography is now listed in Science Citation Index Expanded/ ISI Thomson Master Journal List, Medline/
PubMed, Scopus, Pro Quest, Ebsco, and Index Copernicus data bases. Impact Factor 1.75 (JCR 2021); 5 year IF= 1.975
Editorial Office
2nd Medical Clinic, 2-4 Clinicilor str., 400006 Cluj-Napoca, Romania
Tel.: +4 0264 591942/442, Fax: +4 0264 596912, Email: medultrasonography@gmail.com
Contact person: Daniela Fodor, email: dfodor@ymail.com
Journal web site: http://www.medultrason.ro
Editorial board
Editor in Chief Methodological adviser Editors Assistant Editors English language editors
Daniela Fodor Petru Adrian Mircea Radu Ion Badea Carolina Solomon Sally Wood-Lamont
Sorin Marian Dudea Bogdan Chis Ioana Robu
Oana Serban
Members
Mihaela Băciuţ (Cluj-Napoca, Romania) Richard Hoppmann (Columbia, South Carolina, USA Alina Popescu (Timişoara, Romania)
Boris Brkljacic (Zagreb, Croatia) Walter Grassi (Ancona, Italy) Alper Ozel (Istambul, Turkey)
Ciprian Brisc (Oradea, Romania) Lucas Greiner (Wuppertal, Germany) Adrian Săftoiu (Craiova, Romania)
Vito Cantisani (Rome, Italy) Norbert Gritzmann (Salzburg, Austria) Paul Singh Sidhu (London, UK)
Anca Ciurea (Cluj-Napoca, Romania) Zoltán Harkányi (Budapest, Hungary) Zeno Spârchez (Cluj-Napoca, Romania)
Sorin Crişan (Cluj-Napoca, Romania) Anamaria Iagnocco (Rome, Italy) Ioan Sporea (Timişoara, Romania)
Adrian Costache (Bucureşti, Romania) Adnan Kabaalioglu (Antalya, Turkey) Florin Stamatian (Cluj-Napoca)
Jarosław Czubak (Otwock, Poland) Daniel Lichtenstein (Paris, France) Dan Stănescu (Bucureşti, Romania)
Christoph Dietrich (Frankfurt am Main, Germany) Carmen Mihaela Mihu (Cluj-Napoca, Romania) Iwona Sudoł-Szopińska (Warsaw, Poland)
Dan Dumitraşcu (Cluj-Napoca) Dan Mihu (Cluj-Napoca, Romania) Kazmierz Szopinski (Warsaw, Poland)
Viorela Enăchescu (Craiova, Romania) Daniel Muresan (Cluj-Napoca, Romania) Adrian Şanta (Sibiu, Romania)
Otilia Fufezan (Cluj-Napoca, Romania) Luca Neri (Milan, Italy) Roxana Sirli (Timişoara, Romania)
Odd Helge Gilja (Bergen, Norway) Monica Platon Lupsor (Cluj-Napoca, Romania)
Tehnical staff Instruction for authors: Subscription information:
Iulia China Full instructions are available online at http://www.medultrason.ro/ Medical Ultrasonography is published quarterly.
authors-guidelines/ and at the end pages of the journal. ISSN (print) 1844–4172; ISSN (online) 2066–8643
The annual subscription:
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Contents
(continued)

Continuing education
Ultrasound guided Interpectoral, Pectoserratus and Serratus anterior plane blocks
G. Armissoglio, P. Serchan, L. Griseto, G. Iohom ....................................................................................................................... 98

Case report
Transcatheter aortic valve implantation in a patient with interventricular membranous septal aneurysm
resulted in cardiac tamponade of unclear etiology
M.I. Dregoesc, D.I. Bindea, M.C. Marc, V. Sasarman, A.C. Iancu ........................................................................................... 104
The “starry night” (diffuse microcalcific myopathy) – thousands of muscle microcalcifications after 30 years of
Trichinella infection detected by ultrasound
D. Fodor, C. Georgiu, M. Pelea, O. Serban, A. Micu, M.C. Micu ............................................................................................ 107

Letters to the Editor


Echocardiography in the detection of lead-related infective endocarditis
T. Bečić, V. Carević, R. Perković-Avelini, D. Fabijanić ............................................................................................................. 111
EUS-guided drainage for pancreatic duct stone combined with main pancreatic duct stenosis after
pancreaticoduodenectomy: a case report
H. He, T. Yu, Y. Li, S. Hou, L Zhang .......................................................................................................................................... 112
Right atrial thrombosis and lymphoblastic leukemia
F. Jiang, C. Han ......................................................................................................................................................................... 113
Evaluation and subsequent treatment for superficial peroneal entrapment and hypertrophic scar using
high-resolution ultrasound
C-Y. Kuo, K-C. Wei .................................................................................................................................................................... 114
EUS-guided fine needle biopsy for hepatocarcinoma of the right liver lobe as a rescue diagnostic technique
after a negative percutaneous guided liver biopsy
A.I. Tantau, T. Zaharie ............................................................................................................................................................... 115
Flexor hallucis brevis’ trigger point and dry needling treatment: a myofascial pain syndrome perspective
on big toe pain
M.H. Temel, E. Özyiğit .............................................................................................................................................................. 116
Intramural ectopic pregnancy at 21 weeks of gestation
Y. Wei, J. Wang, H. Luo ............................................................................................................................................................. 117
Ultrasound imaging and guided intervention for the middle cluneal nerve
W-T. Wu, Y-C. Hsu, K. Mezian, V. Ricci, K-V. Chang, L. Özçakar ............................................................................................ 119
Ultrasonographic and pathological findings of a secretory carcinoma of the parotid gland
X. Zhang, D. Wu, J. Chen .......................................................................................................................................................... 120
Editorial Med Ultrason 2023, Vol. 25, no. 1, 5-6
DOI: 10.11152/mu-4099

The vincula system - an anatomical and functional crossroad


Mihaela Cosmina Micu1, Carlos Miquel García-de-Pereda-Notario2

1Rheumatology Division, Rehabilitation Clinical Hospital Cluj-Napoca, Romania, 2Department of Anatomy and
Embryology, Faculty of Medicine, Universidad Complutense of Madrid, Madrid, Spain

In psoriatic arthritis (PsA), the heterogeneity of the vasodilation and endothelial dysfunction, triggers a chain
clinical features and of the musculoskeletal imaging pic- reaction further amplifying the inflammatory loop [12-17].
tures has attracted a wide interest among rheumatologists The importance of the vascular involvement is sup-
in the last years. In fact, clinicians need to understand the ported also by the fact that the most common digital le-
importance of different anatomical structures that may be sions depicted on ultrasound, in more than half of the
affected at one point in time during the disease evolution. digits, are soft tissue thickening and subcutaneous edema
In PsA, dactylitis, a key feature occurring in about doubled by subcutaneous hyperemia [4]. Indeed, the
50% of the patients mostly in early disease stages, has most frequent combination of ultrasound abnormalities
been now included in the Classification Criteria for Pso- in addition to synovitis proved to be subcutaneous edema
riatic Arthritis (CASPAR) [1,2]. However, the pathoge- and flexor tenosynovitis. Interestingly, flexor tenosyno-
netic sequences, the precise anatomical structures and the vitis was found also as an independent pathology in 17%
tissues involvement is still under scrutiny. of the cases [4].
The use of higher resolution imaging methods, ei- The analysis of the anatomical structures and imaging
ther in clinical studies or in daily practice, together with details designates the digital flexor tendons vincula sys-
anatomical information derived from cadaveric studies, tem as an entity connecting the palmar and articular/digi-
has allowed a better understanding of the involvement of tal arterial vascular system with a transitional synovium
the anatomical structures in PsA patients [4-11]. Recent layer and with the flexor tendon sheath [8,10].
studies have emphasized the relevance of enthesitis and In this framework, Naredo et al [18] compares and
mini-enthesitis, flexor tenosynovitis, flexor tendon pulley discusses sonopathology elements in a mechanical model
inflammation, extensor tendonitis, bone marrow edema, of digital tenosynovitis obtained in cadavers (intra-ten-
synovitis and soft tissue thickening and edema [3-8]. don sheath silicon injection) versus inflammatory teno-
In 2007, McGonagle et al proposed the synovio-en- synovitis in PsA patients. The results of this study reiter-
theseal concept (SEC) to explain the initial trigger and ate not only the importance of the SEC underpinning the
the events succession [11]. This model starts from the structures involvement in PsA but also highlights for the
premise that a primary entheseal biomechanical stress or first time the importance of the vincula system involve-
tissue damage is inducing an aberrant innate and adaptive ment and its contribution to the local inflammatory lesion
immune response which leads abruptly to the release of spectrum, generating particular grey scale and Doppler
endogenous pro-inflammatory molecules that will further ultrasound findings.
commence and perpetuate inflammation and damage in- Moreover, among the vincula system variety (num-
side the synovium (the deep Koebner phenomenon). In ber and precise location) described in anatomical studies
parallel, a massive local angiogenesis process and a vast [8,18], apparently there is also a vascular pattern vari-
vascular inflammation, supported in the initial phases by ety showing different kind of anastomoses between the
arterial branches at metacarpo-phalangeal joints (MCPj)
Received Accepted and the first phalangeal level. Recently, Baksa et al [19]
Med Ultrason described the vascular supply to the MCP joint showing
2023, Vol. 25, No 1, 5-6 the presence of two distinct vascular territories: the meta-
Corresponding author: Mihaela C. Micu
Rheumatology Division, Rehabilitation
carpal half that receives arteries from the palmar meta-
Clinical Hospital Cluj-Napoca, Romania carpal arteries or proper palmar digital arteries, while the
E-mail: mcmicu@yahoo.com phalangeal half is supplied by both proper and common
6 M. C. Micu, C. M. García-de-Pereda-Notario The vincula system - an anatomical and functional crossroad

palmar digital arteries. Therefore, it might be suggested and their reliability in a clinical setting. Clin Rheumatol
that some of the vinculae receive a two-territory com- 2021;40:1061-1067.
bined arterial supply. The vascular pattern description is 5. Healy PJ, Groves C, Chandramohan M, Helliwell PS. MRI
changes in psoriatic dactylitis–extent of pathology, rela-
based on a cadaveric model where arteries were inject-
tionship to tenderness and correlation with clinical indices.
ed, the specimens were cryosectioned, photographed in
Rheumatology 2008;47:92–95.
high-resolution and reconstruction of the arterial pattern 6. Tinazzi I, McGonagle D, Macchioni P, Aydin SZ. Power
of the joints was obtained. Doppler enhancement of accessory pulleys confirming dis-
In this scenario, the vincula system seems to take the ease localization in psoriatic dactylitis. Rheumatology (Ox-
stage as a key player among different musculoskeletal ford) 2020;59:2030-2034.
structures that are involved in PsA. It might be hypothe- 7. Zabotti A, Idolazzi L, Batticciotto A, et al. Enthesitis of the
sized that the vinculae operate as an accessory anchorage hands in psoriatic arthritis: an ultrasonographic perspective.
structure of the flexor tendon, structurally and function- Med Ultrason 2017;19:438-443.
ally bridging different anatomical compartments through 8. Armenta E, Lehrman A. The vincula to the flexor tendons
connective tissue, synovial tissue and via vascularization. of the hand. J Hand Surg Am 1980;5:127-134.
9. Flindall E, McGrouther DA. Accesory roles of the vincu-
In this very peculiar anatomical region, the variation of
lum breve of the flexor digitorum profundus and check-rein
the local vascular supply might generate different ultra- ligaments at the distal interphalangeal joint. J Hand Surg Br
sound disease expression and patterns in different fingers 1991;16: 305-310.
and in different PsA patients. 10. Cohen MJ, Kaplan L. Histology and ultrastructure of the hu-
Today, clearly, dactylitis is still waiting for a more man flexor tendon sheath. J Hand Surg Am 1987;12:25-29.
comprehensive definition and the imaging methods are 11. McGonagle D, Lories RJ, Tan AL, Benjamin M. The con-
therefore increasing our knowledge of the anatomical cept of a “synovio-entheseal complex” and its implications
structures that are contributing to the inflammatory pro- for understanding joint inflammation and damage in psori-
cess involved in dactilytis. Therefore, the definition is atic arthritis and beyond. Arthritis Rheum. 2007;56:2482-
clearly under evolution and refining. Moreover, we are 2491.
12. Bissonnette R, Harel F, Krueger JG, et al. TNF-α An-
progressively discovering that the vasculature is playing
tagonist and Vascular Inflammation in Patients with Pso-
a pivotal role in the different patterns that we may detect
riasis Vulgaris: A Randomized Placebo-Controlled Study. J
with imaging. Invest Dermatol 2017;137:1638-1645.
For this reason, in the next future, we should consider 13. Karbach S, Croxford AL, Oelze M, et al. Interleukin 17
that targeted therapies should also strike the endothelial drives vascular inflammation, endothelial dysfunction, and
dysfunction and angiogenic factors that are novel addi- arterial hypertension in psoriasis-like skin disease. Arterio-
tional players in the generation of dactilytis in PsA pa- scler Thromb Vasc Biol 2014;34:2658-2668.
tients. 14. Mohd Noor AA, Azlan M, Mohd Redzwan N. Orchestrat-
ed Cytokines Mediated by Biologics in Psoriasis and Its
References Mechanisms of Action. Biomedicines 2022;10:498.
15. Silvagni E, Missiroli S, Perrone M, et al. From Bed to
1. Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Bench and Back: TNF-α, IL-23/IL-17A, and JAK-Depend-
Mielants H. Classification criteria for psoriatic arthritis: de- ent Inflammation in the Pathogenesis of Psoriatic Synovitis.
velopment of new criteria from a large international study. Front Pharmacol 2021;12:672515.
Arthritis Rheum 2006;54:2665–2673. 16. Yamamoto T. Angiogenic and inflammatory properties of
2. Brockbank JE, Stein M, Schentag CT, Gladman DD. Dac- psoriatic arthritis. ISRN Dermatol 2013 30;2013:630620.
tylitis in psoriatic arthritis: a marker for disease severity? 17. Varricchi G, Granata F, Loffredo S, Genovese A, Marone G.
Ann Rheum Dis 2005;64:188–190. Angiogenesis and lymphangiogenesis in inflammatory skin
3. Tan AL, Fukuba E, Halliday NA, Tanner SF, Emery P, McG- disorders. J Am Acad Dermatol 2015;73:144-153.
onagle D. High-resolution MRI assessment of dactylitis in 18. Naredo E, Largo R, Olivas-Vergara O, et al. What happens
psoriatic arthritis shows flexor tendon pulley and sheath- under the flexor tendons of the fingers in dactylitis? Med
related enthesitis. Ann Rheum Dis 2015;74:185–189. Ultrason 2023;25:42-47.
4. Felbo SK, Østergaard M, Sørensen IJ, Terslev L. Which ul- 19. Baksa G, Czeibert K, Sharp V, et al. Vascular supply of the
trasound lesions contribute to dactylitis in psoriatic arthritis metacarpophalangeal joint. Front. Med 2022;9:1015895.
Original papers Med Ultrason 2023, Vol. 25, no. 1, 7-13
DOI: 10.11152/mu-3815

Diagnostic performance of a novel ultrasound-based quantitative


method to assess liver steatosis in histologically identified
nonalcoholic fatty liver disease
Kyung A Kang*1, Sung Ryol Lee*2, Dae Won Jun3, In-Gu Do4, Mi Sung Kim5
* the authors share the first authorship

1Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 2Department

of Surgery, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, 3Department of Internal
Medicine, Hanyang University College of Medicine, 4Department of Pathology, Kangbuk Samsung Hospital,
Sungkyunkwan University School of Medicine, 5Department of Radiology, Kangbuk Samsung Hospital, Sungkyunk-
wan University School of Medicine, Seoul, Korea

Abstract
Aims: To investigate the diagnostic performance of ultrasound-guided attenuation parameter (UGAP) for the detection
of hepatic steatosis in nonalcoholic fatty liver disease (NAFLD) cohorts using histopathology as the reference standard and
comparing it with that of various imaging modalities. Materials and methods: A total of 87 subjects who underwent UGAP,
controlled attenuation parameter (CAP), and magnetic resonance imaging-based proton density fat fraction (MRI-PDFF) be-
tween December, 2020 and January, 2022 were enrolled. Of these patients, 38 patients had NAFLD. The association between
UGAP and clinical and imaging parameters was assessed using Pearson’s or Spearman’s correlations. The area under the
receiver operating characteristic curve (AUROC) was used to evaluate the diagnostic performance. Results: The UGAP and
MRI-logPDFF demonstrated strong positive correlations (correlation coefficient= 0.704, P <0.0001). UGAP showed excellent
diagnostic performance for distinguishing steatosis grade ≥1 with an AUROC of 0.821 (95% confidence interval [CI], 0.729–­
0.913), which was comparable to that of MRI-PDFF (0.829, 95%CI, 0.723–0.936). The AUROCs of BUSG (B-mode ultra-
sonography) (0.766, 95% CI, 0.767–0.856) and CAP (0.788, 95% CI, 0.684–0.891) were slightly lower than those of UGAP.
The AUROCs of UGAP, MRI-PDFF, CAP, and BUSG for detecting steatosis grade ≥2 were 0.796 (95% CI, 0.616–0.975),
0.971 (95% CI, 0.936–1.000), 0.726 (95% CI, 0.561–0.891) and 0.774 (95% CI, 0.612–0.936), respectively. Conclusion:
UGAP may be a valuable potential screening tool as a first-line assessment of liver steatosis in patients with NAFLD.
Keywords: ultrasound-guided attenuation parameter; pathology; magnetic resonance imaging; non-alcoholic fatty liver
disease; prospective studies

Introduction of obesity, diabetes, and metabolic syndrome worldwide


[1]. Although liver fibrosis is a key driver of morbidity
The prevalence of non-alcoholic fatty liver disease and mortality in chronic liver disease, early detection and
(NAFLD) has been increasing along with increasing rates monitoring of simple steatosis are also important because
identifying fatty liver is the first step in the screening of
Received 12.07.2022 Accepted 20.11.2022 hepatic fibrosis in the general population. Furthermore,
Med Ultrason it has been reported that coexistence of steatosis acceler-
2023, Vol. 25, No 1, 7-13
Corresponding author: Mi Sung Kim, MD
ates the disease progression to hepatic fibrosis [2,3].
Department of Radiology, Kangbuk Samsung Various imaging techniques have been developed
Hospital, Sungkyunkwan University School for NAFLD diagnosis. In routine clinical practice, ul-
of Medicine, 29 Saemunan-ro, Jongno-gu, trasound (US) is the most commonly used tool for the
Seoul 03181, Korea
Phone/fax: +82-2-2001-1031
evaluation of fatty liver, owing to its easy accessibility
+82-2-2001-1030 and cost-effectiveness. However, there are several obsta-
E-mail: misung70@gmail.com cles to conventional B-mode US; for example, the results
8 Kyung A Kang, Sung Ryol Lee et al Nonalcoholic fatty liver, a novel US-based quantitative method to assess liver steatosis

are highly operator dependent and subjective. Moreover,


it performs poorly in cases of mild steatosis [4].
Several US-based methods have been proposed for
quantitative assessment of steatosis. The controlled at-
tenuation parameter (CAP) using transient elastography
is one of the techniques that enables the quantification
of liver fat. However, it can only be performed in the A-
mode using a dedicated probe without visual guidance.
Recently, a new method for attenuation coefficient
measurements using an US-guided attenuation parameter
(UGAP) was introduced to quantify hepatic steatosis. For
this technique to be widely used as a screening tool for
fatty liver, validation studies using gold standard meth-
ods must precede it. Thus far, there have been limited
validation studies on UGAP, including the heterogeneous
etiology of chronic liver disease [5-9]. The usefulness of
the UGAP in specific population groups, particularly in
patients with NAFLD, has not yet been fully established. Fig 1. Study participant flow.
Validation studies in patients with NAFLD using liver
biopsy as the reference standard are difficult to establish, and alanine aminotransferase five times the upper limit
because liver biopsies in asymptomatic patients with of normal (ULN), total bilirubin three times the ULN, or
NAFLD are rarely available. platelet counts <50×103/mm3; 3) alcohol intake of 210 g/
This study aimed to investigate the diagnostic per- week for men and 140 g/week for women [11]; 4) posi-
formance of UGAP in the diagnosis of hepatic steatosis tive serologic markers for hepatitis B or C; and 5) past
in a cohort of adults with biopsy-confirmed NAFLD. In or current use of medications associated with NAFLD,
addition, magnetic resonance imaging-based proton den- such as valproate, amiodarone, methotrexate, tamoxifen
sity fat fraction (MRI-PDFF) has emerged as a leading or corticosterodis. After applying the exclusion criteria,
quantitative imaging method for the assessment of stea- liver biopsy was performed during cholecystectomy in
tosis. Hence, the diagnostic performance of UGAP was all the patients enrolled in the study. The study protocol
compared with that of MRI-PDFF, using histopathology was approved by the institutional review board of each
as the reference standard. hospital.
The study population comprised 92 consecutive pa-
Materials and methods tients who underwent UGAP, CAP, and MRI-PDFF at
Kangbuk Samsung Hospital from December 2020 to Jan-
Study population and design uary 2022. This study was approved by the institutional
The study population was obtained from a cohort of review board, and all participants signed an informed
patients prospectively collected from two different hos- consent form. Of these patients, five were excluded be-
pitals in Korea. This cohort study was conducted among cause of incomplete self-administered questionnaires
adults aged ≥20 years, who underwent cholecystectomy about alcohol consumption (n=2) or incomplete clinical
for benign gall bladder disease. Most of these cases in- data (n=3). Ultimately, 87 patients were enrolled in this
volved patients with cholecystitis. This prospective study study (fig 1).
aimed to investigate the association between NAFLD US examination
and bile acid alterations in the general population. The All US examinations were performed 1 or 2 days
diagnosis of NAFLD was based on the detection of he- before surgery using the LOGIQ E10 US machine (GE
patic steatosis by histology together with the absence Healthcare, Wauwatosa, WI, USA), which was equipped
of the secondary causes of hepatic steatosis. To exclude with UGAP. Two experienced abdominal radiologists
other identifiable cases of secondary hepatic steatosis and with 20 and 7 years of post-fellowship experience per-
minimize the effect of cholecystitis on hepatotoxicity, we formed the examinations using a C1-6 convex array
excluded participants with the following criteria: 1) mod- probe. All measurements were performed after at least 4
erate-to-severe acute cholecystitis according to the Tokyo hours of fasting.
guidelines 2018 (grade II or III) [10]; 2) significant bio- Before the UGAP measurements, qualitative scoring
marker abnormalities, defined as aspartate transaminase of fatty liver was performed using B-mode ultrasonogra-
Med Ultrason 2023; 25(1): 7-13 9
phy (BUSG) based on known standard criteria [12]. Fatty sue slides. The severity of steatosis was assessed using
liver degree was scored as follows: 1) mild steatosis, dif- a 4-point scale based on the percentage of hepatocytes
fuse increase of liver parenchymal echoes compared with with macrovesicular steatosis: 0 (<5%), 1 (5–33%), 2
the kidney; 2) moderate steatosis, impaired visualization (33–66%), and 3 (>66%) [16].
of wall echogenicity of the main portal vein; and 3) se- Statistical analysis
vere steatosis, blurring of the diaphragm. All statistical analyses were conducted using R soft-
For the UGAP measurements, a single fixed-size ware (v.4.0.4). Continuous variables were expressed as
region of interest (ROI) was placed on the right liver, a mean ± standard deviation or median (IQR) according
avoiding large vascular structures, with a fixed depth of to the data distribution. Categorical variables were ex-
4–8 cm using an intercostal scan. A quality map was used pressed as frequencies (percentages). The significance
to obtain high-quality signals. The UGAP measurements between the two groups (NAFLD vs. non-NAFLD) was
were considered reliable when at least 10 valid measure- assessed using the two-sample t-test or Wilcoxon rank-
ments had an interquartile range (IQR)/median lower sum test for continuous variables, and chi-squared test or
than 30%. The success rate of obtaining reliable meas- Fisher’s exact test for categorical variables. The associa-
urements using UGAP was 100%, irrespective of body tion between UGAP and clinical and imaging parameters
mass index (BMI). was assessed using Pearson’s or Spearman’s correlation
CAP measurements according to normal distribution. A correlation coeffi-
Immediately after the UGAP measurements, CAP cient () below 0.2 was considered to be minimal (<0.2),
measurements were performed using intercostal scan 0.2–0.4, weak; 0.4–0.7, moderate; and >0.7, strong [17].
of the right liver using FibroScan502 (Echosens, Paris, We also used one-way ANOVA to compare the UGAP
France) and M probe (3.5 MHz). Because the reliability values for the different steatosis grades. For pair-wise
criteria for CAP measurements are not yet well-defined, comparisons, post-hoc analysis with Bonferroni correc-
CAP measurements with 10 successful acquisitions were tion was used after ANOVA. We set optimal cut-off val-
considered reliable [13,14]. Of the 87 patients, 5 were ues where the sum of the sensitivity and specificity was
excluded from the evaluation of diagnostic performance maximized for the diagnosis of NAFLD. We compared
because of failed measurements with the M probe. the sensitivity, specificity, positive predictive value, and
MRI-PDFF negative predictive value between the imaging modali-
Preoperative magnetic resonance cholangiopancrea- ties using cut-offs obtained from the receiver operating
tography (MRCP) was performed to detect unexpected curves. Statistical significance was set at p<0.05.
common bile duct stones in 77 patients using 3 T MRI
(Ingenia CX, Philips Healthcare, Best, Netherlands). Results
The mean interval between operation and MRCP was
7.6±27.3 days. The MRCP examination included in- and Baseline characteristics
opposed phases and T2* maps (mDIXON Quant) to ob- The characteristics of the 87 participants according
tain the PDFF maps with the following parameters: TR/ to the presence of NAFLD are summarized in Table I.
TE = 5.7/0.9–4.8 ms; FOV = 40 cm; flip angle = 3°; Of the 38 patients with NAFLD, 28, 8, and 2 had histo-
phase FOV = 0.8; matrix = 160×133; slice thickness logical steatosis grades 1, 2, and 3, respectively. Patients
= 5 mm; acquisition time = 15 s; bandwidth = 252.02 with NAFLD had a higher BMI, waist circumference,
kHz. Images were processed using an interactive post- and liver enzyme levels. The mean and median values of
processing platform (Intelli-space Portal, ISP) provided CAP, UGAP, and MRI-PDFF were significantly higher
by the manufacturer. Semi-automatic segmentation of in the NAFLD group than in the non-NAFLD group (all
the whole liver was performed, and the hepatic fat frac- p<0.0001). The mean UGAP values for the non-NAFLD
tion was automatically calculated. A hepatic fat frac- and NAFLD group were 0.57 ± 0.08 dB/cm/MHz and
tion of less than 5% was considered normal. The cut-off 0.68 ± 0.09 dB/cm/MHz, respectively. The median MRI-
values for the diagnosis of mild, moderate, and severe PDFF values for the non-NAFLD and NAFLD groups
steatosis were 5.2%, 11.3%, and 17.1%, respectively were 4.1% (IQR, 2.9–4.8%) and 8.8% (IQR, 5.0–11.1%),
[15]. respectively. Of the 38 patients with NAFLD, 8, 28, 1, 1
Liver biopsy and histopathologic examination had histological fibrosis grades 0, 1, 2, and 3, respective-
Liver biopsies of segment IV of the gallbladder fossa ly. The mean values of UGAP were 0.64±0.54 dB/cm/
were performed using laparoscopic scissors. The incised MHz and 0.69±0.98 dB/cm/MHz for fibrosis grade 0 and
liver surface was then coagulated using a monopolar 1. UGAP values were 0.72 dB/cm/MHz and 0.79 dB/cm/
device. A single expert pathologist reviewed the tis- MHz for grade 2 and 3.
10 Kyung A Kang, Sung Ryol Lee et al Nonalcoholic fatty liver, a novel US-based quantitative method to assess liver steatosis
Table I. Baseline characteristics
Characteristics Non-NAFLD N= 49 NAFLD N= 38 P-value
Age (years) 44.73 ± 9.98 49.11 ± 12.01 0.0745
Males, n (%) 21 (42.86) 19 (50) 0.6555
Body mass index (kg/m2) 22.21 (20.08, 24.69) 25.33 (23.59, 27.32) <0.0001
Waist circumference (cm) 79 (73.5, 86) 88 (84, 92.75) <0.0001
Diabetes, n (%) 3 (6.12) 4 (10.53) 0.6941
Hypertension, n (%) 2 (4.08) 7 (18.42) 0.0379
Metabolic syndrome, n (%) 3 (6.12) 12 (31.58) 0.0046
Platelet (109/L) 237 (210, 279) 242.5 (223, 274.75) 0.7192
AST (U/L) 17 (14, 21) 19.5 (17, 26.75) 0.003
ALT (U/L) 14 (11, 17) 22 (18, 26.75) <0.0001
GGT (U/L) 22 (13, 30) 27 (20, 51.75) 0.0028
TG (mg/dL) 89 (70, 127) 137.5 (106, 200) <0.0001
HDL-C (mg/dL) 59 (48, 68) 52.5 (49.25, 62) 0.3397
LDL-C (mg/dL) 115.47 ± 31.19 119.55 ± 30.47 0.5412
Fasting glucose (mg/dL) 93 (88, 103) 93 (86.25, 103.75) 0.9181
HbA1c (mmol/L) 5.5 (5.2, 5.7) 5.5 (5.3, 5.8) 0.1314
Insulin (IU/mL) 5.72 (4.01, 9.41) 8.67 (7.06, 14.54) <0.0001
Total bilirubin (mg/dL) 0.59 (0.47, 0.73) 0.54 (0.46, 0.66) 0.5264
CAP (dB/m)* 211 (193, 241) 264 (244, 289) <0.0001
UGAP (dB/cm/MHz) 0.57 ± 0.08 0.68 ± 0.09 <0.0001
UGAP (dB/m) 200.55±27.28 238.76±32.12 <0.0001
MRI-PDFF (%)† 4.05 (2.88, 4.77) 8.80 (5, 11.05) <0.0001
NAFLD = nonalcoholic fatty liver disease; AST = aspartate transaminase; ALT = alanine transaminase; GGT = gamma-glutamyl-transferase;
TG = triglyceride; HDL-C = high-density lipoprotein cholesterol; LDL-C = low-density lipoprotein cholesterol; HbA1c = hemoglobin A1c;
CAP = controlled attenuation parameter; UGAP = ultrasound-guided attenuation parameter; MRI = magnetic resonance imaging; PDFF=
proton density fat fraction. * Data on 82 patients; † Data on 77 patients

Correlation between UGAP and clinical and


imaging parameters
Table II shows the correlation between UGAP and
clinical and imaging parameters. The MRI-PDFF values
were log-transformed because the data showed a skewed
distribution. There was a strong positive relationship be-
tween UGAP and MRI-logPDFF (r=0.704, p<0.0001)
(fig 2). CAP values were positively associated with
UGAP values (r=0.623, p<0.0001). There was no sig-
nificant association between liver stiffness measurements
by transient elastography and UGAP values (r=0.013,
p=0.91).
Correlation between UGAP and steatosis grade Fig 2. Scatterplot for linearity between UGAP and MRI-log-
Figure 3 shows the step-wise increase in UGAP PDFF.
values corresponding with the severity of steatosis
(p<0.0001). The mean UGAP values were 0.57, 0.67, Diagnostic performance of UGAP
0.69, and 0.84 dB/cm/MHz for steatosis grades 0, 1, 2, Table III summarizes the results of the comparison
and 3, respectively. In pair-wise comparisons, there were of diagnostic performance between the imaging modali-
significant differences between subjects with S0 versus ties. The areas under the receiver operating curves (AU-
S1 (p<0.0001), S0 versus S2 (p=0.002), S0 versus S3 ROCs) for the diagnosis of fatty liver were 0.821 (95%
(p<0.0001), and S1 versus S3 (p=0.033). confidence interval [CI], 0.729–0.913), 0.829 (95% CI,
Med Ultrason 2023; 25(1): 7-13 11
Table II. Association between UGAP and clinical and imaging
parameters
Characteristics Correlation p-value
coefficient (r)
Age 0.223 0.0375
Body mass index 0.501 <0.0001
AST 0.256 0.0168
ALT 0.310 0.0035
GGT 0.149 0.1686
Fasting glucose -0.095 0.3828
HbA1c 0.184 0.0882
Insulin 0.373 0.0004
Fig 3. UGAP values according to the steatosis grade.
Total bilirubin (mg/dL) -0.064 0.5548
0.723–0.936), 0.788 (95% CI, 0.684–0.891), and 0.766 CAP (dB/m)* 0.623 <0.0001
(95% CI, 0.767–0.856) for UGAP, MRI-PDFF, CAP, and Transient elastography 0.013 0.9051
BUSG respectively. The best cut-off value of UGAP for MRI-PDFF (%)† 0.660 <0.0001
diagnosing fatty liver was 0.59 (dB/cm/MHz) according MRI-PDFF (%) in log scale† 0.704 <0.0001
to Youden index. The accuracy of UGAP was compara- AST = aspartate transaminase; ALT = alanine transaminase; GGT =
ble to that of MRI-PDFF (75.9% vs. 76.8%); however, gamma-glutamyl transferase; HbA1c, hemoglobin A1c; CAP, con-
trolled attenuation parameter; MRI, magnetic resonance imaging;
the sensitivity of UGAP was superior to that of MRI- PDFF, proton density fat fraction. * Data on 82 patients; † Data on
PDFF (86.8% vs. 71.0%). For the diagnosis of grade ≥2, 77 patients
the AUROCs were 0.796 (95% CI, 0.616–0.975), 0.971
(95% CI, 0.936–1.000), 0.726 (95% CI, 0.561–0.891), to define an optimal cut-off for the diagnosis of fatty liver
and 0.774 (95% CI, 0.612–0.936) for UGAP, MRI-PDFF, (Youden index), substantial discrepancies were found
CAP, and BUSG, respectively. The numbers of correctly with a cut-off of 0.53–0.69. Several covariates, such as
diagnosed patients with histologic steatosis grade ≥2 etiology, BMI, and age, may have contributed to these
were 8 of 10, 9 of 10, 6 of 10, and 6 of 10 when using differences. In a previous study of 163 patients with
UGAP, MRI-PDFF, and CAP, respectively. two different etiologies (hepatitis C virus infection and
NAFLD), patient characteristics were significantly dif-
Discussion ferent between the two groups [6]. This finding supports
the notion that UGAP values are influenced by etiology.
Our study demonstrated a high diagnostic yield of Therefore, the study of specific populations is essential to
UGAP for detecting fatty liver in patients with NAFLD establish optimal cut-off values that appear to be specific
using histopathology as the gold standard. The AUROC for individual etiologies. Previous studies have investi-
for hepatic steatosis grade ≥1 was higher for UGAP for gated the accuracy of UGAP including the heterogene-
BUSG, which is the most widely used in routine clinical ous etiology of chronic liver disease. The strength of this
practice for the detection of fatty liver (0.821 vs. 0.766). study was that the data were gathered from patients in
Additionally, the AUROC of UGAP was similar to that the pure NAFLD group. In this study, the optimal cut-off
of MRI-PDFF (0.821 vs. 0.829), and UGAP showed su- value of UGAP for the detection of fatty liver in patients
perior sensitivity and similar accuracy than it did in MRI- with NAFLD was 0.59 (dB/cm/MHz). Imajo K et al [7]
PDFF (sensitivity, 86.8% vs. 71.0%; accuracy, 75.9% have proposed an optimal cut-off of UGAP for the diag-
versus 76.8%). UGAP not only had a high diagnostic nosis of NAFLD grade 1 of 0.69 dB/cm/MHz in the sub-
performance, similar to that of MRI-PDFF for the diag- group analysis. The difference between the cut-off values
nosis of steatosis, but also had the advantages of conven- can be attributed to demographic differences in the en-
tional US in terms of easy accessibility and cost-saving. rolled populations. Here, we recruited participants with
Ultimately, UGAP is expected to be a valuable screening average-to-low risk of NAFLD; however, they enrolled
tool for first-line assessment of steatosis in patients with patients with chronic liver disease. Also, the difference
NAFLD. between the cut-off values may be the result of the small
Overall, these findings are in accordance with find- number of NAFLD patients with unbalanced steatosis
ings reported by previous studies with AUROCs of 0.83– distribution in this study. The majority of NAFLD pa-
0.92 [5-8]. However, even when using the same method tients were steatosis grade 1 (74%, 28/38) and only 10
12 Kyung A Kang, Sung Ryol Lee et al Nonalcoholic fatty liver, a novel US-based quantitative method to assess liver steatosis
Table III. Diagnostic performance of imaging modalities for the diagnosis and grading of NAFLD
Modalities Cut-off AUROC (95% CI) Accuracy Sensitivity Specificity PPV NPV
(%) (%) (%) (%) (%)
≥S1 UGAP 0.59 (206.5)* 0.821 (0.729-0.913) 75.9 86.8 67.4 67.4 86.8
MRI-PDFF† 5.70 0.829 (0.723-0.936) 83.1 71.0 91.3 84.6 82.4
CAP‡ 243.0 0.788 (0.684-0.891) 76.8 75.7 77.8 73.7 79.6
BUSG NA 0.766 (0.767-0.856) 81.6 81.3 83.6 78.9 83.7
≥S2 UGAP 0.69 (241.5)* 0.796 (0.616-0.975) 83.9 80.0 84.4 40.0 97.0
MRI-PDFF† 9.25 0.971 (0.936-1.000) 93.5 100.0 92.7 64.3 100.0
CAP‡ 285.5 0.726 (0.561-0.891) 81.7 60.0 84.7 35.3 93.9
BUSG NA 0.774 (0.612-0.936) 90.8 60.0 94.8 60.0 94.8
NAFLD = nonalcoholic fatty liver disease; UGAP = ultrasound-guided attenuation parameter; MRI = magnetic resonance imaging; PDFF=
proton density fat fraction; CAP = controlled attenuation parameter; BUSG = B-mode ultrasonography; NA = Not applicable. *The numbers
in parentheses indicate values of UGAP measurements in dB/m. †Data on 77 patients; ‡Data on 82 patients.

patients were steatosis grade 2 or higher (26%, 10/38). In conclusion, UGAP may be considered a promising
Finding robust estimates for cutoff values require con- screening tool for first-line assessment of liver steatosis
siderable sample size. However, our sample size was too in patients with NAFLD.
low to optimize cutoff values.
Previous studies have shown a very high accuracy of Conflict of interest: none
UGAP in differentiating all steatosis grades. The overall
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Original papers Med Ultrason 2023, Vol. 25, no. 1, 14-21
DOI: 10.11152/mu-3774

Percutaneous transhepatic ultrasound-guided gallbladder aspiration:


Still a safe option for gallbladder decompression in patients at high
surgical risk
Kilian Bock, Benjamin Heidrich, Steffen Zender, Heiner Wedemeyer, Andrej Potthoff*,
Henrike Lenzen*
* both authors contributed equally to this work

Dept. of Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Carl-Neuberg-Str.1,


30625 Hannover, Germany

Abstract
Aims: Cholecystitis generally warrants immediate cholecystectomy; however, high-risk patients require non-surgical op-
tions for gallbladder decompression. The continuous evolution of endoscopic techniques makes it difficult for clinicians to
choose the best technique for high-risk patients. Here we aimed to show that percutaneous transhepatic gallbladder aspiration,
a technique that has fallen into disuse, is a safe and rapid method for gallbladder decompression. Materials and methods:
In our local database, we identified 48 patients who had undergone transhepatic punctures of the biliary system,34 of whom
were excluded because they had received bile duct punctures. The remaining 14 patients had received gallbladder punctures,
of whom 9 were considered eligible for analysis. Cases were retrospectively analyzed for technical success, complications,
and individual outcomes. Results: Our analysis included 9 patients (3 female, 6 male; median age, 51 years; range, 32-84
years). Underlying malignancy was found in 5 patients, while 4 were in a palliative situation. Underlying infection was found
in 8 cases. All punctures were technically successful without complications. In all patients, individual therapy goals were
met,including clinical stabilization in palliative situations, stabilization before liver surgery, exclusion of gallbladder empyema
and infection in gallbladder hydrops, and avoidance of gallbladder rupture. The white blood cell counts at the day of punction
were significantly reduced one week after the puncture (p=0.023). Conclusions: When selecting an appropriate technique for
high-risk patients, clinicians should remember that gallbladder aspiration is a feasible and successful bedside procedure in
patients at high surgical risk, which does not require an experienced endoscopist.
Keywords: gallbladder; decompression; interventional ultrasonography; puncture; aspiration

Introduction higher in patients with significant comorbidities [3-5]. In


high-risk patients, an alternative to surgical gallbladder
For patients with acute cholecystitis, current guide- removal is a timely decompression, especially in gall-
lines recommend laparoscopy within 24-72 h [1,2]. bladder hydrops. Minimally invasive decompression can
Although open and laparoscopic cholecystectomy are be performed as a temporary measure or as definitive
generally considered safe surgeries, the mortality rate is treatment [6-8].
Several gallbladder drainage techniques are available.
The oldest procedure is percutaneous cholecystostomy,
Received 01.06.2022 Accepted 04.01.2023 which involves ultrasound-guided percutaneous tran-
Med Ultrason
2023, Vol. 25, No 1, 14-21
shepatic gallbladder aspiration (PTGBA) or gallbladder
Corresponding author: Prof. Dr. Andrej Potthoff, MD drainage (PTGBD). Tokyo guidelines recommend PT-
Dept. of Gastroenterology, Hepatology and GBD as standard procedure for patients with acute chol-
Endocrinology, Hannover Medical School, ecystitis who are at high risk for perioperative morbidity
Carl-Neuberg-Str.1,
30625 Hannover, Germany
and mortality. Compared to aspiration, drainage therapy
Phone: +49 511 532 3415 can more effectively mobilize thick exudate [9]. An in-
E-mail: potthoff.andrej@mh-hannover.de ternational multicenter study showed that the 3-day clini-
Med Ultrason 2023; 25(1): 14-21 15
cal success rate was significantly higher after PTGBA
than after PTGBD and endoscopic gallbladder stenting
(EGBS), although the 7-day clinical success rates did not
significantly differ [10]. Cholecystostomy has a techni-
cal success rate of 98.5-100% [11]. The choice of access
route (direct gallbladder puncture or transhepatic access)
is not associated with significantly different complication
rates [12].
Newer procedures include endoscopic transpapillary
gallbladder drainage (ETGBD) and endoscopic ultra-
sound-guided gallbladder drainage (EUSGBD). ETGBD
is safe and effective [13,14], and is associated with less
pain and better objective treatment response than PT-
GBD [15]. However, it is also technically challenging,
associated with an increased risk of pancreatitis, and
may fail when cystic duct obstruction (by stones or in-
flammation) prevents selective cannulation of the cystic
duct. EUSGBD has become popular in recent years be-
cause it improves patients’ quality of life through internal
drainage, and reduces the risks of repeated hospitaliza-
tions and necessary re-interventions [16]. Endoscopic
ultrasound-guided puncture is usually performed via the
duodenum or stomach [9,17,18]. Drainage can be pro-
Fig 1. Screening for the study population
vided using various stents, e.g., self-expendable metal
stents (SEMS), double-pigtail stents, lumen-apposing shepatic punctures of the biliary system between 2000-
metal stents (LAMS), or electrocautery-enhanced LAMS 2019. Of these patients, 34 were excluded because they
[9,17,18]. had undergone ultrasound-guided bile duct punctures.
EUSGBD and PTGBD show comparable technical The remaining 14 cases were classified as gallbladder
(97% vs. 97%) and clinical (100% vs. 96%) success rates punctures. The inclusion criteria were: age>18 years,
[19]. Teoh et al report that compared with PTGBD, EUS- high risk for surgery according to a multidisciplinary
GBD was associated with significantly lower 1-year rates team, and symptomatic gallbladder disease. Exclusion
of adverse events (32.2% vs. 74.6%, p<0.001) and re- criteria were age<18 years, punctures performed for his-
admission for re-intervention (6.8% vs. 71.2%, p<0.001) tological reasons (e.g., tumor biopsies), and lack of medi-
[20]. Most adverse events in the PTGBD group were due cal reports.
to tube-related problems, including leaks, obstructions, Among the 14 patients, 2 were excluded because
or infections. Clinicians must choose among these con- medical records were unavailable, and 3 were excluded
stantly evolving endoscopic options to select an appro- for not meeting the criteria for gallbladder aspiration (1
priate individual treatment plan, considering technical underwent puncture of a large gallbladder carcinoma,
requirements and costs, patient factors, and the expertise 1 underwent puncture of an adenomyomatosis, and 1
of the treating physician. underwent puncture of a cystic formation near the gall-
In this article, we report the technical and clinical bladder). The remaining 9 patients were considered as
success of PTGBA among nine patients who were not the study population. Figure 1 presents the screening
candidates for surgical therapy. We aimed to demonstrate procedure. The included patients’ medical records were
that this procedure can be considered for patients with retrospectively analyzed. This study was performed in
different clinical backgrounds, particularly when an ex- compliance with the local data protection regulations,
perienced endoscopist is not available. and our local ethics committee regulations. According to
our local institution’s guidelines, retrospective studies do
Materials and methods not require ethics committee approval.
For ultrasound evaluation of the gallbladder wall,
Study population and data collection all patients fasted for >4 hours. Acute cholecystitis was
We searched our local medical database, and identi- diagnosed using the following ultrasound criteria [21-
fied 48 patients who had undergone percutaneous tran- 25]: no movement of impacted echogenic gallstones,
16 Kilian Bock et al Percutaneous transhepatic US-guided gb aspiration: Still a safe option for gb decompression

Fig 2. Percutaneous transhepatic gallbladder aspiration: a) Insertion of the needle into the gallbladder lumen (arrow); b) Aspiration
and Flushing of the Gallbladder with 0.9% NaCl (sodium chloride); c) Removal of the needle, air along the Gallbladder wall (arrow).
Doppler function was used to exclude significant bleeding.

sonographic Murphy sign, gallbladder wall thickening tion, the needle was introduced with its tip positioned
(>4.5 mm), echolayering of the gallbladder wall (alter- within the gallbladder lumen. Diagnostic aspiration of a
nating hypoechoic and hyperechoic layer with prominent small amount of fluid was performed to obtain samples
specular mucosal lining), and pericholecystic fluid. Pa- for microbiology analysis and culture. Gallbladder fluid
tients were examined for gallbladder hydrops by apply- was evacuated, and the gallbladder was rinsed with 0.9%
ing graduated pressure on the gallbladder, and considered NaCl. The examiner decided whether to administer an-
positive if the gallbladder maintained its round contour tibiotic injection, depending on macroscopic aspects of
during compression [26]. Additional criteria included the bile and clinical necessity. The decision concerning
transverse width >4 cm, longitudinal length >9 cm, and injected antibiotics was made following previous anti-
straight or convex borders. biograms (fig 2).
The nine cases were analyzed for technical success, Statistical analysis
complications, and patient outcome. Technical success All statistical analyses were performed using SPSS
was assumed when the needle could be visualized in the Statistics 26 (IBM Corp, Armonk, NY). Laboratory re-
gallbladder and fluid was evacuated. Medical reports sults on the day of punction were compared with the re-
were analyzed for major complications associated with sults one week after the first punction. Statistical signifi-
gallbladder aspiration, such as increased pain, rupture, cance was evaluated using a two-sided exact Wilcoxon
hemodynamic instability, or bleeding. Patient outcome test. Cases with no laboratory data after one week were
was analyzed in terms of the achievement of various in- excluded from statistical analysis.
dividual goals, such as clinical stabilization, symptom
relief, and infection control in palliative patients, stabi- Results
lization and infection control before liver surgery, exclu-
sion of gallbladder empyema and infection in gallbladder Patient characteristics
hydrops, and prevention of gallbladder rupture. Of the nine included patients, six were male and the
Technical procedure median age was 51 years (range, 32-84 years). No pa-
Percutaneous gallbladder aspiration was performed tient had liver cirrhosis or was liver transplanted. All pa-
by two certified examiners under ultrasound guidance tients were severely pre-diseased, and too high-risk for
(Toshiba Aplio XG; Tokyo, Japan) using a special biopsy cholecystectomy according to multidisciplinary assess-
transducer (Toshiba PLT308P 3.75 MHz), with a 0.9- ment. Five patients had underlying malignant diseases,
mm (20-gauge) or 0.7-mm (22-gauge) needle (Pajunk including cholangiocarcinoma (n=3), stomach cancer
Germany). Only local anesthesia (xylocaine, 1%; Aspen with hepatic metastasis (n=1), and breast cancer with he-
Pharmacare, South Africa) was typically required. Be- patic metastasis (n=1). Four patients were in a palliative
fore puncture, color Doppler assessment was performed situation. Eight patients exhibited underlying infection,
to prevent accidental vascular injury by excluding the including spontaneous bacterial peritonitis (n=1), chole-
presence of any major hepatic or portal vessels within cystitis (n=5), post-ERCP pancreatitis (n=3), cholangitis
the intended route. The drainage route was planned under (n=1), and gallbladder empyema (n=1). Patient charac-
ultrasound guidance. After local anesthesia administra- teristics are described in Table I.
Med Ultrason 2023; 25(1): 14-21 17
Table I. Patients’ baseline characteristics In one patient, PTGBA was performed with the aim of
Characteristics Cohort excluding gallbladder empyema, and to flush the bile
Male gender, n (%) 6 (66.7%) system with antibiotics prior to an ERCP. The individual
goal of puncture was reached in this patient. In one pa-
Age in years, median (range) 51 (32-84)
tient with very high surgical risk and signs of discontinu-
Ascites, n (%) 5 (55.6%)
ity in CEUS, PTGBA was performed with the aim of pre-
ALT, mean 91±58.2 venting gallbladder rupture and promoting stabilization.
INR, mean 1.24±1.2 Aspiration successfully prevented gallbladder rupture,
Jaundice, n (%) 6 (66.7%) and this patient later underwent elective cholecystectomy
Underlying malignant disease, n (%) 5 (55.6%) as recommended by our surgeons.
Underlying infection, n (%) 8 (88.9%) Complications and adverse events
High surgical risk, n (%) 9 (100%) Detailed analysis of all medical data revealed that
no patient experienced complications or adverse events
Quantitative values expressed as mean±SD. Normal range of labo-
ratory values: INR, 0.9-1.25; ALT<34 U/L. ALT: Alanine transami- during their hospital stay. PTGBA was a safe procedure,
nase; INR: International Normalized Ratio even in patients with underlying abdominal infection,
such as spontaneous bacterial peritonitis and ascites. No-
Technical details and success tably, no complication occurred in a patient facing immi-
Every puncture was successful on its first attempt. nent gallbladder rupture, with gangrenous cholecystitis,
Gallbladder hydrops was observed in seven cases, and and proved discontinuity of the gallbladder wall.
cholecystitis in five cases. Six patients could be treated
with a single PTGBA. Three patients required a second Discussion
PTGBA. Concomitant systemic antibiotic therapy was
needed in eight patients. No patient required permanent In most patients, early cholecystectomy is the stand-
drainage. This increases patient comfort, which is espe- ard therapy for gallbladder diseases, such as acute chol-
cially important in a palliative situation. Table II presents ecystitis. However, patients with severe comorbidities,
detailed information about macroscopic aspects of bile, especially advanced palliative patients, face high surgical
microbiological analysis, antibiotic administration, con- risk with an overall high morbidity and mortality. Such
comitant antibiotic therapy, and underlying disease. patients require alternative therapeutic strategies to avoid
Patient outcomes surgical complications and prolonged distress. In this ret-
All patients were alive after treatment, and were suffi- rospective study, we demonstrated that PTGBA is a safe
ciently stabilized for their individual therapy goals. Table and feasible procedure in patients with severe comorbidi-
III presents laboratory value comparisons. ties, such as palliative diseases, tumors, and infection.
Among the four palliative patients, clinical stabili- Our analysis revealed that gallbladder aspiration was
zation, relief of symptoms, and infection control were an appropriate technique not only in cases of proven chol-
achieved in all four. Three palliative patients could be ecystitis in high-risk surgical patients, but also in cases of
discharged after puncture and concomitant systemic gallbladder hydrops requiring puncture to prevent chol-
therapy, and were able to avoid high-risk surgery, which ecystitis development, to prevent rupture, and for pain
can delay systemic tumor therapy and minimize hospital- relief in palliative situations. PTGBA was an adequate
free lifetime due to prolonged recovery time. One pallia- procedure for gallbladder decompression, especially in
tive patient needed repeated PTGBAs because hydrops cases not requiring a long-term strategy—for example, to
was mechanically evoked by metastasis of the underly- allow patients to recover from other underlying diseases
ing tumor. In this case, PTGBA was the only applicable (e.g., post-ERCP pancreatitis), and to prepare patients for
technique for decompression and clinical stabilization, extended liver surgeries. Among patients not eligible for
because massive peritoneal carcinosis prevented chol- surgery, PTGBA can be of additional benefit, because the
ecystectomy, and drainage therapy can lead to patient proof of bacteria with sub-specification can help in the
discomfort. selection of suitable antibiotic therapy. PTGBA should
In the three patients with a disease that might require especially be considered in palliative patients because it
extended liver surgery, such as a suspicious bile duct ste- avoids the discomfort of a permanent drainage, especially
nosis, PTGBA was performed with the aim of stabiliza- when endoscopic drainage approaches are not possible.
tion before liver surgery. All three patients were stabi- Besides PTGBA, other alternative therapeutic strate-
lized with PTGBA and concomitant antibiotic therapy, gies for gallbladder interventions include PTGBD, EUS-
creating a better starting point for potential liver surgery. GBD, and ETGBD, which have mostly been evaluated
18 Kilian Bock et al Percutaneous transhepatic US-guided gb aspiration: Still a safe option for gb decompression
Table II. Characteristics of percutaneous gallbladder aspiration and concomitant therapy
Underlying Gall- Macroscopic Bile Antibiotic Second Concomitant Aim of
disease bladder aspects of microbiology instillation punc- systemic punction
bile tion therapy
CCC, Hydrops Green bile Streptococcus No No Ceftriaxone Clinical
hepatic metastasis, mitis, Enterobacter Metronidazole stabilization
SBP cloacae, Candida (palliative
tropicalis situation)
PSC, jaundice, Hydrops Pus Streptococcus Vancomycin Yes Linezolid Stabilization
suspicious bile duct mitis, ORSA 500 mg, Ciprofloxacin before liver
stenosis, pancreatitis during Metronidazole surgery
2nd punction
Hepatic metastasis, Cholecystitis Clear liquid No bacteria No No Meropenem Clinical
fever Hydrops Vancomycin stabilization
(palliative
situation)
Hepatic metastasis, Hydrops Milky No bacteria No No Piperacillin/ Stabilization
CCC, hydrops, yellow Tazobactam before
necrosing Meropenem liver surgery
pancreatitis Linezolid
PSC, bile duct Hydrops Murky yel- Staphylococcus Gentamycin, Yes Piperacillin/ Stabilization
stenosis, Cholecystitis low aureus during Tazobactam before
cholangitis 2nd punction Metronidazole liver surgery
Levofloxacin
Painless occlusive Hydrops Unknown No bacteria Ampicillin/ No No Exclusion of
jaundice, hydrops, sulbactam gallbladder
large pancreatic 1.5 g empyema
cyst, failure of and infection
previous ERCP
Hepatic metastasis Acalculous Pus No bacteria Tobramycin Yes Levofloxacin Clinical
cholecystitis Murky 40 mg stabilization
yellow (palliative
situation)
Pancreatic mass Cholecystitis Unknown Escherichia coli Ampicillin/ No Piperacillin/ Clinical
highly suspicious of sulbactam Tazobactam stabilization
cancer, post-PTCD 1.5 g Meropenem (palliative
pancreatitis Linezolid situation)
Ampicillin/
Sulbactam
High perioperative Hydrops Tenacious Lactobacillus No No Piperacillin/ Avoidance of
risk and Interruption bloody rhamnosus Tazobactam gallbladder
recommendation for of gall material Metronidazole rupture
antibiotic therapy bladder
continuity.
Gangrenous
Cholecystitis
Abbreviations (table II):CCC:Cholangiocellular Carcinoma, SBP: Spontaneous bacterial peritonitis, ORSA: Oxacillin restistant staphylo-
coccus aureus, PSC: Primary Sclerosing Cholangitis, ERCP: Endoscopic retrograde cholangiopancreatography, PTCD: Percutaneous Tran-
shepatic Cholangial Drainage

for high-risk surgical patients with cholecystitis [9,27]. In a prospective study, Haas et al reported that gall-
PTGBA, as performed in our study, is a simple and low- bladder aspiration was successful in 76% of patients with
cost bedside procedure that does not require X-ray use. acute cholecystitis [28]. Komatsu et al demonstrated that
It can be performed outside of tertiary endoscopic high- 95.6% of their patients with acute cholecystitis recovered
volume centers, can thus be widely used as a method after PTGBA, including those at high risk [29]. Present
of decompression in patients with acute cholecystitis. guidelines do not recommend gallbladder aspiration for
Moreover, it does not have a negative impact on further all acute cholecystitis patients partly because thick dense
surgeries. material cannot be sufficiently aspirated, and therefore
Med Ultrason 2023; 25(1): 14-21 19
Table III. Biochemical characteristics of the patient cohort
Parameter Baseline Follow-up T1 p value
CRP, mg/L 89±87 (2.5-232) 57±64 (1-192) 0.07
WBC, 1000/µL 17±10 (6.7-39) 13±11 (5.4-39.9) 0.023
Creatinine, µmol/L 63±18 (39-34) 86±52 (43-192) 0.523
Bilirubin, µmol/L 102±104 (3-335) 99±75 (30-217) 0.09
GGT, U/L 519±735 (68-2379) 858±926 (35-2463) 0.022
AP, U/L 643±676 (60-2223) 518±419 (119-1047) 0.438
Quantitative variables are expressed as mean±SD (range). Normal range of laboratory values: CRP<5 mg/L; WBC 3.9-10.2 1000/µL;
creatinine 45-84 µmol/L; bilirubin 2-21 µmol/L; GGT<38 U/L; AP 35-104 U/L. CRP:C-reactive protein, WBC: white blood cell count,
GGT: Gamma-Glutamyltransferase, AP: Alkaline Phosphatase

gallbladder aspiration may not be successful in patients severe coagulopathy and thrombocytopenia, in cases
with this presentation [9]. In their study comparing gall- with ascites, or in constellations where the gallbladder is
bladder aspiration and percutaneous cholecystostomy, anatomically difficult to access for percutaneous drain-
Ito et al reported that 18% of attempted gallbladder as- age [32]. Comparison of endoscopic nasogallbladder
pirations failed due to thick material, such as pus, in the drainage (ENGBD) with endoscopic gallbladder stenting
gallbladder [30]. Chopra et al retrospectively analyzed (EGBS) revealed high clinical success rates of 94.1% and
gallbladder aspiration and percutaneous cholecystos- 90.3%, respectively [32]. Nakahara et al. tested a novel
tomy with application of a pigtail catheter in high-risk stent, with a three-dimensional spiral-shaped structure
surgical patients. They reported that clinical outcomes and side holes, for EGBS in patients with acute chol-
did not differ between patients treated with gallbladder ecystitis, and demonstrated high clinical success rates
aspiration versus percutaneous cholecystostomy, and of 100% with the novel stent, and 95.7% for the con-
that the complication rate was significantly lower with trol group with alternative stents [33]. They found that
gallbladder aspiration compared to percutaneous chol- stent migration was significantly higher in the control
ecystostomy [31]. On the other hand, in their prospec- group, especially with straight stents, compared to the
tive study, Ito et al found that compared to gallbladder novel stent group [33]. Interestingly, post-procedure pain
aspiration, percutaneous cholecystostomy with a pigtail ratings are reported to be significantly higher following
catheter had superior clinical effectiveness, without a ENGBD compared to EGBS [32]. However, it has also
higher complication rate, and was therefore considered been reported that abdominal pain is less frequent in
the preferred technique for high-risk surgical patients ENGBD compared to PTGBD [34]. Iino et al compared
[30]. PTBGD and ETGBD (including ENGBD and EGBS),
Itoi et al compared percutaneous gallbladder inter- and found that the success rate was 100% for PTGBD
ventions (PTGBI), including PTGBA and PTGBD, with versus 77% for ETGBD; however, the clinical effective-
ETGBD in high-risk surgical patients [10]. The clinical ness did not significantly differ between the two groups
success rates did not significantly differ between PTGBI [13]. Another interesting finding is that hospitalization
and ETGBD (62.5% and 69.8%, respectively), and PTG- time was significantly shorter in the ETGBD group than
BA had a higher clinical success rate than PTGBD (75% in the PTGBD group [13].
vs. 59.6%) [10]. PTGBA was superior to PTGBD in Since ETGBD involves transpapillary drainage, the
terms of the clinical success rate at 3 days after the inter- complications can include pancreatitis, and clinicians
vention, which may be partly because the PTGBA group should be aware of this problem when using ETGBD for
included patients with less severe cholecystitis based on continuous drainage therapy. Furthermore, cystic duct
the experience of the interventionalist [10]. This finding cannulation, especially in patients with acute cholecys-
reveals the importance of an adequate selection of pa- titis, may be challenging due to the infection and corre-
tients who only require a simple PTGBA versus requiring sponding swelling of the duct itself.
continuous drainage. Patients requiring continuous drainage, who are not
Notably, although Itoi et al reported similar clinical considered eligible for percutaneous drainage or aspira-
success rates for ETGBD and PTGBI, not every patient tion therapy, can also be treated with EUSGBD, which
is eligible for percutaneous drainage and sometimes an is an echoendoscopic technique for continuous gallblad-
endoscopic approach is needed. Advantages of endo- der drainage. Teoh et al compared EUSGBD and PT-
scopic transpapillary access with subsequent drainage GBD, and reported high clinical success rates of 92.3%
include that these techniques can be used in patients with and 92.5%, respectively [17]. Notably, the 1-year rate of
20 Kilian Bock et al Percutaneous transhepatic US-guided gb aspiration: Still a safe option for gb decompression

adverse events was significantly lower in the EUSGBD Conclusions


group than the PTGBD group (p<0.0001) [17]. Lisotti et
al reported an 88% overall clinical success rate for EUS- PTGBA is a safe technique that can be easily per-
GBD, and identified acute kidney injury and severe co- formed for gallbladder interventions, such as for gall-
morbidities as factors predicting long-term mortality in bladder hydrops, cholecystitis, pain relief in a palliative
these patients [18]. In a meta-analysis, Krishnamoorti et situation, or as a bridging strategy for surgery. Especially
al reported that EUSGBD had significantly higher clini- for patients who do not require long-term drainage, PTG-
cal and technical success rates than ETGBD [35]. The BA is a cost-effective and easily performed bedside tech-
authors stated that the increased clinical success rate of nique, which should not be overlooked as an alternative
EUSGBD could be associated with the higher lumen of therapeutic strategy, even in endoscopic high-volume
the SEMS and LAMS, leading to more sufficient drain- centers.
age and allowing stones to pass [35]. Since EUSGBD
with stent placement is considered for patients who are Conflict of interest: none
not eligible for cholecystectomy, EUSGBD may be an
appropriate technique in cases requiring prolonged drain- References
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Original papers Med Ultrason 2023, Vol. 25, no. 1, 22-28
DOI: 10.11152/mu-3841

Can the Vesical Imaging Reporting and Data System (VI-RADS)


score be applied in conventional ultrasound and contrast-enhanced
ultrasound to differentiate muscle-invasive bladder cancer?
Ju Zhu, Xiao Huang, Luping Liu, Nan Wang, Fang Nie

Medical Center of Ultrasound, Lanzhou University Second Hospital, Lanzhou City, Gansu Province, China

Abstract
Aim: To investigate the value of vesical imaging reporting and data system (VI-RADS) score based on conventional ul-
trasound and contrast-enhanced ultrasound (CEUS) in differentiating muscle-invasive bladder cancer (MIBC). Material and
methods: Thirty-eight patients who underwent conventional ultrasound and CEUS examinations at our ultrasound department
between March 2021 and June 2022 were retrospectively included in this study. Two sonographers analyzed the conventional
ultrasound and CEUS images of each patient separately and scored them in strict accordance with VI-RADS scoring system
based on conventional ultrasound and CEUS. The VI-RADS score of each lesion was compared with the pathological findings
to assess the diagnostic performance of VI-RADS. The sensitivity, specificity, positive predictive value, negative predictive
value, and accuracy of the VI-RADS score in the diagnosis of MIBC were analyzed when the cutoff values were 3 and 4,
respectively. Interobserver agreement was evaluated using the weighted-kappa coefficient (κ). Results: The final pathological
results evidenced 25 (65.8%) non-muscle-invasive bladder cancers (NMIBCs) and 13 (34.2%) MIBCs. When the VI-RADS
score ≥ 4, the sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of the VI-RADS score
for predicting muscle-invasive bladder cancer were 92.3%, 84.0%, 75.0%, 95.5%, and 86.8%, respectively. The area under
the receiver operating curve for the VI-RADS score was 0.882 (95%CI:0.761-1). Inter-reader agreement for VI-RADS scores
was good. Conclusion: The VI-RADS score based on conventional ultrasound and CEUS is useful in differentiating muscle-
invasive bladder cancer.
Keywords: Vesical imaging reporting and data system; ultrasound; contrast-enhanced ultrasound; bladder cancer

Introduction [4]. Meanwhile, BC is also the most expensive tumor to


treat and has caused a great burden to society [5].
Bladder cancer (BC) is the tenth most common cancer The bladder wall is divided into three layers: the mu-
worldwide, with approximately 573,000 new cases and cosa (includes urothelium and lamina propria), the mus-
213,000 deaths in 2020: it is four times more common in cularis propria, and the serosa with perivesical fat. The
men than in women [1,2]. The incidence is usually high muscularis propria represents a specific landmark for
in people over 65 years of age [3]. There were 81,400 BC staging [6]. Histopathological muscular invasion is
new cases and 17,980 deaths in the United States in 2020 one of the most important factors affecting the treatment
and prognosis of BC [7]. Non-muscle-invasive bladder
cancers (NMIBCs) are usually based on transurethral
Received 05.08.2022 Accepted 18.12.2022
Med Ultrason
resection of bladder tumors (TURBT), supplemented by
2023, Vol. 25, No 1, 22-28 intravesical chemotherapy or immunotherapy. For mus-
Corresponding author: Fang Nie cle-invasive bladder cancers (MIBCs), treatment meth-
Medical Center of Ultrasound, ods usually include radical cystectomy, adjuvant/neoad-
Lanzhou University Second Hospital,
Lanzhou City, Gansu Province, 730030, China
juvant chemotherapy, radiotherapy, and immunotherapy
Phone: +86 13993163088 [8,9]. Because patients with NMIBC and MIBC require
E-mail: ery_nief@lzu.edu.cn different treatment options, accurate preoperative assess-
Med Ultrason 2023; 25(1): 22-28 23
ment of muscular invasion is essential for the choice of submucosal layer show rapid hyperenhancement, while
treatment modality. the muscularis propria shows slow hypoenhancement. In
At present, accurate staging of BC depends on patho- cases with MIBC, the hypoenhancement layer between
logical staging, but pathologists may make a false-neg- the mucosal and serosal layers will disappear [16]. Tak-
ative diagnosis due to the lack of muscularis propria in ing into consideration the results of the previous studies
the resected specimen or the sample quality has been regarding the application of US and CEUS in BC stag-
affected by the burning of bladder tumor tissue during ing and the application of VI-RADS in multiparametric
TURBT [7,10,11]. Since the introduction of Vesical Im- MRI, we created a VI-RADS scoring system suitable for
aging Reporting and Data System (VI-RADS) as a stand- US and CEUS examinations. The purpose of this study
ard imaging and diagnostic method in 2018 [12], the sys- was to investigate the value of VI-RADS scoring system
tem has been increasingly more widely used. VI-RADS based on US and CEUS in differentiating MIBC.
classifies the probability of muscle invasion suggested by
multiparametric MRI findings into five stages, VI-RADS Materials and methods
1 indicates tumors highly unlikely to invade the muscu-
laris; VI-RADS 2 indicates tumors unlikely to invade the Study design
muscularis; VI-RADS 3 indicates the presence of mus- Owing to the study being retrospective, the require-
cle invasion is equivocal; VI-RADS 4 indicates muscle ment for informed consent was waived by the Ethics
invasion is likely; VI-RADS 5 indicates that invasion Committee of Lanzhou University Second Hospital. In-
of the muscle and beyond the bladder is very likely [10, formed consent was obtained from all patients prior to
13]. However, the application of MRI in bladder cancer CEUS examination. The area under the receiver operat-
staging is limited due to the high cost, nephrotoxicity of ing characteristic (ROC) curve for CEUS in differentiat-
contrast agents, and possible overstaging in patients with ing MIBC has been reported to be between 0.92 and 0.99.
mucosal edema. The study design for this study is a diagnostic test. As-
Conventional ultrasound (US) is a widely used and suming a 1:1 ratio of NMIBC patients to MIBC patients,
recommended method for assessing hematuria and for the desired area under the ROC curve is at least 0.85, and
tumor staging. The bladder wall appeared homogene- assuming α = 0.05, β = 0.10, at least 11 NMIBC and 11
ously hyperechoic on US, interruption of hyperechoic MIBC patients are required. Assuming a loss to follow-
bladder wall being considered a key feature to differen- up rate of 10%, a total of 24 subjects were required.
tiate NMIBC and MIBC. However, studies using these Patients
criteria have shown that it cannot accurately show the A total of 138 patients who underwent bladder CEUS
depth of local invasion of the tumor [14-16]. In the re- prior surgical treatment in our hospital from March 2021
cent years, with the more and more mature application to June 2022 were included in this study (fig 1). All path-
of contrast-enhanced ultrasound (CEUS), the technique ological specimens were evaluated by 2 senior patholo-
has also been preliminarily applied for staging the BC. gists. Inclusion criteria: 1) complete clinicopathological
In CEUS, the three-layer structure of the bladder wall data; 2) initial diagnosis of BC; 3) patients with BC who
is more clearly visualized, the mucosal and especially have not received other treatment. Exclusion criteria:
1) incomplete clinicopathological data; 2) patients with
previously treated BC; 3) patients with poor image qual-
ity of US and CEUS; 4) patients with hypersensitivity
to contrast agent; 5) patients with severe respiratory and
circulatory failure.
Conventional US and CEUS examination
US was performed using Aplio i800 (Toshiba Medi-
cal Systems, Tokyo, Japan) and ACUSON Sequoia (Sie-
mens Medical Solutions, Erlangen, Germany) machines.
The Aplio i800 system was equipped with a convex array
i8CX1 transducer (frequency, 1.0-8.0 MHz) for US and
CEUS, with mechanical index 1.6. The Sequoia system
was equipped with a convex array 5C1 transducer (fre-
quency, 1.0-5.0 MHz) for US and CEUS, with mechani-
cal index 1.01. One hour before the examination, the
Fig 1. Flowchart of the study population patient was asked to drink 500-1000 ml of water until
24 Ju Zhu et al Applying the VI-RADS score in conventional US and CEUS to differentiate muscle-invasive bladder cancer
Table I. VI-RADS category assessment of conventional US and CEUS (adapted from Panebianco et al [12])
Structural category (US) Contrast-Enhancement category (CEUS) VI-RADS
Intact hyperechoic bladder wall at base of tumor No early enhancement of the muscularis propria 1
(lesion <1 cm, exophytic tumor with or without stalk (lesions corresponding to SC1 findings)
and with or without thickened inner layer) (SC1)
Intact hyperechoic bladder wall at base of tumor No early enhancement of muscularis propria 2
(lesion >1 cm, exophytic tumor with stalk or without with early enhancement of inner layer
thickened inner layer, when present, or sessile tumor (lesions corresponding to SC2 findings)
with thickened inner layer, when present) (SC2)
Lack of category 2 findings with associated presence Lack of category 2 findings 3
of an exophytic tumor without thickened inner layer, (lesions corresponding to SC category 3 findings)
or sessile tumor without thicken inner layer but but with no clear disruption of hypoenhancing
without clear disruption of hyperechoic bladder wall (SC3) muscularis propria
Interruption of hyperechoic bladder wall suggesting Tumor early enhancement extends focally 4
extension of tumor tissue to muscularis propria (SC4) to muscularis propria
Tumor tissue extending into the extravesical fat, representing Tumor early enhancement extends to the entire bladder 5
invasion of the entire bladder wall and extravesical tissues wall and extravesical fat, representing the invasion of
(SC5) entire bladder wall and extravesical tissues

the bladder volume reached approximately 400 ml. The


examination was performed with the patient in supine
position. The size, location, shape, blood flow signals of
the lesion and continuity of the bladder wall need to be
assessed in US.
When multiple tumors were identified, only the larg-
est tumor was selected for CEUS examination, switching
to CEUS mode at the maximum section of the lesion. A
bolus of 3.6 ml SonoVue (Bracco SpA, Milan, Italy) was
injected via an antecubital vein, followed by a flush with
5.0 ml of saline. Images and cine clips of entire CEUS
were stored for offline analysis.
Image analysis
All US and CEUS images were scored by 2 sonogra-
phers with more than 5 years of experience in abdominal
Fig 2. Schematic representation of VI-RADS scoring based on
CEUS, blinded to the pathological results and other im- conventional US and CEUS
aging results. The criteria for US, CEUS image analysis
and VI-RADS scoring was performed according to crite- predictive value, negative predictive value, and accuracy
ria detailed in Table Ⅰ and figure 2. were calculated using a two-way contingency table. In-
Statistical analysis terobserver agreement was evaluated using the weight-
A VI-RADS score, which represents an overall risk ed-kappa coefficient (κ). Weighted kappa values ≤0.4
score of muscle invasion, was assigned to each patient. indicate fair agreement, 0.41-0.6 moderate agreement,
A VI-RADS score greater than 3 (4 or 5) was consid- 0.61-0.8 good agreement, and ≥0.81 excellent agreement.
ered MIBC, a score less than 3 (1 or 2) was considered
NMIBC, and a score of 3 was considered equivocal. Results
Data analysis was performed using SPSS version 23.0
and MedCalc version 20.115 data analysis software. The Patient characteristics
count data are expressed as mean ± SD and percentage, A total of 38 patients (including 32 males and 6 fe-
and the measuring data are expressed as frequency distri- males; age range, 24-79 years; mean age ± SD, 60.8±11
bution table. ROC curve analysis and area under the curve years) were included in this study. Of the 38 patients, 10
(AUC) were used to assess the diagnostic performance of (26.3%) had multiple tumors. Among the 38 patients,
VI-RADS score in differentiating MIBC. Difference be- 17 (44.7%) underwent radical cystectomy, 1 (2.6%) un-
tween areas under the curve using the method described derwent partial cystectomy, and 20 (52.6%) underwent
by Hanley and McNeil. Sensitivity, specificity, positive TURBT. Histopathological results found 25 patients
Med Ultrason 2023; 25(1): 22-28 25
(65.8%) with NMIBC and 13 patients (34.2%) with Table II. The characteristics of tumor
MIBC. The characteristics of all tumors are shown in Characteristic Value
Table Ⅱ. Maximum diameter 3.19±1.42
Inter-reader agreement in scoring for each type of
Tumor grade
image
Inter-reader agreement on US scoring was excellent High 27 (71.1)
(κ=0.824). Inter-reader agreement on CEUS scoring was Low 11 (28.9)
good (κ=0.791). Tumor staging
Diagnostic performance of VI-RADS Ta 6 (15.8)
The US and CEUS scores for each image type, VI- T1 19 (50.0)
RADS score, and pathological stage established by the T2 8 (21.1)
two readers are shown in Table Ⅲ. In figures 3 to 6 we
T3 4 (10.5)
exemplified the US and CEUS aspect of VI-RADS score
1 to 5. T4 1 (2.6)
Diagnostic performance of different VI-RADS Location
score cutoff values for MIBC identification Anterior wall 5 (13.2)
The diagnostic performance of VI-RADS for predict- Posterior wall 19 (50.0)
ing MIBC at different cutoff values is shown in Table Ⅳ. Lateral wall 12 (31.2)
When comparing the VI-RADS score with pathological Diverticulum 2 (5.3)
findings, the AUC value of ROC analysis was 0.862 (95%
Histology
CI:0.734-0.989) for reader 1 and 0.882 (95%CI:0.761-1)
for reader 2. There was no statistical difference between Urothelial carcinoma 37 (97.4)
the AUCs (p=0.455) of the ROC curves for the VI-RADS Adenocarcinoma 1 (2.6)
scores of the two observers. Data are presented as number (percent) unless otherwise noted.

Table III. Pathological stage corresponding to each image score and VI-RADS score by the readers.
Reader 1 Reader 2
n NMIBC MIBC n NMIBC MIBC
US
1 2 2 (100) 0 (0) 2 2 (100) 0 (0)
2 6 6 (100) 0 (0) 6 5 (83.3) 1 (16.7)
3 13 12 (92.3) 1 (7.7) 14 14 (100) 0 (0)
4 12 4 (33.3) 8 (66.7) 9 3 (33.3) 6 (66.7)
5 5 1 (20.0) 4 (80.0) 7 1 (14.3) 6 (85.7)
CEUS
1 2 2 (100) 0 (0) 2 2 (100) 0 (0)
2 6 6 (100) 0 (0) 6 5 (83.3) 1 (16.7)
3 13 12 (92.3) 1 (7.7) 14 14 (100) 0 (0)
4 11 5 (45.5) 6 (54.5) 7 3 (42.9) 4 (57.1)
5 6 0 (0) 6 (100) 9 1 (11.1) 8 (88.9)
VI-RADS
1 2 2 (100) 0 (0) 2 2 (100) 0 (0)
2 6 6 (100) 0 (0) 6 5 (83.3) 1 (16.7)
3 13 12 (92.3) 1 (7.7) 14 14 (100) 0 (0)
4 11 5 (45.5) 6 (54.4) 7 3 (42.9) 4 (57.1)
5 6 0 (0) 6 (100) 9 1 (11.1) 8 (88.9)
Data are presented as number (percent). n- number of patients; VI-RADS, vesical imaging reporting and data system; CEUS, contrast-
enhanced ultrasound; NMIBC, non-muscle-invasive bladder cancer; MIBC, muscle-invasive bladder cancer.
26 Ju Zhu et al Applying the VI-RADS score in conventional US and CEUS to differentiate muscle-invasive bladder cancer

Fig 3. A 57-year-old male with bladder carcinomas pathologi- Fig 4. A 55-year-old male with bladder carcinomas pathologi-
cally diagnosed as stage T1. A, A longitudinal section conven- cally diagnosed as stage T1. A, A longitudinal section conven-
tional ultrasound image showed an approximately 0.9-cm-sized tional ultrasound image showed an approximately 1.7-cm-sized
exophytic neoplastic lesion at the posterior bladder wall, and exophytic tumor lesion with stalk (arrowhead) at the posterior
hyperechoic bladder wall (white arrows) at tumor base is intact bladder wall, and hyperechoic bladder wall (white arrows) at
(score 1). B, The CEUS image showed an enhanced tumor le- tumor base is intact (score 2). B, The CEUS image showed an
sion with no enhancement of muscularis propria (white arrows) enhanced tumor without enhancement of muscularis propria
(score 1). Overall, VI-RADS score is 1. (white arrows) (score 2). Overall, VI-RADS score is 2.

Fig 5. A 67-year-old male with bladder carcinomas pathologi- Fig 6. A 62-year-old male with bladder carcinomas pathologi-
cally diagnosed as stage T1. A, A longitudinal section conven- cally diagnosed as stage T2. A, A transverse section conven-
tional ultrasound image showed an approximately 2.3-cm-sized tional ultrasound image showed an approximately 3.8-cm-sized
exophytic tumor lesion without stalk at the right lateral blad- exophytic tumor lesion with interruption of hyperechoic blad-
der wall, and hyperechoic bladder wall (white arrows) at tumor der wall (arrowheads) at the anterior bladder wall (score 4). B,
base without clear disruption (score 3). B, The CEUS image The CEUS image showed early enhancement tumor extends
showed a tumor with no clear disruption of hypoenhancing focally to muscularis propria (arrowheads) (score 4). Overall,
muscularis propria (score 3). Overall, VI-RADS score is 3. VI-RADS score is 4.

Fig 7. A 54-year-old male with bladder carcinomas pathologi-


cally diagnosed as stage T3. A, A longitudinal section conven-
tional ultrasound image showed an approximately 6.1-cm-sized
exophytic tumor lesion (arrowheads) at the anterior bladder
wall had extended to the extravesical adipose tissue (score 5).
B, The CEUS image showed early enhancement and heteroge-
neous tumor (arrowheads) extended to the entire bladder wall Fig 8. Comparison of receiver operating characteristics curve
and extravesical fat (score 5). Overall, VI-RADS score is 5. analysis for both readers
Med Ultrason 2023; 25(1): 22-28 27
Table IV. Diagnostic performance of different VI-RADS score cutoff values for muscle-invasive bladder cancer identification
VI-RADS cutoff value Se Sp PPV NPV Acc AUC
Reader 1 ≥3 100.0 32.0 43.3 100.0 55.3
≥4 92.3 80.0 70.6 95.2 84.2 0.862 (95%CI:0.734-0.989)
Reader 2 ≥3 92.3 28.0 40.0 87.5 50.0
≥4 92.3 84.0 75.0 95.5 86.8 0.882 (95%CI:0.761-1)
All results indicate percentages. VI-RADS, vesical imaging reporting and data system; Se, sensitivity; Sp, specificity; Acc, Accuracy;
PPV, positive predictive value; NPV, negative predictive value; AUC, area under curve.

Discussion We first give a VI-RADS score according to the US


images of the lesion, and then upgrade or downgrade the
In patients with BC an accurate preoperative staging lesion scores according to the CEUS findings. For exam-
is crucial. This staging is not related only to the clini- ple, in our study, some lesions with a US score of 4 were
cal management of the patient, especially to the surgi- upgraded to VI-RADS 5 after CEUS assessment, this
cal approach, but also closely related to prognosis [17]. gives clinicians sufficient confidence to perform radical
CEUS can achieve comparable sensitivity and specificity cystectomy for patients.
to MRI in staging of BC, which suggests that CEUS is Similar to Metwally et al [19], in our study all the
a valuable method in preoperative staging of BC [18]. lesions scored as VI-RADS 1 were pathologically con-
VI-RADS was originally developed to standardize MRI firmed as NMIBC. This increases clinicians’ confidence
image collection in BC patients at risk for muscularis in performing TURBT in these patients. We found only
invasion [9], but our results showed that the VI-RADS a very few lesions scored as VI-RADS 2 and 3 that had
scoring system based on US and CEUS can be used for MIBC aspect in histopathological examination, while
the same purpose. the vast majority of lesions scored as VI-RADS 5 were
The layers of the bladder are sometimes difficult to MIBC. We found that VI-RADS 4 had the poorer diag-
be distinguished using US [16], so the correct staging of nostic performance for predicting MIBC, with patho-
BC is not enough accurately. In CEUS, the mucosal layer logically confirmed NMIBC in 5 (45.5%) of 11 patients
showed early and intense enhancement, while the muscu- scored VI-RADS 4 in reader 1 and 3 (42.9%) of 7 pa-
lar propria showed late and low enhancement. If BC had tients scoring VI-RADS 4 in reader 2. This suggests that
infiltrated the muscle layer, this layer would show early our score needs to be supplemented with more details to
and strong enhancement. Caruso et al [16] have shown improve its diagnostic performance. Overstaging of the
that CEUS has excellent diagnostic performance in dis- lesion may be related to overfilling of the bladder prior
tinguishing MIBC, nevertheless, as they mentioned, they examination. This may increase the patient discomfort,
were simply asked to distinguish between infiltrating and resulting in difficulty in examination and increased arti-
non-infiltrating tumors, regardless of the degree of infil- fact [16]. In addition, the location of the lesion may also
tration. We used the disappearance of the hypoenhancing lead to overstaging of the tumor. Tumors of the lateral
muscle layer as a landmark sign to determine whether wall of the bladder are difficult to examine compared to
muscular invasion was present, and if the hypoenhanc- the trigone [16,20].
ing muscle layer was intact, the lesion was scored 1 to 3 Using a score ≥4 as the cutoff value, the AUC value
according to other signs; conversely, if the hypoenhanc- of VI-RADS was 0.882 (95%CI:0.761-1), with a sensi-
ing muscle layer was partially interrupted or completely tivity of 92.3%, with a specificity of 84%, and with accu-
disappeared, the lesion was scored 4 to 5 according to the racy of 86.8%. The same cut off was established by Kim
degree of invasion. The degree of BC invasion in each et al [2]. Using a lower VI-RADS total score as a cutoff
patient could be explained in more detail by the given for evaluating MIBC has a high false positive rate.
score, and clinicians decide the patient’s next treatment The aim of VI-RADS is to optimize and standardize
options by different scores, TURBT being the best op- image acquisition for bladder MRI and ultimately stand-
tion for patients with VI-RADS 1, whereas patients with ardize future treatment response. Accurate preoperative
a score of VI-RADS 5 must undergo radical cystectomy. staging can avoid repeated TURBT, thereby reducing
It should be noted that in our study, tumors with stalk postoperative complications and the economic burden
refer to morphology in US, which differed from the score [21,22]. Our study suggests that VI-RADS based on US
of multiparametric MRI. In addition, there are three se- and CEUS may have some value in differentiating MIBC.
quences in MRI that help scoring, while our scoring sys- Our study still has some limitations. First, our sample
tem relies only on US and CEUS. size was small, which requires subsequent inclusion of
28 Ju Zhu et al Applying the VI-RADS score in conventional US and CEUS to differentiate muscle-invasive bladder cancer

more cases to validate this approach. Second, this study 9. Wang H, Luo C, Zhang F, et al. Multiparametric MRI for
was retrospective and there is inevitable bias in the selec- Bladder Cancer: Validation of VI-RADS for the Detection
tion of samples. To reduce the impact of this bias, a pro- of Detrusor Muscle Invasion. Radiology 2019;291:668-
674.
spective study is required. Third, for patients with mul-
10. Ueno Y, Takeuchi M, Tamada T, et al. Diagnostic Accuracy
tiple lesions, the section of the specimen during surgery
and Interobserver Agreement for the Vesical Imaging-Re-
was not always consistent with that identified by US, porting and Data System for Muscle-invasive Bladder Can-
which may have affected the accuracy of the study results cer: A Multireader Validation Study. Eur Urol 2019;76:54-
to some extent. Further studies need to exclude patients 66.
with multiple lesions to eliminate this effect. Fourth, the 11. Hansel DE, Amin MB, Comperat E, et al. A contemporary
accuracy of US often relies on the operator’s technique update on pathology standards for bladder cancer: transure-
and to really appreciate the utility of US, the comparison thral resection and radical cystectomy specimens. Eur Urol
with MRI VI-RADS must be done. 2013;63:321-332.
12. Panebianco V, Narumi Y, Altun E, et al. Multiparametric
Conclusions Magnetic Resonance Imaging for Bladder Cancer: Devel-
opment of VI-RADS (Vesical Imaging-Reporting And Data
System). Eur Urol 2018;74:294-306.
In conclusion, our study yielded some encouraging 13. Wang Z, Shang Y, Luan T, et al. Evaluation of the value of
results about the use of US and especially CEUS in stag- the VI-RADS scoring system in assessing muscle infiltra-
ing the BC. However, a prospective trial with a larger tion by bladder cancer. Cancer Imaging 2020;20:26.
number of cases is needed in order to validate the feasi- 14. Salmanoglu E, Halpern E, Trabulsi EJ, Kim S, Thakur ML.
bility of this VI-RADS based on US and CEUS score in A glance at imaging bladder cancer. Clin Transl Imaging
differentiating MIBC from NMIBC in subsequent stud- 2018;6:257-269.
ies. 15. Li QY, Tang J, He EH, et al. Clinical utility of three-dimen-
sional contrast-enhanced ultrasound in the differentiation
Conflict of interest: none between noninvasive and invasive neoplasms of urinary
bladder. Eur J Radiol 2012;81:2936-2942.
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Original papers Med Ultrason 2023, Vol. 25, no. 1, 29-34
DOI: 10.11152/mu-3832

Mammography and breast ultrasound analysis in male and female


transgender persons using long-term gender affirming hormone
therapy: a cross-sectional study in Brazil
Ana A. Bartolamei Ramos1,2, Cristiane Spadoni2, Paulina A. Santander1, Beatriz dos Santos3,
Rosires P. Andrade3, Jaime Kulak Jr.1,3

1Post Graduation Program in Obstetrics and Gynecology at Federal University of Paraná, 2IMAX Image Center,
3Department of Obstetrics Gynecology at Federal University of Paraná, Curitiba, Brazil

Abstract
Aim: There is not much information about breast health in transgender (transexual) persons given the historical stigma
that this population suffers. This research aimed to describe breast imaging patterns in transgender (trans) women and men
that had been using gender affirmation hormone treatment for at least 3 years. Material and methods: In this observational,
cross-sectional study, 67 transgender individuals (34 trans women and 33 trans men) had mammography and breast ultrasound
performed. We also classified the findings by the American College of Radiology – Breast Imaging Reporting and Data Sys-
tem (ACR BI-RADS®). Results: We found that there was a higher frequency of dense breasts in trans women (75.8%) and in
trans men (66,6%) than expected for cisgender (cis) women. Conclusions: This study highlights the importance of a deeper
understanding of the image patterns of transgender breasts because of hormonal effects that the gender transition entails so we
can offer better health care and preventive services in the transgender (transexual) population.
Keywords: transgender; mammography; breast ultrasound; mammary density

Background preventive measures, including imaging evaluation for


breast cancer prevention [2].
Transgender (transexual) individuals identify them- For better expressing their intended gender, trans
selves with a gender different than the biological sex people undergo gender-affirming hormone therapies and
assigned to them at birth. A current estimate indicates breast procedures that may impact their imaging evalua-
that 0.5–1.3% and 0.4-1.2% of all individuals assigned, tions and impose challenges to radiologists. Most clinical
respectively, a male and female biological sex become issues that trans people face are similar to those experi-
transgender [1]. These individuals are victims of preju- enced by cisgender people, although some uncertainties
dice and face substantial quality gaps in health care and remain, particularly regarding cancer screening [3]. For
example, breast cancer screening guidelines and proto-
cols followed for trans men and women are often the
Received 29.07.2022 Accepted 04.12.2022 same as those recommended for cis women [4].
Med Ultrason
2023, Vol. 25, No 1, 29-34
Gender-affirming hormone therapy is one of the ap-
Corresponding author: Jaime Kulak Jr., MD, PhD proaches to change secondary sexual characteristics.
Gynecology and Obstetrics Department Trans women – individuals labeled as male at birth but
Federal University of Paraná defining themselves as female – undergo such therapy
181 General Carneiro street,
80060-900 Curitiba, Paraná, Brazil
with the use of oestrogens and anti-androgens. In breast,
Phone +55413525-6855 this results in mammary gland development with forma-
E-mail: jaimekulak@gmail.com tion of lobules and acini and increased probability of
30 Ana A. Bartolamei Ramos et al Mammography and breast US analysis in transgender persons using g-a hormone therapy

pseudo-lactation. Prolonged use of these hormones can Material and methods


reduce substantially the volume of the testis and prostate
gland [4,5]. Trans men – individuals labeled as female at The protocol of the study was approved by the Re-
birth but defining themselves as males – undergo gender- search and Ethics Committee of the Federal University of
affirming hormone treatment with testosterone alone, Paraná (CEP-UFPR; Curitiba, Brazil) and all participants
and this approach is sufficient to induce male secondary signed an informed consent form.
sexual characteristics. With this therapy, trans men pre- In this cross-sectional study, we performed mam-
sent a reduction in the breast glandular tissue with invo- mographic and breast ultrasound evaluations of 34 trans
lution of lobular structures and increased fat deposition women and 33 trans men. For inclusion in the study, trans
[6]. women were required to have visible breast develop-
In addition to cancer screening, breast imaging is also ment and >3 years of hormone therapy, while trans men
commonly performed in this population in preparation for were required to have >3 years of testosterone use and
gender-affirming surgeries (mastectomy in trans men and no mastectomy. The individuals were included in a non-
breast enlargement in trans women). In the “frequently randomized manner, by invitation during their regular
asked questions” section of the Breast Imaging Reporting outpatient clinic visits, and by handout and invitations
and Data System (ACR BI-RADS), the American Col- on social media by non-governmental organizations sup-
lege of Radiology recommends the sex assigned at birth porting this population.
to be used for imaging analysis (i.e., male protocol in We used the equipment Selenia Dimensions (Hologic,
trans women) [7]. However, as pointed out by Kahai et Bedford, MA, USA) for mammography and Aplio 300
al [5], trans women receiving gender-affirming hormone (Toshiba Medical Systems, Tokyo, Japan) for all ultra-
therapy have completed acinar and lobular formations, sound evaluations. The images were analyzed separately
suggesting that the breast gland behaves biologically and and blindly by two radiologists experienced in breast im-
radiographically as a female breast. In trans men, includ- aging evaluation. For participants with breast implants,
ing those who do not undergo mastectomy, the use of tes- mammography was performed using the Eklund tech-
tosterone also modifies the characteristics of the breast nique. The reports were prepared following the ACR BI-
on imaging evaluation, leading to an important reduction RADS guidelines. Disagreements between both radiolo-
in glandular tissue [8]. However, breast cancer screening gists were resolved by adjudication with the inclusion,
in trans men continues to be performed according to the when necessary, of a third radiologist.
protocols followed for cis women [9]. Statistical analysis
Indications for breast imaging in trans people are the The results are presented as mean and standard devia-
same as those for cis women, e.g., palpable abnormalities tion values, and as rates and percentages. Stata/SE v.14.1
and unilateral nipple discharge. Additionally, the same (StataCorp LP, College Station, TX, USA) was used to
incidences and protocols used for cis women are adopted calculate the Cohen’s kappa coefficient of the agreement
for trans people. For example, in the absence of free liq- between the reports of the two radiologists and to classify
uid silicone, palpable abnormalities should be evaluated the magnitude of the agreement being considered absent
with both mammography and ultrasonography, while the agreement with a coefficient < 0.00, mild with a coeffi-
presence of breast implants should prompt the use of the cient of 0.01-0.20; regular with 0.21-0.40; moderate with
Eklund technique in mammography. 0.41-0.60; important with 0.61-0.80, almost perfect with
Injections of industrial-grade liquid silicone are 0.81-0.99 and perfect with 1.00.
sometimes used in low-income and medically underpriv-
ileged trans populations for the increase of volume in the Results
breasts and buttocks and manipulation of facial features.
When used for breast enlargement, these injections hin- Trans women compared with trans men were older
der the radiologic evaluation of the breast parenchyma as (38.7±11.2 years vs. 30.4± 6.0 years, respectively) and
they may be associated with the development of scleros- had used hormones for a longer time (10.7±8.7 years
ing lipogranuloma, infection, and abscess [3,10,11]. vs. 3.5±1.0 years, respectively). All trans men and trans
Considering the increasing rates of gender-affirming women were using testosterone and oestrogen, respec-
hormone and surgical therapies and the scarcity of infor- tively. Although trans men used exclusively testosterone,
mation regarding breast imaging among trans people, the trans women also used anti-androgens (85.3%, including
aim of this study was to evaluate breast imaging patterns cyproterone) and non-cyproterone progestins (61.8%).
and findings in a population of male and female transex- Since Brazilian regulations control the prescription of
ual individuals in Brazil. androgens, all trans men had a medical prescription for
Med Ultrason 2023; 25(1): 29-34 31

Fig 1. Mammography of a breast with normal glandular devel- Fig 2. Mammography of a breast enlarged with industrial grade
opment in a trans woman. liquid silicone

Fig 3. Breast ultrasonography showing industrial-grade free


liquid silicone, in which the silicone deposits hinder the visu- Fig 4. Mammography of a trans woman: dense breast with ret-
alization of any element underneath. roglandular intact silicone implant.

ferent birth control preparations (most with formulations


containing progestin) was found in this group.
All trans women in this study had breast glandular
tissue enlargement (fig 1). Six of them had free liquid
silicone, 1 by implant rupture and the other 5 by indus-
trial silicone injections (fig 2, fig 3). Calcifications and
axillary lymph nodes were seen more frequently in mam-
mography exams. Of the 33 trans women, only 8 had
breasts implants, all of which were retroglandular (fig 4,
fig 5). We eventually defined most of the ultimate results
in trans women as BI-RADS 1 and 2. In our sample only
2 individuals were BI-RADS 3, one due to a nodule (fig
6) and the other due to grouped microcalcifications. As
for breast density, the most frequent result were catego-
ries C and D both in trans women (60.6% and 15.2% re-
spectively) and in trans men (45.4% and 21.2% respec-
Fig 5. Mammography of a trans woman: dense breast with ret- tively) (fig 7).
roglandular intact silicone implant with Eklund technique. Both radiologists had a strong agreement in their re-
ports. Table I shows the Cohen’s kappa coefficients for
testosterone. In contrast, 53.9% of the trans women had the agreements.
no prescription for the hormones in use, while 5.9% of all Tables II and III show the results of the mammogra-
trans women had never had a prescription for hormones. phy and breast ultrasound evaluations in the overall co-
A substantial variation among the hormones used by hort. We identified breast nodules and cysts in 3 individu-
trans women, with 18 different treatment protocols, 9 dif- als (1 trans woman and 2 trans men).
32 Ana A. Bartolamei Ramos et al Mammography and breast US analysis in transgender persons using g-a hormone therapy
Table I. Correlations of the agreement between the two radiolo-
gists in evaluating the breast findings.
Variable Correlation (kappa)
ACR BI-RADS 0.69
Breast composition 0.96
Breast implants 0.87
Free liquid silicone 0.91
Calcifications 0.61
Fig 6. Breast ultrasonography in a trans woman showing a Lymph nodes 0.45
solid nodule: oval shape, circumscribed margin, hypoechoic: Lymph node classification 1.00
a) transversal plane and b) longitudinal plane.
Table II. Mammography patterns in trans women and trans
men
Trans women Trans men
BI-RADS
1 6 (18.2%) 12 (36.4%)
2 25 (75.8%) 18 (54.5%)
3 2 (6.1%) 3 (9.1%)
Breast composition
A 3 (9.1%) 2 (6.1%)
B 5 (15.2%) 9 (27.3%)
C 20 (60.6%) 15 (45.4%)
D 5 (15.2%) 7 (21.2%)
The results are expressed as number (%)

Fig 7. Mammography of a trans man: dense breasts.


Table III. Breast ultrasound patterns in trans women and trans
men
Discussion
Trans women Trans men
There is very little information on breast health in BIRADS
the transexual population, mainly because of the historic 1 12 (35.3%) 20 (60.6%)
2 21 (61.8%) 11 (33.3%)
prejudice and scorn that individuals in this population re-
3 1 (2.9%) 2 (6.1%)
ceive in our current society and in medicine in particular.
Echotexture
Therefore, very few studies have focused on this popula-
homogeneous background
tion’s specific needs [12].
– fat 7 (20.6%) 7 (21.2%)
Gender-affirmation treatments and surgeries are an homogeneous background
important aspect in the lives of transexual (trans) peo- – fibroglandular 15 (44.1%) 20 (60.6%)
ple. Interventions targeting the breasts (e.g., enlargement heterogeneous 12 (35.3%) 6 (18.2%)
therapy and implants in trans women and mastectomy in The results are expressed as number (%)
trans men) have an enormous impact on the psychologi-
cal and social wellbeing of the trans population. study, we identified dense breasts in 75.8% of the trans
In the US, the incidence of dense breasts in cis wom- women (60.6% type C and 15.2% type D) and in 66.6%
en has been described at 50%. Breast density by itself is of the trans men (45.4% type C and 21.2% type D), in-
considered an independent risk factor for breast cancer, dicating an even higher prevalence of this finding in our
and individual risk stratification models use it for this cohort.
purpose. The notification of a “dense breast” result is All participants in our study used medical grade gen-
also mandatory in more than half of that country’s states der-affirming hormones, i.e., all trans men used testos-
[7,13]. terone and all trans women used oestrogen. Among trans
In 2010, Weyers et al [14] performed mammographic women with dense breasts, 88% also used antiandrogens
evaluation of 50 trans women and reported the occur- (including cyproterone) and 68% used a non-ciproterone
rence of dense breasts in 60% of them (breast composi- progestin, even though the protocols recommend the
tion type D in 22% and type C in 38%). In the present use of oestrogen and a single antiandrogen [4,15,16]. A
Med Ultrason 2023; 25(1): 29-34 33
substantial variation among the hormones used by trans the actions of testosterone on breast tissue are less clear
women, with 18 different treatment protocols, 9 different as it can have both androgenic and estrogenic effects
birth control preparations (most with formulations con- [21].
taining progestin) was found in this group. This explains Although there is no consensus for breast screen-
the increased amount of progestins used by our cohort of ing in transgender, Sowinski at al [9] suggest screening
trans women in relation to current protocols [4,15,16]. mammography every one or two years beginning at age
Patients who had industrial silicone injection had 50 in transgender women who have been using hormone
their breast assessments impaired. Free silicone reduces therapy for at least 5 years. For transgender women with-
the sensitivity of both ultrasound and mammography. out hormone use, no screening is necessary. Transgender
Breast augmentation by direct injection of silicone pre- men without bilateral mastectomy follow recommenda-
sents a special challenge for imaging because fibrosis and tions for cisgender women. For transgender men post-
granulomas obscure normal tissue on mammography and mastectomy, screening is not recommended.
ultrasound. An option is contrast enhanced MRI because The difficulty in recruiting patients from the general
granulomas are non-enhancing lesion that has T2 high population was the main limiting factor for this research.
signal with absent signal in T1-weighted fat-suppressed All participants were recruited from a specialized outpa-
images. Tomosynthesis image can show displacement of tient clinic, which may have underestimated the altera-
silicone granulomas in case of breast tumor [3]. tions found in this study.
Breast augmentation with implants is commonly
used as part of sex reassignment surgery and will have Conclusions
the typical appearance of breast implants on mammogra-
phy. Evaluation for implant rupture is like that performed There is little evidence in the literature regarding the
in cis-woman, incorporating ultrasound, mammography, effects of gender-affirming hormone treatment on breast
and possibly MRI. Some transgender women may opt to in trans men and trans women. Breast imaging of liv-
have large volumes of liquid silicone injected into their ing transgender individuals is even more scarce. To the
breasts for breast augmentation [12]. best of our knowledge, this is the first study evaluating a
We found no other published studies evaluating breast large sample of trans men with mammography and breast
imaging findings in trans men. Grynberg et al [8] evalu- ultrasound, and one of the few examining with the same
ated histological samples of 100 breast tissues obtained imaging tests a large cohort of trans women.
from mastectomy of trans men who had used at least 6 This study clearly shows that our knowledge of breast
months of hormone therapy. The authors observed an im- health in transexual people is not what it should be. The
portant decrease in glands and proliferation of connective high prevalence of dense breasts in this population in
tissue in 93% of their samples. Accentuated lobular atro- comparison to cis women indicates that transexual peo-
phy was found in 7% and moderate atrophy in 86% of ple are probably not receiving the best care that medicine
them, while fibrocystic lesions and fibroadenomas were can provide, simply because the protocols used are not
found in 34% and 2%, respectively. fitted to these individuals. It is urgent that more and large
We found that 66.6% of the trans men in our cohort studies are conducted so we can determine if this is true
had dense breasts (45.4% type C and 21.2% type D). in other settings, and if so, what are the clinical implica-
Hormonal proliferative stimuli cause increased breast tions of these findings.
density. It is oestrogen that promotes increase in breast If our results are confirmed in other studies, proto-
size and differentiation of duct epithelial and connective cols of preventive measures in the transexual population
tissues [17]. There is gonadal (ovaries) and extragonadal should be immediately and urgently reviewed and pos-
production of oestrogens. This extra-gonadal produc- sibly changed.
tion is in adipose tissue where the enzyme aromatase
converts androgens in oestrogen [18]. Therefore, exog- Conflict of interest: none
enous testosterone in trans men behaves as a precursor
and is converted (by the enzyme aromatase) in some Acknowledgments: the authors would like to thank
metabolites (e.g., 17-beta-estradiol and 5-alpha-dihy- the CPATT (Centro de Pesquisa e Atendimento ao Trav-
drotestosterone) [19]. The study of Tan et al backs this esti e Transexual) which is a government-funded out-
hypothesis [20] when they evaluated 34,016 cis men us- patient clinic for transexual individuals in the state of
ing hormone replacement therapy with testosterone in- Paraná, Brazil, and its Coordinator Andressa Verchai de
jections and observed an increase in 17-beta-oestradiol, Lima and Dra. Edna Barbosa for help in contacting will-
especially among 25-44-year-old subjects. In cis women, ing trans people to take part in the study.
34 Ana A. Bartolamei Ramos et al Mammography and breast US analysis in transgender persons using g-a hormone therapy
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Original papers Med Ultrason 2023, Vol. 25, no. 1, 35-41
DOI: 10.11152/mu-3827

Ultrasound-guided versus computed tomography-controlled


periradicular injections of the first sacral nerve:
a prospective randomized clinical trial
Michaela Plaikner1, Nikolaus Kögl2, Hannes Gruber1, Reto Bale1, Wing Mann Ho2,
Elisabeth Skalla-Oberherber1, Alexander Loizides1

1Department of Radiology, 2Department of Neurosurgery, Medical University of Innsbruck, Innsbruck, Austria

Abstract
Aim: To compare ultrasound (US)-guided versus computed tomography (CT)-controlled periradicular injections of the
first sacral spinal (S1) nerve in a prospective randomized clinical trial. Materials and methods: Thirty-nine patients with
S1-radiculopathy were consecutively enrolled for 40 periradicular injections and assigned to an US or CT guided group.
Needle position after US-assisted placement was controlled by a low-dose CT-scan. Accessibility, accuracy, and intervention
time were compared. The overall effect on pain was matched evaluating the visual analog scale (VAS) decrease before and
one month after the intervention. Results: The mean intervention time was lower in the US-group compared to the CT-group:
4.4±3.46 min (1.3-13.2) vs. 6.5±3.03 min (2.4-12.5). Using CT-controlled infiltration the mean number of needle passes was
with 1.15 higher than utilizing US-guidance. The therapeutic effect (mean difference between pre- and post-intervention,
VAS scores) for the CT-group was 4.85±2.52 and for the US-group 4.55±2.74 with no significant difference between the two
groups (p=0.7). Conclusion: US-controlled infiltrations of the first sacral nerve show a similar therapeutic effect to the time
consuming, and ionizing CT-controlled injections and result in a significant reduction of procedure expenditure and avoidance
of radiation.
Keywords: image-guided; infiltration; injection; pain; ischialgia

Introduction [4]. Many different opinions regarding the image guid-


ance techniques, the agents to be injected, the dose and
In today`s clinical routine a selective nerve root block the timing of repeated injections exist [5,6]. Besides the
has become an important non-surgical treatment option “blind” access, which is not regarded as a valid option,
that – beside physiotherapy and analgesics – is increas- several imaging modalities are used to reach the com-
ingly offered to patients with radicular compression neu- pressed nerve root. These include fluoroscopy, computed
ropathy [1,2]. Steroids directly injected locally at the tomography (CT) and ultrasound [7]. Due to anatomic
affected nerve root provoke an anti-inflammatory effect precision and spatial resolution CT is currently the pre-
[3] by stabilizing cellular membranes, suppressing im- ferred method [8-10] and is therefore regarded the “gold
mune responses, enhancing neuronal blood flow, releas- standard” imaging tool. However, potential benefits of
ing fibrosis and washing out inflammatory substances ultrasound guidance, including real time needle control
and avoidance of radiation seem to be attractive. Mean-
Received 21.07.2022 Accepted 18.12.2022 while, comparative clinical studies between CT and ul-
Med Ultrason
2023, Vol. 25, No 1, 35-41
trasound exist for periradicular injection therapies (PRT)
Corresponding author: Wing Mann Ho in the cervical [11] and lumbar spine [12]. The lumbosa-
Department of Neurosurgery, cral region as a mechanic transition zone is prone to in-
Medical University of Innsbruck juries [13] and degeneration changes: disc herniation,
35 Anichstrasse, 6020 Innsbruck, Austria
Phone/fax +43 (0)512 504 27452
spinal or foraminal stenosis can provoke relatively com-
+43 (0)512 504 27453 mon, radicular compression neuropathy of the first sacral
E-mail: wing.ho@i-med.ac.at nerve (S1 radiculopathy) [14]. Moreover, in a previous
36 Michaela Plaikner et al US-guided versus CT-controlled periradicular injections of the first sacral nerve

cadaver study the accuracy of US-guided needle place- Image-guided infiltrations


ment within the dorsal sacral foramen has already been The patients were randomized using a computer-
proven [15]. generated randomization table Microsoft Excel (Version
The aim of this study was the comparison of US- 21, Redmond, Washington, USA) into two groups (US-
guided versus CT-controlled S1 periradicular injections group vs CT-group):
in a prospective randomized clinical trial evaluating ac- 1. US-guided infiltration
cessibility, accuracy, and intervention time as well as For all US-guided interventions a standard US-device
overall effect on pain relief of US-guided periradicular under default settings (Canon Medical Systems GmbH,
S1 injections compared with the standard CT-controlled Aplio i800) with a convex I8CX1 curved array transduc-
approach. The primary objective of this trial is to prove er was used. Infiltrations were performed by two radi-
that US-guided S1 periradicular injections have the same ologists (HG and ALL) with long-lasting experience in
treatment results as the standard CT-controlled approach. US-guided musculoskeletal interventions.
The patient was placed in a prone position on the CT
Material and methods table. Based on similar preceding studies [11,12] time re-
cording was started with the first US-transducer`s contact
This prospective randomized clinical trial was ap- of the patient`s skin. The injection material was prepared
proved by the local institutional Ethics Board of the under aseptic conditions including the sterile coverage of
Medical University of Innsbruck. (Innsbruck EK Nr: the US transducer. The lower back was cleansed and cov-
1099/2019). ered sterile. The periradicular area of S1 was identified
Patients using landmarks as previously described [15]. Thereby
Thirty-nine patients, based on a standard clinical neu- the first sacral foramen was depicted by positioning the
rological examination and functional testing, were con- transducer in a cranially tilted median-transversal orien-
secutively enrolled by the department of Neurosurgery tation to assess the typical transition from the fifth lum-
of the Medical University of Innsbruck between 06/2020 bar to the first sacral spinous process as described by
and 05/2021 for 40 image guided PRT of S1 (1 patient Loizides et al [12]. By moving the transducer laterally,
was injected on both sides). Inclusion criteria were clini- the respective fifth lumbar and first sacral facet joints
cal and radiological (MRI images) signs of a radicular were identified. Moving the probe slightly caudally the
S1-compression (radiculopathy), age over 18 and in- first sacral foramen was identified as a bony gap. Fol-
formed consent for study participation. Contraindications lowing, a spinal needle (BD Quincke Point spinal anes-
included a known allergy to the applied medical agent thesia needle 20G 3.50 IN 0.9x90 mm – yellow; 405253,
(1 ml Solucelestan, 4 mg Betamethasone), any disease GIMA S.p.A, Gessate, Milan, Italy) was introduced in
or medication which exclude or are critical for injection in-plane technique under real-time visualization (fig 1)
therapies such as diabetes, local, spinal, or systemic in- and advanced into the foramen S1 on the respective side
fection, a spinal tumor, a current anticoagulation therapy until the tip reached the medial osseous border of the
or uncorrectable coagulopathy, a present or not exclud- first sacral foramen (estimated tip depth about 1cm un-
able pregnancy as well as all patients with an appointed der the bone surface). Time recording was stopped with
guardian or a patient`s provision against study partici- the needle in place. Subsequently a low-dose CT scan
pation. Further, for US guided procedures a body-mass (Somatom Confidence®; Siemens, Erlangen, Germany)
index over 36 kg/m2 [16] counted as a further exclusion was obtained to document the final needle position and
criterion. The recruited 39 patients were randomized into evaluate accuracy. Adopted parameters (scan with tube
equal sample sizes with the permuted block randomiza- current at 80kV, 30 mAs), a scan level of 28 mm with
tion method and assigned to the 2 treatment groups. the tip in the center, a field of view of 150 and a gantry
VAS (visual analog scale) tilt parallel to the positioned needle were used. In case of
To evaluate the patient’s harm and pain relief a paper- wrong level or if the needle tip did not reach the aimed
based VAS concerning the actual perception of pain at periradicular position, the needle had to be repositioned
rest graded from 0 (no pain) to 10 (maximum pain) was under US-guidance and the respective time was added to
documented before randomization and one month after the aforementioned. If the correct needle level was con-
the intervention. firmed additional axial scans in a low-dose protocol were
The difference between pre- and post-intervention obtained for exact control of the needle tip position (fig 2).
VAS scores was interpreted as therapeutic effect devia- Once CT documented the correct needle tip position,
tion. In addition, pain relief medications before as well 1 ml of Solu-Celestan (4 mg betamethasone) was inject-
as 1 month after the infiltration were noted. ed into the periradicular compartment. After removing
Med Ultrason 2023; 25(1): 35-41 37
assigned to this group. Time recoding was started with
the low-dose CT scan (Somatom Confidence; Siemens,
Erlangen, Germany). First, a topogram of the lumbosa-
cral region was carried out. Thereafter, a small section of
axial images with a scan level of 28 mm with the first sa-
cral foramen in the center and a slice thickness of 2.4 mm
were acquired for the planning CT. Based on these data
the needle access pathway to reach the periradicular S1
region in the sacral foramen was planned. Using the CT-
positioning laser function the entrance point was marked
on the skin with a sterile pen. The same spinal needle as
described above, was introduced along the planned ac-
cess to the periradicular compartment of S1. Once the
needle was estimated to be positioned correctly, the time
recording was stopped. Time recording was recontinued
just when the control CT scan for verification of the nee-
dle tip started. If the needle tip was in an unsatisfactory
position, a repositioning was carried out until a correct
Fig 1. Example of US-guided infiltration of the first sacral spi- needle placement was documented (fig 3).
nal nerve (S1) on the right side with spinal needle in correct At this timepoint recording was stopped and again 1
position in situ (a without, b with annotations). Arrow: inserted ml of betamethasone (4 mg Solucelestan) was injected
needle, circle: sacral foramen traced by the sacral bone (dotted into the periradicular compartment. After removing the
line: lateral sacral crest, linear line: intermediate sacral crest).
Star: non-fusion of the sacral process. needle, a plaster was applied to the skin’s puncture side.
After the infiltration all patients of both groups were
observed for 15 minutes subsequently for potential com-
plications.
Measurements and statistics
For both groups the following parameter were evalu-
ated and compared: intervention time (in minutes); ra-
diation dose report (dose-length product in mGy*cm);
accuracy of needle tip position (correct level, potential
repositioning); VAS before and one month after the in-
filtration including the difference between pre- and post-
intervention VAS scores; underlying pathology (discal
Fig 2. Example of accuracy check of US-guided infiltration of hernia, discal recessus stenosis, bony recessus stenosis,
the right S1: a) shows the correct needle position in the scout luxated discal hernia)
with verification of the proper needle tip within the first sacral
foramen in the additional axial CT scan in b). Circle: sacral fo-
ramen traced by the sacral bone. Star: non-fusion of the sacral
process.

the needle and cleansing the punctured skin a dressing


was applied at the puncture side.
2. CT-controlled infiltration
Injections were performed on a Somatom Confi-
dence®; Siemens, Erlangen, Germany CT-scanner by one
radiologist with distinctive and long-standing experi-
ence in CT-controlled interventions (BR). Patients were
placed in prone position at the CT table and preparation
of sterile material as well as patient´s cleansing were
Fig 3. a) The planned access pathway for CT controlled infil-
performed in the same manner as already described for tration of the left S1; b) axial CT scan showing the correct nee-
the US-guided group. Additionally, a linear radio-opaque dle tip position within the first sacral foramen. Circle: sacral
marker was attached at the lumbosacral region of patients foramen traced by the sacral bone.
38 Michaela Plaikner et al US-guided versus CT-controlled periradicular injections of the first sacral nerve

The statistical analysis contained basic mean value


calculations including standard deviations, Pearson coef-
ficient calculation between needle repositioning and dif-
ference between pre- and post-intervention VAS scores
as well as intervention time and difference between pre-
and post-intervention VAS scores, both for CT und ul-
trasound. Further, Student`s t-test for the difference be-
tween pre- and post-intervention VAS scores of patients
undergoing CT and sonography (p-value≤0.05 estimated
as significant) was performed.
Given a standard deviation of 1 for the measure and
assuming a drop-out rate of 16%, an estimated total of 22
patients were required in each group for the study to have
a power of 90% at a 2-sided α level of 0.05.
Fig 4. Number of needed repositioning using CT- and US-guid-
Results ed infiltration to achieve a correct needle tip position.

Common data
Forty image-guided periradicular injections, 20 US-
guided (10 men and 9 women, one female patient re-
ceived an injection on both sides, 15 left and 5 right) and
20 CT-controlled (11 left, 9 right on 13 men and 7 women
were performed in 39 patients (23 male) aged between 20
to 82 years (mean age female 45±14.2; mean age male
48±15 years).
Intervention time
The mean intervention time for the US-guided treat-
ment group was 4.4±3.46 min (between 1.3-13.2 min)
and for CT-controlled treated group it was 6.5±3.03 min
(between 2.4-12.5 min), respectively.
Radiation exposure dose
Using CT as an image-guidance, the mean dose length
product (DLP) contained 25.405±32 mGy*cm (between
7-149.1 mGy*cm).
For the ultrasound-guided group the CT-based nee-
Fig 5. VAS values of all patients for CT (top) and US (bottom)
dle verification induced a DLP mean value of 8.165±4.93 group before and after the intervention and the results with nee-
mGy*cm (between 3-25 mGy*cm). dle repositioning.
Accuracy of needle tip position
Using US guidance, in 6 cases the CT-based needle mean difference between pre- and post-intervention VAS
verification revealed an initial needle position at the sec- scores (interpreted as therapeutic effect) for the CT group
ond sacral level, whereby in two cases this was observed was 4.85±2.52 and for the US group 4.55±2.74, respec-
again after the first repositioning. A repositioning of the tively. Comparing the two groups no significant differ-
needle in the CT-group was necessary in 12 cases. Fi- ence of therapeutic effect (difference between pre- and
nally, in all 40 infiltrations a correct needle tip position post-intervention VAS scores) could be found (t-test 0.7).
could be achieved. Details regarding required reposition- The flow chart in figure 5 reveals an overview of differ-
ing are listed in figure 4. The mean value of required re- ence between pre- and post-intervention VAS scores for
positioning attempts using CT-controlled infiltration was both groups regarding needle repositioning.
1.15±1.27 and applying US-guidance 0.4±0.68, respec- Before injection therapy all besides 3 patients re-
tively. ceived pain medication (NSAIDs such as ibuprofen, di-
VAS clofenac, naproxen, and/or metamizole). The used drug
In 3 cases (2 of the US group and 1 of the CT group) and the dosage were chosen by their family doctor. One
the VAS did not change; in the other 37 it decreased. The month after infiltration 21 patients (9 of the CT group
Med Ultrason 2023; 25(1): 35-41 39
and 12 from the US group) had no need of further pain guidance; however, the wrong level (S2) was initially
medications, 3 patients of the CT group only if required. addressed 6 times under US-guidance. We hypothesize
The others had reduced the use of medication. Of note, that an increased lordosis of the lumbosacral transition
5 patients (1 of the CT group, 4 of the US group) under- zone may result in a local “collapse” of the lumbosacral
went surgery within one month after the infiltration with area and induce an incorrect interpretation of the spinal
persisting pain intensity. level. Further, degenerative changes may worsen the
Underlying pathology sonographic overview. Therefore, the importance of a
The underlying pathology was in 33/40 cases (82.5%) correct placed role over a cushion underneath the lower
a disc herniation, whereby a fragmented type could be abdomen must be emphasized which seems essential for
found in 15/40 (37.5%) cases. In 11/40 cases (27.5%) a patient positioning and the definition of the correct level
herniation associated lateral stenosis and in 9/40 cases under ultrasound guidance.
(22.5%) a bony lateral recess stenosis was the causative Optionally, it can be discussed from a therapeutic
reason. point of view: it is anatomically irrelevant to catch the
Correlation analysis second rather than the first sacral foramen, as we know
Correlation analysis regarding repositioning and that a perineural spread of the applied medication reaches
mean difference between pre- and post-intervention VAS the intraspinal epidural space and therefore potentially
scores (CT group Pearson ρ=0.24, US group Pearson reaches adjacent nerve structures. This phenomenon was
ρ=0.24) was similar. As well as intervention time and the described in a preceded cadaver study [15] where an in-
difference between the VAS scores (CT group Pearson jection in the sacral spine induced a fluid dispersal along
ρ=0.18, US group Pearson ρ=0.26) showed no relevant this virtual cavity. However, this query was beyond the
effect on each other. scope of our study and should be evaluated in further
Also, when correlating the underlying pathologies, no clinical trials. Nevertheless, the injections of the S2 sa-
relevant linear associations could be found, such as discal cral foramen were obviously a mis“target” probably due
hernia to discal recessus stenosis (Pearson ρ= 0.28) or to the mentioned hyperlordosis described above. This
to fragmented type hernia (ρ = 0.36). Also, for patients was adapted during the course of this study using a roll
with discal herniation the association with the pre- and over cushion and should be implemented in every US-
post-intervention VAS scores concerning CT (ρ= 0.03) as guided injection of the sacral spine.
well as regarding US (ρ=0.24) were not significant. For Altogether using CT guidance first puncture success
patients with discal recessus stenosis the correlation to was lower and repositioning was more often required.
pre- and post-intervention VAS scores showed no signifi- This fact seems reasonable based on real-time target and
cance (ρ=0.13). It was the same for disc herniation and intervention visualization only in the case of US guided
VAS before infiltration (ρ= 0.02), for discogenic recessus interventions [18]. Once the first sacral foramen is recog-
stenosis and VAS before infiltration (ρ=0.01), for bony or nized simple needle advancement provides “live” moni-
ligamentous recessus stenosis and VAS before infiltration toring of the insertion along the entire length and path.
(ρ=0.07) and for the fragmented disc herniation and VAS On the other side, if CT-controlled imaging is used, once
before infiltration (ρ=0.1). the pathway is planned, any patient`s movement may
inevitably result in a discrepancy of the planned target
Discussion point and a correction of the inserting needle could be
necessary.
This prospective study is the first clinical trial com- As is known ultrasound is a radiation free modality:
paring US-guided versus CT-controlled infiltrations of this is an important advantage, especially if injections are
S1, evaluating accessibility, accuracy, needed interven- necessary in young adults or even more important in chil-
tion time, and the overall effect on pain relief for both dren or in cases during pregnancy. Also, the cumulative ra-
imaging methods. diation dose should not be underestimated considering that
Like previously published studies in the cervical und periradicular injections are often performed repeatedly.
lumbar spine [11,12,17] we could prove accessibility Moreover, the ultrasound technique is a bedside
and potential accuracy of US-guided periradicular injec- method and can be performed anywhere, in contrast to
tions in patients with S1 radiculopathy. In all 40 injec- the CT-technique where a patient needs to appear in a
tions accessibility was granted by a finally correct needle specialized center to undergo PRT which also provokes
position without difference between US-guided versus higher costs by in comparison limited availability.
CT-controlled periradicular injections. The number of Time to perform was also shorter when using US-
required repositioning attempts was higher using CT- guidance compared to the CT-controlled method. Of
40 Michaela Plaikner et al US-guided versus CT-controlled periradicular injections of the first sacral nerve

course, the duration of an intervention does not state final under ultrasound guidance is generally radiation free, al-
success, but patients with radiculopathy are often in pain lows for bedside therapy even in outpatients and should
and have difficulties staying in a prone position. be considered as an alternative to CT-guided injections.
No significant difference of the therapeutic effect (dif-
ference between pre- and post-intervention VAS scores) Conflict of interest: none
was found comparing the two image-based methods.
Nevertheless, problems with US-guidance may arise - as References
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Original papers Med Ultrason 2023, Vol. 25, no. 1, 42-47
DOI: 10.11152/mu-4026

What happens under the flexor tendons of the fingers in dactylitis?


Esperanza Naredo1,2, Raquel Largo2, Otto Olivas-Vergara1,2, Carmen Herencia2, Myriam
Mateos-Fernández2, Carlos Miquel García-de-Pereda-Notario3, José Ramón Mérida-Velasco3,
Gabriel Herrero-Beaumont1,2, Jorge Murillo-González3

1Department of Rheumatology. Hospital Universitario Fundación Jiménez Díaz, 2Bone and Joint Research Unit.
IIS-Fundación Jiménez Díaz- Universidad Autónoma of Madrid, 3Department of Anatomy and Embryology, Faculty
of Medicine, Universidad Complutense of Madrid, Madrid, Spain

Abstract
Aim: Tenosynovitis is one of the most frequently described inflammatory lesions in psoriatic dactylitis. The aim of the
study was to assess by ultrasound the distribution of content within the synovial sheath of the finger flexor tendons in a cadav-
eric experimental model of tenosynovitis and to describe anatomically the elements of the space between the flexor tendons
and the palmar aspect of the proximal phalanx of the fingers. Material and method: Silicone was injected under ultrasound
guidance into the digital flexor sheath of the index finger of a hand specimen. Ultrasound images of the distribution of the
filling of the flexor synovial space with the injected material were obtained. These images were compared with images from
patients with psoriatic dactylitis. The palmar regions of the hand and fingers were dissected to check the distribution of the
injected silicone in the synovial cavity. Additionally, we dissected the 2nd to 5th fingers of five cadaveric hands, including
the one used for the experiment. Results: During the injection of the substance, we observed an increasing homogeneous
hypoechoic band around the flexor tendons that differed from the images of patients. Dissection of the specimen showed the
injected silicone distributed throughout the digital flexor sheath to the distal interphalangeal joint. In addition, we provided an
illustrated anatomical description of the elements located between the flexor tendons and the palmar aspect of the proximal
phalanx, the inflammation of which could simulate flexor tenosynovitis. Conclusion: The observations of this study may
contribute to a better understanding of the anatomical structures involved in PsA dactylitis.
Keywords: ultrasound; anatomy; digital flexor sheath; dactylitis; psoriatic arthritis

Introduction consists of a variable combination of digital extra-syn-


ovial and synovial inflammatory lesions which may be
Dactylitis, defined as a diffuse swelling of a digit accompanied by intra- or periarticular proliferative and
(sausage-like digit), is a hallmark clinical feature in pso- erosive bone changes [3-7]. Among these abnormalities,
riatic arthritis (PsA) [1]. Dactylitis is also a marker of finger flexor tenosynovitis is one of the most frequently
clinical severity and joint damage development in PsA described in imaging studies of PsA dactylitis (7). On B-
[2]. On imaging, particularly on high-resolution ultra- mode ultrasound, tenosynovitis is defined as an abnor-
sound and magnetic resonance imaging (MRI), dactylitis mal anechoic and/or hypoechoic widening of the tendon
synovial sheath which can be related to both the presence
Received 30.12.2022 Accepted 30.01.2023 of tenosynovial abnormal fluid and/or hypertrophy [8].
Med Ultrason On Doppler mode, tenosynovitis can show abnormal per-
2023, Vol. 25, No 1, 42-47 itendinous Doppler signal within the synovial sheath [8].
Corresponding author: Esperanza Naredo
Department of Rheumatology and Bone and
However, other anatomical structures located between
Joint Research Unit, Hospital Universitario the flexor tendons and the phalanges, such as the vincular
Fundación Jiménez Díaz, IIS Fundación system or the attachment between the parietal synovial
Jiménez Díaz, and Universidad Autónoma layer of the digital synovial sheath and the periosteum
Av. de los Reyes Católicos, 2,
28040 Madrid, Spain
could also potentially become inflamed in PsA dactylitis
Phone: +34915504800 producing an ultrasound image of tissue inflammation
E-mail: enaredo@ser.es similar to that of tenosynovitis.
Med Ultrason 2023; 25(1): 42-47 43
The digital fibrous sheath extends from the head of model. With the dorsal surface of the hand facing down,
the metacarpals to the base of the distal phalanges. It is 5 ml of white universal silicone diluted in turpentine was
attached to the periosteum of the lateral borders of the injected slowly and progressively, using a 22-gauge nee-
proximal and middle phalanges and to the palmar liga- dle, into the proximal aspect of the digital flexor sheath
ments of the digital joints [9]. The periosteum is firmly of the index finger of the cadaveric hand, under ultra-
attached to the underlying bone by collagenous fibres, i.e. sound guidance with a LOGIQ E10 ultrasound system
Sharpey’s fibres, which pass from the superficial layer of (GE Medical Systems Ultrasound and Primary Care Di-
the periosteum to the superficial part of the bone [10]. agnostics, LLC, Wauwatosa, WI, USA) equipped with
The digital flexor sheath has a fibrous pulley system in a multifrequency linear hockey-stick transducer (L6-24
most cases composed of five annular pulleys and three MHz). B-mode frequency was set at 24 MHz, B-mode
cruciform pulleys [11]. The digital synovial sheath is lo- gain at 45 dB, and dynamic range at 63 dB.
cated inside the digital flexor sheath. It forms a transpar- Longitudinal sagittal ultrasound images of the dis-
ent, double-walled structure composed of an inner viscer- tribution of the filling of the flexor synovial space with
al layer, i.e. the epitenon, which surrounds both tendons the injected material as well as morphological changes
and an outer parietal layer which lines the inside of the caused in the sheath itself and other nearby anatomical
digital fibrous sheath. These two layers merge at their structures at the level of the proximal phalanx were ob-
proximal and distal ends to create a closed cavity with tained and recorded. These images were compared with
synovial fluid inside it [12], except in the case of the fifth some anonymized illustrative images obtained from pa-
finger in which the synovial sheath of the carpal flexor tients with PsA dactylitis in clinical practice.
tendons is prolonged around the tendons to the little finger Following the above experiment, the hand was fixed
and is usually continuous with its digital synovial sheath by immersion for 24 hours in embalming fluid. After fix-
[13]. ation, the palmar regions of the hand and palmar surfaces
The vincula are specialized mesotenon containing ar- of the fingers were dissected to check the distribution of
teries originating from four digital volar arterial arches the injected silicone in the synovial cavity of the digital
which are formed by the anastomoses of the two proper fibrous sheath of the index finger.
palmar digital arteries on each digit. From each individ- Anatomical investigation
ual arterial arch, arteries branch out, some to the bone, To anatomically evaluate the elements of the space
some to distribute into the adjacent synovial sheath, and between the flexor tendons and the proximal phalanx,
some to pass through the synovial sheath and form the we additionally dissected the 2nd to 5th fingers of five
vincula. In general, the vincula are considered to be of embalmed hands, including the one used for the above
two types. The vincula longa, more variable in arrange- experiment (four right and one left) belonging to five
ment, are filiform slips that extend to the dorsal aspect of bodies (3 males, 2 females; age of death 76 to 98 years).
the tendons [14]. The vincula breve, two in number, are a All lateral views of the dissected specimens were
more constant feature. They arise as triangular bands and prepared in the figures according to the same orientation
join near the insertions of each flexor tendon [15]. used for the ultrasound images, showing the proximal
The objectives of this proof-of-concept study were side on the left of the figure.
the following: 1) To assess by high-resolution ultrasound The study was performed following the Declaration
the distribution of increased content within the synovial of Helsinki. The corpse belonged to the Center of Do-
sheath of the flexor tendons of the fingers of a cadav- nation of Corpses, Universidad Complutense of Madrid.
eric specimen and to compare this experimental model of All local and international ethical guidelines and laws
tenosynovitis with some illustrative ultrasound findings regarding using human cadaveric donors in anatomical
detected in patients with PsA dactylitis. 2) To describe research were followed. Before death, all individuals
anatomically the elements of the space between the flex- gave written informed consent to use their donation for
or tendons and the palmar aspect of the proximal phalanx scientific purposes.
of the fingers.
Results
Material and methods
Experimental model of tenosynovitis
Experimental model of tenosynovitis Prior to the injection of silicone, the flexor tendons
A right hand specimen from a fresh-frozen human ca- were visualized, the dorsal aspect of the flexor digitorum
daver, thawed at room temperature for 12 hours (female; profundus being very close to the palmar aspect of the
age of death 76 years) was used for the experimental proximal phalanx, with a thin layer of echogenic tissue
44 Esperanza Naredo et al What happens under the flexor tendons of the fingers in dactylitis?

Fig 1. Longitudinal sagittal scan of the digital flexor tendons


at the level of the proximal phalanx of the index finger of the Fig 2. Longitudinal sagittal scan of the digital flexor tendons
cadaveric hand before the silicone injection. A thin layer of at the level of the proximal phalanx of the index finger of the
echogenic tissue between the flexor digitorum profundus and cadaveric hand after intra-sheath injection of 3 ml of silicone.
the proximal phalanx is seen (between crosses). mcp, metacar- A hypoechoic band around the flexor tendons is visualized (be-
pophalangeal joint; pp, proximal phalanx; fds, flexor digitorum tween crosses). pp, proximal phalanx; fds, flexor digitorum su-
superficialis tendon; fdp, flexor digitorum profundus tendon. perficialis tendon; fdp, flexor digitorum profundus tendon.

Fig 3. Longitudinal sagittal scan of the digital flexor tendons Fig 4. Longitudinal sagittal scan of the digital flexor tendons at
at the level of the proximal phalanx of the index finger of the the level of the metacarpophalangeal joint of the index finger of
cadaveric hand after intra-sheath injection of 5 ml of silicone. the cadaveric hand after intra-sheath injection of 5 ml of sili-
A hypoechoic band of increasing thickness around the flexor cone. The proximal synovial cul-de-sac appears distended with
tendons is visualized (between crosses). pp, proximal phalanx; hypoechoic material within it (between crosses). mch, metacar-
fds, flexor digitorum superficialis tendon; fdp, flexor digitorum pal head; fds, flexor digitorum superficialis tendon; fdp, flexor
profundus tendon. digitorum profundus tendon.

between the two anatomical structures (fig 1). During


the injection of the substance, we observed an increasing
hypoechoic band around the flexor tendons, of similar
thickness in the palmar and dorsal part of the tendons
and interposed between the dorsal tendon aspect and the
thin layer of echogenic tissue overlaying the proximal
phalanx (fig 2, fig 3). Also, the proximal synovial cul-de-
sac showed progressive hypoechoic distension during the
procedure (fig 4).
In the hand where silicone was injected into the digi-
tal flexor sheath of the index finger, dissection of the
palmar surfaces of the hand and fingers showed that the
injected silicone had been distributed to the distal inter-
phalangeal joint (fig 5).
Fig 5. Dissection of the palmar region and palmar surfaces of When comparing the experimental ultrasound im-
fingers. Note that the silicone injected into the digital fibrous
sheath of the index finger (II) has been distributed to the dis- ages with those of patients with PsA dactylitis, the lat-
tal interphalangeal joint. dfs, digital flexor sheath; pa, palmar ter showed a large hypoechoic thickening of the tissue
aponeurosis; ppda, proper palmar digital arteries. between the flexor digitorum profundus and the palmar
Med Ultrason 2023; 25(1): 42-47 45
aspect of the phalanx, in some cases with pathological
Doppler signal, with or without accompanying flexor
tenosynovitis, different from that obtained in the cadaver
(fig 6).
Anatomical investigation
Dissection of the digital flexor sheaths of all hands
studied revealed the five annular pulleys and the three
cruciform pulleys (fig 7). To visualise the space between
the flexor tendons and the palmar aspect of the proximal

Fig 7. Dissection of the digital fibrous sheaths revealing the an-


nular (A1 to A5) and cruciform (C1 to C3) pulleys in the middle
(III) and index (II) fingers. In the index finger (II) the membra-
nous portion of the digital fibrous sheath has been resected to
reveal the pulleys. The annular (A1 and A2) and oblique (O)
pulleys on the thumb (I) are also shown.

Fig 8. Anatomical preparation in which the digital fibrous


sheath has been disinserted from the lateral edge of the perios-
teum of the proximal phalanx (pp) and the flexor tendons (fds,
fdp) have been tractioned. Note the proximal synovial cul-de-
sac (arrow) as well as the parietal layer (pl) of the digital syno-
vial sheath attached to the metacarpophalangeal joint (mcp) and
the proximal phalanx (pp). III, middle finger.
Fig 6. a) Longitudinal sagittal scan of the finger flexor tendons
in patients with psoriatic dactylitis: a) extended field of view phalanx, the digital fibrous sheath was disinserted from
scan. A thick hypoechoic material is seen between the flexor
digitorum profundus and the proximal phalanx (between cross- the periosteum of the lateral borders of the proximal and
es). A minimal tenosynovitis is detected in the proximal aspect middle phalanx and from the palmar ligaments of the in-
of the tendons (arrowhead); b) A thick hypoechoic material is terphalangeal joints and the flexor tendons were pulled
seen between the flexor digitorum profundus and the proximal palmarly. The two sheets of the synovial sheath were ob-
phalanx (between crosses). A minimal tenosynovitis is detected served to continue at the proximal end to form a proximal
in the superficial aspect of the tendons (arrowheads); c) A thick
hypoechoic material is seen between the flexor digitorum pro- synovial cul-de-sac as well as the parietal sheet of the
fundus and the proximal phalanx (between crosses). A minimal synovial sheath was attached to the metacarpophalangeal
tenosynovitis is detected in the superficial aspect of the tendons joint and the palmar aspect of the proximal phalanx (fig
(arrowheads); d) A thick hypoechoic material is seen between 8). The insertion of the flexor digitorum profundus ten-
the flexor digitorum profundus and the proximal phalanx (be- don into the palmar aspect of the base of the distal pha-
tween crosses). Abnormal Doppler signal is detected deep to
the flexor tendon and intra-tendon. mcp, metacarpophalangeal lanx was verified after perforating the flexor digitorum
joint; pp, proximal phalanx; pip, proximal interphalangeal superficialis tendon. It was also visualised how the flexor
joint; ft, flexor tendons. digitorum superficialis tendon divides into two bundles
46 Esperanza Naredo et al What happens under the flexor tendons of the fingers in dactylitis?

Fig 9. a) Anatomical preparation showing the insertion of the flexor digitorum superficialis (fds) and flexor digitorum profundus
(fdp) tendons. Arrow, tendinous chiasm; b) Usual arrangement of the vinculum longum (vls) and the vinculum breve (vbs); c) The
vinculum longum (vls) and the vinculum breve (vlb) are joined by a sheet of serous tissue (arrow); d) The vinculum breve (vbs)
appears thickened, with fibroadipose tissue beneath the serous epithelium of the vinculum; e) The vinculum longum (vls) and the
vinculum breve (vbs) are thickened, with fibroadipose tissue beneath the serous epithelium of the vincula; f) Absence of vinculum
longum) (vls). II, index finger; IV, ring finger; V, little finger; dp, distal phalanx; mcp, metacarpophalangeal joint; mp, middle pha-
lanx; pp, proximal phalanx.

that delimit a leaflet; once through this, the two bundles Discussion
partially merge, i.e. tendinous chiasm, to separate again
and insert into the lateral borders of the base of the mid- For more than two decades enthesitis has been con-
dle phalanx (fig 9a). sidered the primary inflammatory lesion in PsA [16,17].
The vinculum breve of the flexor digitorum superfi- However, currently, there is little knowledge about the
cialis (VBS) was found consistently in all dissected fin- pathophysiology of PsA dactylitis, mainly due to the
gers. As usually described, the VBS was constant in this limitation in obtaining tissue from human fingers with
study. It was seen as a thin, triangular shaped, mid-line this condition. In clinical practice, ultrasound imaging
condensation of the synovial sheath which extended from of patients with PsA dactylitis frequently shows abnor-
the tendinous chiasm of the flexor digitorum superficialis mal hypoechoic material between the flexor tendons
to the adjacent proximal interphalangeal joint (fig 9b). and the proximal phalanx of disproportionately large
Sometimes the VBS was continued by a dorsal lamina thickness compared to the tenosynovitis-related disten-
with the vinculum longum of the flexor digitorum su- sion of the flexor synovial sheath in other areas of the
perficialis (VLS) (fig 9c). In one of the hands studied, same finger, or even in the absence of the latter. This
the VBS of the ring and little fingers was thickened and raises the question of possible inflammation of other re-
fibroadipose tissue was observed under the serous epithe- lated structures in the aforementioned anatomical loca-
lium of the synovial sheet (fig 9d,e). tion.
The VLS showed a higher variability than the VBS. Although previous ultrasound or MRI studies have
It was cord shaped, arose from the radial or ulnar side of described inflammatory involvement of some finger en-
the proximal phalanx and attached to one slip of the flex- theses in PsA dactylitis, such as the distal extensor en-
or digitorum superficialis just proximal to the tendinous thesis, deep flexor enthesis or the flexor pulleys [3-6],
chiasm (fig 9b). The VLS was not found in some cases inflammation of other entheses such as the parietal syno-
(fig 9f). In one case, the VLS of the index finger was vial layer attached to the periosteum of the diaphysis of
thickened and fibroadipose tissue was observed under the the phalanges or other related anatomical structures has
serous epithelium of the synovial sheet (fig 9e). not been reported to the best of our knowledge.
Med Ultrason 2023; 25(1): 42-47 47
On ultrasound, enthesitis is seen as a hypoechoic 3. Tan AL, Fukuba E, Halliday NA, Tanner SF, Emery P, McG-
thickening of the enthesis with or without abnormal onagle D. High-resolution MRI assessment of dactylitis in
Doppler signal or structural changes [18]. Thus, the ul- psoriatic arthritis shows flexor tendon pulley and sheath-
related enthesitis. Ann Rheum Dis 2015;74:185-189.
trasound image of enthesitis of the parietal synovial layer
4. Zabotti A, Idolazzi L, Batticciotto A, et al. Enthesitis of the
under the flexor tendons can be confused with that of
hands in psoriatic arthritis: an ultrasonographic perspective.
flexor tenosynovitis, an abnormality with which it can Med Ultrason 2017;19:438-443.
also coexist. The presence or absence of displacement of 5. Furlan A, Stramare R. The thickening of flexor tendons pul-
the abnormal hypoechoic material with movement of the leys: a useful ultrasonographical sign in the diagnosis of
flexor tendons can probably contribute to distinguish the psoriatic arthritis. J Ultrasound 2018;21:309-314.
intra-sheath or extra-sheath location of these lesions. 6. Tinazzi I, McGonagle D, Macchioni P, Aydin SZ. Power
Moreover, the vincula are covered by synovial tis- Doppler enhancement of accessory pulleys confirming dis-
sue [19], making them an anatomical structure with the ease localization in psoriatic dactylitis. Rheumatology (Ox-
potential for inflammation. Given their anatomical loca- ford) 2020;59:2030-2034.
tion between the flexor tendons and the phalanges, in- 7. Felbo SK, Østergaard M, Sørensen IJ, Terslev L. Which ul-
trasound lesions contribute to dactylitis in psoriatic arthritis
flammation of the vincula could produce or contribute
and their reliability in a clinical setting. Clin Rheumatol
to the grey scale and Doppler findings found in patients 2021;40:1061-1067.
with PsA dactylitis. Interestingly, the co-inflammation of 8. Naredo E, D’Agostino MA, Wakefield RJ, et al. Reliability
the enthesis of the parietal synovial layer and the vincula of a consensus-based ultrasound score for tenosynovitis in
would be consistent with the concept of synovio-enthe- rheumatoid arthritis. Ann Rheum Dis 2013;72:1328-1334.
seal involvement in PsA and spondyloarthitis introduced 9. Gajisin S, Bednarkiewicz M, Zbrodowski A. Blood supply
by McGonagle et al 15 years ago [20]. of the digital sheath. Chir Main 1998;17:147-153.
In conclusion, the observations of our study may 10. Brüel A, Christensen EI, Tranum-Jensen J, Qvortrup K,
contribute to a better understanding of the anatomical Geneser F. Geneser Histología. 4th ed. México D.F.: Edito-
structures involved in the inflammatory process in PsA rial Médica Panamericana; 2015.
11. Zancolli E, Cozzi E. Atlas de anatomía quirúrgica de la
dactylitis. Future high-resolution imaging studies in pa-
mano. 1st ed. Montevideo: Panamericana; 1992.
tients with dactylitis are warranted.
12. Verdan C, Kleinert HE. New ideas in hand flexor tendon
surgery. The sliding system. Vascularized flexor tendons
Acknowledgment. We thank General Electric transfers. 1st ed. Beglas: Aquitaine Domaine Forestier;
Healthcare, in particular Mr Fernando de la Torre (Ultra- 2001.
sound Application Sales Specialist) and Mr Luis Ortega 13. Standring S. Gray´s Anatomy E-book: The Anatomical Ba-
(Ultrasound General Manager) for their valuable techni- sis of Clinical Practice. 42th ed. Elsevier; 2021.
cal support for this study. The authors sincerely thank 14. Armenta E, Lehrman A. The vincula to the flexor tendons
those who donated their bodies to science so that anatom- of the hand. J Hand Surg Am 1980;5:127-134.
ical research could be performed. Results from such re- 15. Flindall E, McGrouther DA. Accessory roles of the vincu-
search can potentially increase mankind’s overall knowl- lum breve of the flexor digitorum profundus and check-rein
ligaments at the distal interphalangeal joint. J Hand Surg Br
edge that can then improve patient care. Therefore, these
1991;16:305-310.
donors and their families deserve our highest gratitude. 16. McGonagle D, Gibbon W, Emery P. Classification of in-
Funding: This study was partially supported by a flammatory arthritis by enthesitis. Lancet 1998;352:1137-
grant from the Instituto de Salud Carlos III, co-funded 1140.
by Fondo Europeo de Desarrollo Regional (FEDER) 17. Benjamin M, McGonagle D. The anatomical basis for dis-
[PI19/00176]. ease localisation in seronegative spondyloarthropathy at
entheses and related sites. J Anat 2001;199:503-526.
Conflict of interest: None 18. Balint PV, Terslev L, Aegerter P, et al; OMERACT Ultra-
sound Task Force members. Reliability of a consensus-
References based ultrasound definition and scoring for enthesitis in
1. McGonagle D, Tan AL, Watad A, Helliwell P. Pathophysi- spondyloarthritis and psoriatic arthritis: an OMERACT US
ology, assessment and treatment of psoriatic dactylitis. Nat initiative. Ann Rheum Dis 2018;77:1730-1735.
Rev Rheumatol 2019;15:113-122. 19. Cohen MJ, Kaplan L. Histology and ultrastructure of the hu-
2. Dubash S, Alabas OA, Michelena X, et al. Dactylitis is an man flexor tendon sheath. J Hand Surg Am 1987;12:25-29.
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ated with greater SJC, CRP, ultrasound synovitis and ero- of a “synovio-entheseal complex” and its implications for
sive damage in DMARD-naive early psoriatic arthritis. Ann understanding joint inflammation and damage in psoriatic
Rheum Dis 2022;81:490-495. arthritis and beyond. Arthritis Rheum 2007;56:2482-2491.
Original papers Med Ultrason 2023, Vol. 25, no. 1, 48-55
DOI: 10.11152/mu-3913

The value of percutaneous ultrasound-guided subacromial


bursography in the rotator cuff tears diagnosis
Ruochen Li1*, Miao Li2*, Yipeng Cui1, Pei Yang1, Chen Zhang1
* the authors share the first authorship

1Department of Orthopedics, 2Department of Ultrasound, the Second Affiliated Hospital of Xi’an Jiaotong University,
Xi’an, China

Abstract
Aim: To determine the feasibility and diagnostic value of percutaneous ultrasound-guided subacromial bursography
(PUSB) in the diagnosis of rotator cuff tears. Material and methods: Seventy-eight patients with shoulder arthroscopic
surgery and images of conventional ultrasound (US), Magnetic Resonance Imaging (MRI) and PUSB were included in this
retrospective study. The features of US, MRI and PUSB were evaluated. Results: The overall detection rate via PUSB was
significantly higher than the rates via US and MRI (96.2%, 75.6% and 82.1%, respectively), as were the detection rates for
partial-thickness tears (PTTs) (95.2%, 64.3% and 76.2%, respectively). The sensitivity and specificity of MRI, US and PUSB
in diagnosing PTTs were 90.5%, 90.5%, 100% and 98.2%, 93.0%, 100%, respectively. There was no significant difference
in the accuracy of diagnosing the full-thickness tears (FTTs) and no tears (NTs) among PUSB, US and MRI (100%, 90.5%,
90.5% and 87.5%, 86.7%, 86.7, respectively). Conclusions: It is feasible to diagnose rotator cuff tears by PUSB, which can
be used as an important supplement imaging method to evaluate rotator cuff tears.
Keywords: rotator cuff tears; ultrasound; contrast enhanced ultrasound; bursography

Introduction significantly after the age of forty, and it is around 20-


30% after the age of sixty [4]. Clinical signs and symp-
The painful shoulder or shoulder with limited move- toms that contribute to the diagnosis of rotator cuff tears
ment are very common symptoms in the general popula- include pain from overhead movement, weakness during
tion, with an incidence of 0.9-2.5% in different age groups the Jobe test or the External Rotation Resistance Strength
and a 1-year prevalence of 4.7-46.7% [1]. In musculo- test, and positive impingement sign [5,6].
skeletal pathology, the shoulder is in the third place as Rotator cuff tears must be distinguished from im-
the frequency of pain localization [2]. The shoulder pain pingement syndrome and shoulder instability [7,8].
is generally caused by rotator cuff tears and/or shoulder Shoulder X-rays and physical examinations have been
impingement syndrome (SIS) [3]. Clinically, rotator cuff shown to be inadequate in the effective detection of ro-
tears are usually divided in partial-thickness (PTTs) and tator cuff tears [9-11]. With advances in imaging tech-
full-thickness tears (FTTs) according to the thickness di- niques, ultrasound (US) and Magnetic Resonance Imag-
mension. The prevalence of rotator cuff tears increases ing (MRI) have been routinely used to assess rotator cuff
tears, which have significantly improved the accuracy in
diagnosing rotator cuff tears and in identifying different
Received 16.10.2022 Accepted 05.02.2023
Med Ultrason
causes of shoulder pain and disease staging [12]. Both
2023, Vol. 25, No 1, 48-55 US and MRI showed high soft tissue resolution, sensitiv-
Corresponding author: Chen Zhang ity, and specificity in rotator cuff pathology evaluation.
Department of Orthopedics, the Second The clinical application of MRI is limited due to its high
Affiliated Hospital of Xi’an Jiaotong
University, 710004 Xi’an, China
cost, time-consuming and contraindications. US is in-
E-mail: osteozhang@163.com creasingly widely used in the diagnosis and treatment of
Phone: 18209277651 rotator cuff injury because of its good penetration of soft
Med Ultrason 2023; 25(1): 48-55 49
tissue, real-time, dynamic imaging ability, and repeated to, equipped with a special coil for the shoulder joint.
examination of the site of interest. For coronal section scanning, the scanning plane was
Contrast-enhanced ultrasound (CEUS) is a novel US perpendicular to the glenoid cavity and ranged from the
technology based on the principle of US. Compared with acromion to subscapular humerus with a fast-spin echo
US, CEUS has more advantages, including improved spa- T2-weighted sequence (TR/TE=2200 ms/84 ms) and a
tial resolution and real-time dynamic evaluation of nor- spin echo T1 weighted sequence (TR/TE=450 ms/16
mal and abnormal tissue perfusion, imaging of large ves- ms). For oblique coronal scanning, the scanning plane
sels and microvessels, etc [13]. CEUS has also been used was parallel to the long axis of the supraspinatus muscle
for intravascular injection for urinary US examination, and ranged from the outer end of the clavicle to the ac-
detection of complications after paediatric transplanta- romion with rapid spin echo T2-weighted imaging (TR/
tion, evaluation of inflammatory bowel disease activi- TE= 2370 ms/39 ms). The scanning parameters were as
ties, and evaluation of tumour response to angiogenesis follows: a FOV = 20 cm×20 cm; a matrix =257×192; a
therapy [14]. Cheng et al [12] was the first author that layer thickness =4 mm; and a layer spacing = 4.8 mm.
used percutaneous US-guided subacromial bursography US
(PUSB) to diagnose subacromial impingement syndrome US and PUSB examinations were performed using
by injecting a contrast agent mixture into the subacro- SIEMENS ACUSON Sequoia (Siemens Medical Solu-
mial sac of SIS patients and observing its distribution tions, USA). US examination was performed with a 6-18
[12]. MHz linear array probe (18L6). The patient was seated
In our clinical practice, we observed that the MRI and facing the operator, who performs the procedure ac-
results of some patients were inconsistent with the clini- cording to the shoulder US technical guidelines recom-
cal signs and symptoms, which affected the judgment of mended by the European Society of Musculoskeletal Ra-
whether to undergo shoulder arthroscopic surgery. Also, diology [15]. The biceps long-head tendon, subscapularis
during PUSB we found that, due to the fact that the pa- tendon, supraspinatus tendon, infraspinatus and teres mi-
tients dynamically observe their own rotator cuff injury, nor tendons were examined successively. Transverse and
they better understand their condition and accept eas- longitudinal images were performed, and the dynamic
ily the medical advice. So, we collected clinical data of and static images were retained.
these patients and carried out this retrospective study to PUSB
explore the feasibility and diagnostic value of PUSB in All 78 patients underwent PUSB examination after
evaluating rotator cuff tears. initial US. First, US examination was performed to rou-
tinely scan the rotator cuff and identify the acromial glide
Materials and methods capsule clearly so that the skin puncture site could be
marked. A 2.5 mL of the SonoVue (Bracco, Italy) solu-
Patients tion was diluted with 7.5 mL of 0.9% sodium chloride.
Seventy-eight patients (32 males, 46 females, mean Then, a 4-10 MHz linear array probe (10L4) was used to
age 53.9±9.1 years; age range, 31-70 years) with shoul- perform PUSB. The tip of the needle was directed into
der arthroscopic surgery and images of conventional US, the subacromial bursa and the contrast agent was slowly
MRI and PUSB examined in our department between injected. At the same time, the probe was rotated to ob-
July 2019 to October 2021 were included in this ret- serve the distribution of contrast agent in the bursa and
rospective study. Inclusion criteria were as follows: 1) tendon. Typical images were captured and stored during
having complete clinical, US, MRI and PUSB data; 2) the inspection for recording and analysis. After the ex-
underwent shoulder arthroscopy surgery. The exclusion amination, the puncture site was disinfected and covered
criteria were: 1) having incomplete imaging data; 2) pa- with a sterile dressing.
tients unsuitable for PUSB examination; 3) patients who Diagnostic criteria
have already undergone previous surgery on the shoulder MRI: (1) Full-thickness tear: the supraspinatus ten-
area. don was thickened and twisted, with a high signal in-
The study was approved by the Ethics Committee of volving the whole layer. (2) Partial-thickness tear: the
the Second Affiliated Hospital of Xi’an Jiaotong Univer- supraspinatus tendon was irregular in shape, with a focal
sity and, being a retrospective study, the written informed high signal, and the whole layer is not involved [16,17].
consent was waived. US: (1) Full-thickness tear: (i) a hypoechoic defect
MRI extends from the bursal to the articular sides; (ii) local
MRI was performed with 1.5 T superconducting MRI defects involving both the bursal and articular sides in
equipment from the German Siemens Magnetom Avan- the short-axis and long-axis views; and (iii) the rotator
50 Ruochen Li, Miao Li et al Percutaneous US-guided subacromial bursography in the rotator cuff tears diagnosis

cuff not visible due to extensive full-thickness tears and and the location and size of defects. The diagnostic results
retraction below the acromion. (2) Partial-thickness tear: of shoulder arthroscopy were considered the standard.
(i) an obvious hypoechoic defect area or a discontinuous Statistical analysis
area on the bursal or articular sides of the tendon is pre- SPSS 18.0 (SPSS, Inc., Chicago, IL, USA) software
sent; (ii) focal hypoechoic defects within the tendon are was used for statistical data processing. The MRI, US
seen in the longitudinal and transverse planes [18]. (3) and PUSB results were correlated with the shoulder ar-
No tear (NTs): a normal subacromial-subdeltoid bursa throscopy results. The sensitivity, specificity, positive
(SASD) appeared as a hypoechoic line between two hy- predictive value, negative predictive value and accuracy
perechoic planes, with total thickness of less than 2 mm of MRI, US and PUSB in the diagnosis of rotator cuff
[12]. tears of different types were calculated, with the results
PUSB: (1) Full-thickness tear: the contrast agent of shoulder arthroscopy serving as the standard. Enu-
leaks from the defect area of the bursal side through the meration data are presented as examples, and the X2-test
supraspinatus into the articular side. (2) Partial-thickness (a=0.05, two-sided) was used to compare the difference
tear: for the part of bursal-side tears, PUSB shows that in diagnostic accuracy between different methods.
the contrast agent filled the bursal-side tear part and the
contrast agent flows from the subacromial bursa to the Results
bursal-side tears area in the PUSB dynamic imaging. For
the intratendinous or articular side partial-thickness tears, Arthroscopic diagnosis of the shoulder
the contrast agent can be observed in tendons or from The results of shoulder arthroscopy showed that there
tendons to the articular side by injecting it into the area were 21 cases of FTTs, 42 cases of PTTs and 15 cases of
of the suspected tendon lesion directly. (3) No tear: the NTs (Table I). Among the 42 patients with partial tears, 2
contrast agent is scattered only in the subacromial bursa, cases were intratendinous or articular tears, and the rest
outlines the regular surface of the rotator cuff, and does were bursal tears. Of the 15 patients without tears, 1 had
not leak into the rotator cuff. biceps head-long tendinitis with a small amount of fluid,
Image analysis 1 had low elastic tendons (accompanied by hypertension
The imaging results of US and PUSB were indepen- and diabetes), 5 had calcified supraspinatus tendons, and
dently interpreted by 2 sonographers with 10 and 8 years 8 had acromial bursitis.
of experience in musculoskeletal US. Similarly, 2 radi- Results of MRI, US and PUSB in the diagnosis of
ologists with 9 and 8 years of experience in musculoskel- rotator cuff tears
etal MRI, evaluated all images independently. When the For the 78 patients with suspected rotator cuff tears,
results were inconsistent, multidisciplinary consultation the diagnostic results of MRI, US, and PUSB for FTTs,
was conducted, and a consensus was reached. Finally, the PTTs, and NTs are shown in Table I. The diagnostic and
results of MRI, US and PUSB were compared with those predictive indexes (sensitivity, specificity, positive pre-
of arthroscopy. dictive value and negative predictive value) of these three
Shoulder arthroscopy methods for different rotator cuff tear types are shown in
All the patients underwent shoulder arthroscopy per- Table II, Table III and Table IV.
formed by an associate chief physician with more than Results of full-thickness tears
10 years of shoulder arthroscopy experience. Under ar- Among the 21 patients with full-thickness tears, the
throscopy, the types of rotator cuff tears were classified numbers of cases correctly diagnosed by MRI, US and
as full-thickness tears, partial-thickness tears and no tears PUSB were 19, 19 and 21, respectively (Table I). Both
according to whether there were any rotator cuff defects MRI and US misdiagnosed 2 patients with cases of full-

Table I. Comparison of MRI, US and PUSB in detecting rotator cuff tears with arthroscopy as standard
Arthroscopy MRI US PUSB Total
FTT PTT NT FTT PTT NT FTT PTT NT
FTT 19 2 0 19 2 0 21 0 0 21
PTT 1 32 9 4 27 11 0 40 2 42
NT 0 2 13 0 2 13 0 1 14 15
Total 20 36 22 23 31 24 21 41 16 78
US - ultrasound; MRI - magnetic resonance imaging; PUSB - percutaneous ultrasound-guided subacromial bursography; FTT - full-thick-
ness tear; PTT - partial-thickness tear; NT = no tear.
Med Ultrason 2023; 25(1): 48-55 51
Table II. Performance of MRI, US and PUSB in the diagnosis of full-thickness rotator cuff tears
Se% (95%CI) Sp% (95%CI) PPV% (95%CI) NPV% (95%CI)
MRI 90.5 (76.68,104.17) 98.2 (94.73,101.76) 95.0 (84.53,105.47) 96.6 (91.71,101.39)
US 90.5 (76.68,104.17) 93.0 (86.14,99.82) 82.6 (65.85,99.37) 96.4 (91.26,101.47)
PUSB 100 (-) 100 (-) 100 (-) 100 (-)
MRI - magnetic resonance imaging; US - ultrasound; PUSB - percutaneous ultrasound-guided subacromial bursography; CI - confidence
interval; Se - Sensitivity; Sp - Specificity; PPV - positive predictive value; NPV - negative predictive value.

Table III. Performance of MRI, US and PUSB in the diagnosis of partial-thickness rotator cuff tears
Se% (95%CI) Sp% (95%CI) PPV% (95%CI) NPV% (95%CI)
MRI 76.2 (62.76,89.62) 88.9 (78.10,99.67) 88.9 (78.10,99.67) 76.2 (62.76,89.62)
US 64.3 (49.17,79.40) 88.9 (78.10,99.67) 87.1 (74.60,99.60) 68.1 (54.25,81.92)
PUSB 95.2 (88.52,101.95) 97.2 (91.58,102.86) 97.6 (92.63,102.49) 94.6 (86,95,102.24)
MRI - magnetic resonance imaging; US - ultrasound; PUSB - percutaneous ultrasound-guided subacromial bursography; CI - confidence
interval; Se - Sensitivity; Sp - Specificity; PPV - positive predictive value; NPV - negative predictive value.

Table IV. Performance of MRI, US and PUSB in the diagnosis of no tears of rotator cuff
Se% (95%CI) Sp% (95%CI) PPV% (95%CI) NPV% (95%CI)
MRI 86.7 (67.18,106.15) 85.7 (76.83,94.60) 59.1 (36.78,81.40) 96.4 (91.41,101.44)
US 86.7 (67.18,106.15) 82.5 (72.90,92.18) 54.2 (32.67,75.66) 96.3 (91.09,101.50)
PUSB 93.3 (79.03,107.63) 96.8 (92.37,101.28) 87.5 (69.30,105.70) 98.4 (95.16,101.61)
MRI - magnetic resonance imaging; US - ultrasound; PUSB - percutaneous ultrasound-guided subacromial bursography; CI - confidence
interval; Se - Sensitivity; Sp - Specificity; PPV - positive predictive value; NPV - negative predictive value.

thickness tears as partial-thickness tears, while PUSB PUSB could show clear imaging and provide accurate
could correctly diagnose all patients with full-thickness diagnosis results.
tears (fig 1). The sensitivity of MRI, US and PUSB was
90.5%, 90.5%, 100%, respectively, and the specificity
was 98.2%, 93.0%, 100%, respectively; moreover, the
positive predictive value and negative predictive value
were 95.0%, 82.6%, 100% and 96.6%, 96.4%, 100%, re-
spectively (the 95% CI is shown in Table II).
Results of partial-thickness tears
Among 42 patients with partial-thickness tears, the
numbers of patients whose cases were correctly diag-
nosed on MRI, US and PUSB were 32, 27 and 40, re-
spectively (Table I). For the diagnosis of partial-thick-
ness tears, the sensitivity was 76.2%, 64.3%, and 95.2%,
respectively, the specificity was 88.9%, 88.9%, and 97.2%,
respectively, the positive predictive values were 88.9%,
87.1%, and 97.6%, respectively and negative predictive
values were 76.2%, 68.1%, and 94.6%, respectively (95%
CI is shown in Table III). Among them, MRI diagnosed
1 partial-thickness tear as a full-thickness tear and 9 as no Fig 1. US, MRI, PUSB, and shoulder arthroscopic images
of a 65-year-old woman with full-thickness tear: (A) US re-
tear, US diagnosed 4 partial-thickness tears as full-thick- vealed a partial-thickness tear of the supraspinatus tendon on
ness tears and 11 as no tears, and PUSB diagnosed only 2 the bursal side that did not reach the articular surface (↑); (B)
partial-thickness tears as no tears. Because these 2 partial- The T2 image of MRI indicated the presence of high signal in
thickness tears were articular partial-thickness tears, the the supraspinatus tendon (↑), which did not penetrate the whole
contrast agent couldn’t reach the area of defections due layer; (C) PUSB showed that contrast agent flowed from the
defect of the supraspinatus tendon bursal to the articular side
to the needle limitations and patient complaints of pain, (↑) and reached the articular cavity, suggesting a full-thickness
(fig 2). For the typical bursal side partial-thickness tears supraspinatus tear. (D) Arthroscopy showed a full-thickness
(fig 3) and intratendinous partial-thickness tears (fig 4), tear of the supraspinatus tendon.
52 Ruochen Li, Miao Li et al Percutaneous US-guided subacromial bursography in the rotator cuff tears diagnosis

Fig 3. A 63-year-old female with partial-thickness tear of su-


Fig 2. A 50-year-old female with partial-thickness tear of su- praspinatus on bursal side: (A) US showed that the echo of su-
praspinatus on articular side: (A) US showed that the supraspi- praspinatus tendon was not uniform, and the anechoic zone of
natus tendon bursal plane was intact (↑), and the hypoechoic 2.5×2.1 mm could be detected near synovial surface (+); (B)
zone could be detected near the articular side of the supraspi- MRI showed high signal shadow on the supraspinatus tendon
natus tendon (*); (B) MRI showed high signal shadow at the bursa (↑↑); (C) PUSB results showed that contrast agent could
articular surface of the supraspinatus tendon (↑), indicating a enter the anechoic area near the synovial surface of supraspina-
partial-thickness tear of the supraspinatus tendon on the articu- tus tendon (↑): (D) Arthroscopic results of the shoulder revealed
lar side; (C) PUSB results suggested that the contrast agent was a partial-thickness tear of the supraspinatus tendon on bursal
evenly distributed along the supraspinatus tendon on the bursal side with abundant surrounding synovial tissue hyperplasia
side after entering the subacromial bursa, and no contrast agent (**). SST = supraspinatus tendon; HH = humeral head.
was found in the supraspinatus tendon; (D) Shoulder arthros-
copy revealed a partial-thickness tear of the supraspinatus ten-
don on articular side (**). SST = supraspinatus tendon; HH =
humeral head.

Results of no tears
Among the 15 patients without tears, the numbers
of misdiagnosed cases by MRI, US and PUSB were 2,
2, and 1, respectively, and they were all misdiagnosed
as partial-thickness tears (Table I). The reason PUSB
misdiagnosed 1 NT as PTT may be that a large number
of synovial tissue hyperplasia, resulting in the pseudo-
image formation of the contrast agent during the infiltra-
tion process. For the diagnosis of no tear, the sensitivity
of MRI, US and PUSB was 86.7%, 86.7%, and 93.3%,
respectively, and the specificity was 85.7%, 82.5% and
96.8%, respectively; moreover, the positive predictive
value and negative predictive value were 59.1%, 54.2%,
87.5% and 96.4%, 96.3% and 98.4%, respectively.
The accuracy of MRI, US and PUSB in the diagnosis
Fig 4. A 31-year-old male with intratendinous partial-thickness
of rotator cuff tears tear of supraspinatus: (A) US revealed an intratendinous hypo-
Among all 78 patients, the accuracy and differences echoic area of supraspinatus tendon in the long-axis view (↑↑);
in MRI, US and PUSB for different types of rotator cuff (B) An oblique coronal MRI image revealed a brighter signal
tears are shown in Table V. The overall accuracy of MRI, within the supraspinatus tendon (↑↑); (C) PUSB image revealed
US and PUSB in the diagnosis of rotator cuff tears was contrast agent filling in the tear area within the supraspinatus
tendon (↑↑), which indicated an intratendinous partial-thickness
82.1% (64/78), 75.6% (59/78) and 96.2% (75/78), re- tear in the long-axis view; (D) Arthroscopy confirmed that an
spectively. The overall accuracy of PUSB in the diag- intratendinous partial-thickness tear (↑↑) changed to a bursal-
nosis of rotator cuff tears was higher than that of MRI side partial-thickness tear during surgical exploration.
Med Ultrason 2023; 25(1): 48-55 53
Table V. Comparison of MRI, US and PUSB in overall correct diagnosis of rotator cuff tears with arthroscopy as a standard
Method Rotator cuff, n (%) FTTs, n (%) PTTs, n (%) NTs, n (%)
MRI 64/78(82.1%) 19/21(90.5%) 32/42(76.2%) 13/15(86.7%)
US 59/78(75.6%) 19/21(90.5%) 27/42(64.3%) 13/15(86.7%)
PUSB 75/78(96.2%) 21/21(100%) 40/42(95.2%) 14/15(87.5%)
p-value <0.001 0.344 <0.05 0.997
MRI - magnetic resonance imaging; US - ultrasound; PUSB - percutaneous ultrasound-guided subacromial bursography; FTTs - full-thick-
ness tears; PTTs - partial-thickness tears; NTs - no tears; n - number of patients.

and US (p<0.001). In general, PUSB was more accurate are also limitations of PUSB; that is, only when there is
than MRI and US in the overall diagnostic rate of rotator a tear on the bursal side can the contrast agent flow from
cuff tears, and PUSB had higher diagnostic efficiency for the defect to the deep surface of the tear. When the tear is
patients with partial-thickness rotator cuff tears. small or the disease course is long, there will be a scar or
granulation tissue hyperplasia area in the defect, leading
Discussion to the failure of the contrast agent to enter and result-
ing in false negatives [27]. Therefore, it needs to be
A common cause of shoulder pain or limited move- combined with conventional US to directly inject the
ment is the rotator cuff injury, including rotator cuff ten- contrast agent into the suspected tear area. If there is
dinosis and, most common, rotator cuff tears. Patients a tear in the area, the contrast agent will easily fill it
with calcified tendonitis are also more likely to have rota- and the average total volume of contrast agent used was
tor cuff tears [19]. At present, US and MRI have been fre- 4-6 mL. On the contrary, the contrast agent cannot be
quently applied in the diagnosis of rotator cuff tears. Dif- injected into the normal tendon due to the resistance.
ferent studies have reported the accuracy of US and MRI For patients with shoulder pain or limited motion but
in different levels of FTTs and PTTs [20-22]. However, with no rotator cuff tears, US, MRI, and PUSB can be
with the progress of US technology and the widespread used to accurately diagnose such patients. Many patients,
application of contrast agents, CEUS has become an im- whose imaging findings suggest no tears or small par-
portant diagnostic method [23]. SonoVue, the contrast tial tears, suffer from severe shoulder pain symptoms and
agent used in shoulder arthrography, has been proven to limited mobility, accompanied by severe subacromial
be safe in relevant studies [24,25]. bursitis. These patients have a strong desire for surgery,
We found an overall accuracy of PUSB of 96.2% for and their main purpose for surgery is to clear the hyper-
rotator cuff tears, which was higher than that of both MRI plastic synovial tissue and relieve pain without tendon
and US (82.1% and 75.6%, respectively) (p<0.001). Roy suture.
et al [26] showed that the overall sensitivity and specifici- Currently, MRI is the preferred method for the diag-
ty of US, MRI and MRA in the diagnosis of full-thickness nosis of rotator cuff injury, followed by US, MR arthrog-
rotator cuff tears were all higher than 90%, indicating the raphy (MRA), and PUSB. Although MRA has a high di-
positive role of US, MRI and shoulder arthrography in agnostic accuracy, it is not preferred due to its complex
the diagnosis of full-thickness rotator cuff tears. In our operation and high cost [26]. Compared with invasive
study, MRI and US misdiagnosed 2 FTTs as PTTs prob- PUSB, patients are more willing to choose non-invasive
ably because the defect of the supraspinatus muscle lac- MRI examination. Therefore, MRI examination should
eration on the bursa side was large and easy to observe, be preferred for patients suspected of rotator cuff tears.
but the defect on the articular side was difficult to observe However, PUSB can be used for auxiliary diagnosis
due to the small tear range, the influence of local new when MRI examination is contraindicated, or the type of
granulation tissue and the limitation of MRI stratification tear cannot be clearly diagnosed by MRI. For surgeons,
scanning. These findings also indicate that PUSB is ad- PUSB can be used as a fast and convenient preopera-
vantageous in terms of timeliness and dynamic observa- tive supplementary examination in addition to MRI. As
tions in the diagnosis of rotator cuff tears. the most routine imaging medical diagnosis technology
For the diagnosis of partial-thickness tears, the ac- in clinic, US has the advantages of simple, cheap, and
curacy of PUSB was 95.2%, which was significantly easy to apply, especially for children, pregnant women,
higher than that of US and MRI, these findings being and patients with internal implants. The average cost of
consistent with the results of Tang et al [25]. PUSB US and PUSB is about one-third lower than that of MRI.
can assist in having a clearer and faster diagnosis of typi- Moreover, PUSB examination can dynamically under-
cal supraspinatus partial-thickness tears. However, there stand the pathological conditions of patients in real time,
54 Ruochen Li, Miao Li et al Percutaneous US-guided subacromial bursography in the rotator cuff tears diagnosis

and patients are willing to accept it during follow-up view. Part II - pathology and pathophysiology. Pol Orthop
[28]. Traumatol 2014;79:59-66.
There are still some limitations in the current research. 8. Juel NG,Natvig B. Shoulder diagnoses in secondary care, a
one year cohort. BMC Musculoskelet Disord 2014;15:89.
First, PUSB is an invasive examination, which may be
9. Liu F, Cheng X, Dong J, Zhou D, Han S,Yang Y. Compari-
associated with negative experiences in some patients,
son of MRI and MRA for the diagnosis of rotator cuff tears:
such as pain, fear, and infection. Second, in this study, A meta-analysis. Medicine (Baltimore) 2020;99:e19579.
elderly patients accounted for a large proportion of all 10. Jeong JY, Park KM, Sundar S,Yoo JC. Clinical and radio-
patients. Due to the low activity and high pain threshold logic outcome of arthroscopic rotator cuff repair: single-
of elderly individuals, tears are often serious during ex- row versus transosseous equivalent repair. J Shoulder El-
amination, while young patients usually experience acute bow Surg 2018;27:1021-1029.
trauma. At the same time, the US diagnosis of rotator cuff 11. Aaron JO. A practical guide to diagnostic imaging of the
injury is highly dependent on doctors’ experience. Taken upper extremity. Hand Clin 1993;9:347-358.
together, these factors may affect the reference impor- 12. Cheng X, Lu M, Yang X, et al. The effect of percutane-
tance of this study. ous ultrasound-guided subacromial bursography using mi-
crobubbles in the assessment of subacromial impingement
syndrome: initial experience. Eur Radiol 2015;25:2412-
Conclusions
2418.
In conclusion, PUSB is highly accurate, sensitive, 13. Cantisani V,Wilson SR. CEUS: Where are we in 2015? Eur
J Radiol 2015;84:1621-1622
and specific for the diagnosis of rotator cuff tears. At the
14. Rafailidis V, Deganello A, Watson T, Sidhu PS,Sellars ME.
same time, PUSB can be used to dynamically observe the Enhancing the role of paediatric ultrasound with micro-
rotator cuff tears in a timely manner. When patients have bubbles: a review of intravenous applications. Br J Radiol
MRI contraindications or MRI cannot accurately deter- 2017;90:20160556.
mine the types of rotator cuff tears, PUSB can be used 15. Wang J-C, Chang K-V, Wu W-T, Han D-S,Özçakar L.
for auxiliary diagnosis with decreased cost and increased Ultrasound-Guided Standard vs Dual-Target Subacromial
efficiency, making this method a good choice for patients Corticosteroid Injections for Shoulder Impingement Syn-
in urgent need of surgery. drome: A Randomized Controlled Trial. Arch Phys Med
Rehabil 2019;100:2119-2128.
Conflict of interest: none 16. Fukuda H. The management of partial-thickness tears of the
rotator cuff. J Bone Joint Surg Br 2003;85:3-11.
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Review Med Ultrason 2023, Vol. 25, no. 1, 56-65
DOI: 10.11152/mu-3490

Ultrasonography on the non-living. Current approaches.


Thomas Thomsen1, Michael Blaivas2, Paulo Sadiva3, Oliver D. Kripfgans4, Hsun-Liang
Chan5, Yi Dong6, Maria Cristina Chammas7, Beatrice Hoffmann8, Christoph F. Dietrich9,10

1Department of Internal Medicine, Westküstenkliniken, Brunsbüttel, Germany, 2University of South Carolina School

of Medicine, Columbia, South Carolina, USA, 3Department of Pathology, Faculty of Medicine, University of
São Paulo, Brazil, 4Department of Radiology, Michigan Medicine, University of Michigan, USA, 5Department of
Periodontology and Oral Medicine, School of Dentistry, University of Michigan, USA, 6Department of Ultrasound,
Zhongshan Hospital, Fudan University, Shanghai, China, 7Department of Radiology, Hospital das Clínicas – School
of Medicine, University of São Paulo, Brazil, 8Beth Israel Deaconess Medical Center, Boston MA, USA, 9Department
Allgemeine Innere Medizin (DAIM), Kliniken Hirslanden Beau Site, Salem und Permancence, Bern, Switzerland,
10Johann Wolfgang Goethe Universitätsklinik Frankfurt, Germany.

Abstract
The vast majority of clinicians associate diagnostic ultrasound with a tool that is designed for the living patient. However,
it is of course possible to apply this imaging technology to evaluate the recently deceased patient for postmortem diagnosis,
or even just examine postmortem tissue. We describe several cases in which ultrasound-enabled providers obtain answers in
postmortem examinations and discuss potential future strategies and applications. In addition, we will also illustrate the use of
sonography in minimally invasive post-mortem tissue sampling (MITS), an approach that can be used in post-mortem mini-
mally invasive autopsies as well as for establishing ultrasound diagnostic parameters in new medical fields such as periodontal
and dental implant specialties.
Keywords: postmortem ultrasound; autopsy; imaging; cause of death; validation

Introduction Clinical autopsies are important to determine a pre-


cise cause of death but have been declining worldwide
Imaging for postmortem diagnostics, for instance [2]. Several factors contributed to this shift, including
in forensic medicine, has been used since 1895, and in- increasing accuracy of modern imaging and molecular
clude conventional X-rays, computed tomography (CT) diagnostic procedures, rising costs of autopsies, cultural
and magnetic resonance imaging (MRI). Generally, ul- or religious beliefs prohibiting autopsies.
trasound (US) was never considered to be of particular Aside from macroscopic evaluations, post-mortem
value for postmortem torso imaging because of tissue gas microscopic tissue examination also has an important
formation [1]. However, as US is a readily available and role in medical diagnosis and research. Few examples are
inexpensive imaging modality, it might be of value for tissue sampling from organs that would be problematic
specific postmortem evaluations. in living patients (brain, heart, large vessels); evaluation
the effects of medical interventions, such as end-organ
lung damage as a consequence of mechanical ventilation
Received 10.08.2021 Accepted 05.10.2021
Med Ultrason
or therapeutic agents; studying oral anatomy and diseas-
2023, Vol. 25, No 1, 56-65 es by comparing imaging and histology of post-mortem
Corresponding author: Prof. Dr. Christoph F. Dietrich samples; investigating new infectious diseases; or im-
Department Allgemeine Innere Medizin (DAIM), proving the accuracy of cause of death determination in
Kliniken Hirslanden Beau Site,
Salem und Permancence, Bern, Switzerland
areas devoid of advanced diagnostic systems.
Phone: +41798347180 In this paper we review the literature published on US
E-mail: c.f.dietrich@googlemail.com postmortem examinations and we describe several cas-
Med Ultrason 2023; 25(1): 56-65 57
es in which US enabled physicians to obtain answers to choice for postmortem imaging of neonates and paediat-
open diagnostic questions in postmortem examinations. ric cadavers [3]. By contrast, Roberts et al consider CT to
In addition, we will illustrate how US can assist in mini- be the method of choice in postmortem imaging because
mally invasive post-mortem tissue sampling (MITS) and discrepancies between autopsy and MRI are more com-
how several investigators used cadavers to evaluate diag- mon than between PMCT and autopsy [8].
nostic accuracy of certain ultrasound indications. Simonds et al [9] reported on the use of conventional
radiography in cadavers to detect fractures and foreign
Review of the literature bodies, positron emission tomography to detect tissue
changes especially in Alzheimer’s disease and Lewy
A review of the available literature showed that US body dementia and various uses of CT with stationary
appears to be particularly important in fetal and neonatal and mobile equipment. The working group reported that
postmortem diagnostics [3,4]. However, overall CT and US has so far been underrepresented in cadaver diagnos-
MRI or X-ray dominate the forensic literature. Heine- tics. MRI provides excellent images, but its availability
mann et al reported on the use of postmortem CT and and expense are significant limiting factors. The vastly
CT angiography between 2004 and 2014 [5]. CT is con- superior imaging provided by MRI has placed post-
sidered the standard method in postmortem imaging. It mortem US in a subordinate status in forensic medicine,
is less susceptible to interference from postmorten gas despite cost and availability advantages. This is mainly
formation than US. The biggest advantage over clinical due to the formation of gas on the corpus after few hours
autopsy is the detection of free air. Skeletal changes and and the resultant limitation to US wave propagation in
retained foreign bodies can also often be better detected. the body.
The strength of CT angiography lies primarily in the Egger et al [10] examined 119 cadavers for gas for-
detection of bleeding sources, even in postmortem ex- mation. They found gas formation mainly in the heart
aminations that are lacking an intrinsic blood pressure. and liver. Gas was initially detectable after 5-84 hours
Agreement between postmortem CT (PMCT) and clini- after death. In all cases of natural death, gas was found in
cal autopsy is nearly 90% if the reporting radiologist has the liver vessels and the heart simultaneously; in cases of
sufficient experience in post-mortem imaging [5]. death by gas embolism, gas was noted only in the heart.
Grabherr et al [6] reported on the use of X-ray in fo- Spaienza et al [11] reported on seven victims of a flood
rensic medicine dating back to 1896, the year an X-ray whom they examined with CT for postmortem intrahe-
of a hand was performed on a mummified Egyptian prin- patic gas formation. They found that gas first formed in
cess. Today, many forensic departments have mobile X- the portal vessels and then appeared in the hepatic veins.
ray machines to examine corpuses for radiopaque foreign Fischer et al [12] analyzed intrahepatic gas formation in
bodies or bony lesions. X-rays are also used to identify five male cadavers with non-traumatic causes of death
unknown deceased with the help of dental findings or lo- using a longitudinal study with CT scans at hourly in-
cating osteosynthetic material. The most common tech- tervals over a 24 hour period. They found an increase in
niques used today are PMCT, CT angiography and MRI. gas formation between the fourth and seventh hour after
A new development is the 3-D surface scanner. Blood death, after which conditions remained constant until the
and fluids can be well visualized in CT, even postmor- end of the study period. Intrahepatic gas is predominant-
tem, using this technique. Free air is also imaged without ly caused by mesenteric gas formation [13]. Detection
difficulty. However, interpretation is complicated by gas is possible by both CT and US. The first description of
formation, which begins a few hours after death. Free air portal venous gas was made in 1955 by Wolfe et al in six
can therefore only be detected up to a few hours after newborns that had died of intestinal necrosis [14].
death. The value of CT in cases of natural death is lim- The interference by gas formation and its rapid de-
ited. For example, ischemic heart disease in acute cardiac velopment raises questions regarding what potential
arrest cannot be detected by CT without angiography [6]. significance post-mortem US could have in clinical
MRI is also used in post-mortem imaging. Limita- adult medicine. A search of the literature on this topic
tions include the occurrence of gas, lack of circulation revealed a paucity of publications to date. Duarte-Neto
and low body temperature, which influences the behavior et al [15] described ten US-guided multiorgan punctures
of MR contrast agents. Gas leads to a complete loss of in patients with COVID-19 induced death. The first pub-
signal in MR. Gases formed by autolysis can significantly lished description of this method was in 2002 by Farina
interfere with imaging. On the other hand, the detection et al [16]. They compared US-guided puncture biopsies
of myocardial infarction is as good in postmortem MRI with conventional autopsies on 100 cadavers and found
as in living patients [7]. MRI is currently the method of a concordance rate of 83% for final diagnosis. An easily
58 Thomas Thomsen et al Ultrasonography on the non-living. Current approaches.

overlooked location and timing for postmortem US per- The transducers were protected during the examination
formance is in the emergency department, where deaths with sterile probe covers from Civco Medical Solutions.
may occur suddenly and unexpectedly. Even in older, The US device and the transducers were reprocessed af-
chronically ill patients, immediate postmortem US evalu- ter use according to the local hygiene recommendations.
ations can provide vital clues as to the cause of death
and critical education to clinicians. Some catastrophic Use of US in postmortem diagnosis
etiologies can be assessed with US and include proxi-
mal thoracic aortic dissections, pericardial effusion and Case 1
pneumothorax. Abdominal aortic aneurysm presence can An 87-year-old female patient presented via para-
raise its potential role in a death, even if intraabdominal medics due to a one-day increase in dyspnea, now at
or retroperitoneal fluid is not detected. US examination rest. She denied thoracic pain, cough, fever or chills, as
so quickly after death is unlikely to be encumbered by well as sweating and palpitations. The patient had been
gas formation. Evaluation of pleural cavities is easily discharged from the geriatric ward only 5 days ago. On
performed in search of fluid collections and assessment physical examination the patient was alert and oriented,
of the lower extremity deep venous system may reveal Glasgow Coma Scale 15, reduced general status body
the presence of deep venous thrombosis, thus suggesting habitus was obese, slight bilateral leg oedema. Her res-
pulmonary embolism as a potential cause of death if the pirations were equal on both lungs, percussion sound so-
clinical scenario is supportive. However, more direct evi- norous; heart sounds were regular and rhythmic without
dence of massive pulmonary embolism is unlikely to be murmurs, rub or gallops, norm frequent. Hemoglobin
reliable as blood can quickly gel in the cardiac chambers and white blood cell count, inflammatory parameters,
and lack of intracardiac pressure means acute signs of renal values, electrolytes and urine status were unre-
right heart strain will not be identified [5]. markable. The patient was diagnosed with heart failure,
Postmortem US in the pathology department has been treated conservatively and monitored overnight. After a
used to validate US findings in 20 patients to delineate stable course, the patient was transferred to the ward the
small organ structures, e.g., the adrenal glands [17] and following day. That next evening, the patient rapidly de-
perihepatic lymph nodes [18,19]. teriorated and had to be resuscitated. Cardiac resuscita-
Recently three cases in which post-mortem US within tion was unsuccessful. A post-mortem US was performed
three hours of death enabled the clarification of a previ- given the lack of clinical diagnosis and the unsuspected
ously unclear cause of death have been reported [20]. In clinical course. There were no signs of pulmonary embo-
all three cases, an autopsy could not be performed for lism (fig 1).
various reasons. The examinations were performed with Case 2
the GE S7 (GE Medical Systems Information Technolo- A 71-year-old male undomiciled and living alone in
gies, Freiburg i. Breisgau, Germany). Multifrequency the woods is brought in by the ambulatory emergency
transducers were used: a phased array (3-5 MHz), a mul- service for decreased responsiveness. Prehospital trans-
tifrequency linear array (6-15 MHz) and a sector trans- port time was approximately 40 minutes and the patient
ducer (2-4 MHz). A Mindray M7 with a phased array expired on the way, despite aggressive and constant re-
(2-5 MHz) transducer was also utilized for evaluation. suscitative efforts by paramedics. The family and the lo-

Fig 1. Postmortem a) echocardiography, after resuscitation was stopped: right atrium slightly dilated, the other cardiac cavities are of
normal width; b) US, after resuscitation was stopped: lower caval vein of normal width and c) left femoral vein perfusion detectable
after compression.
Med Ultrason 2023; 25(1): 56-65 59
cal coroner both declined an autopsy by phone, with the
coroner planning to list the death as natural. The deceased
patient was placed in an empty patient room shortly after
EMS arrival and a point of care US was performed show-
ing an 8.1 cm abdominal aortic aneurysm with retroperi-
toneal fluid (fig 2).
Case 3
An 81-year-old patient with multiple medical comor-
bidities including prior cerebrovascular accident with
residual dysphagia, dementia was admitted to the hospi-
tal for several days of gradual decrease in mental status,
high fevers, and hypotension. The clinical team felt the
most likely diagnosis was urosepsis and started treatment Fig 2. Postmortem ultrasound, transverse scan of an abdominal
with broad-spectrum antibiotics. Her inflammatory pa- aortic aneurysm (a), with retroperitoneal fluid (b, arrow).
rameters improved, but the patient’s condition continued
to deteriorate. Five days after hospitalization the patient MIAs played a major role in COVID-19 from March
died due to cardiovascular failure. Since the exact cause 2020 up to submission of the paper and São Paulo was
of death was unclear, an immediate postmortem US was the epicenter of the present pandemic, allowing a team of
performed and clear evidence of significant pulmonary examiners to investigate more than 200 cases of a highly
artery embolism was detected (fig 3). contagious disease in an autopsy facility without level
three biosafety needs [15,24-26]. In the course of the
Use of ultrasound for minimally invasive present pandemic, over 180 autopsies were performed,
post-mortem tissue sampling including on COVID-19 patients and patients admitted
to the intensive care units for other causes. A portable
Minimally invasive post-mortem tissue sampling SonoSite M-Turbo R (Fujifilm, Bothell, WA, USA) ultra-
(MITS) may be an alternative to overcome the obstacles sound equipment with a C60x (5-2 MHz Convex) multi-
to conventional autopsy. This type of procedure has been frequency broadband transducers and DICOM® standard
employed since the mid 1930’s in Brazil, when infectious images has been used. Tissue sampling was performed
diseases were extensively studied by post-mortem tissue either using Tru-Cut semi-automatic coaxial needles of
sampling with the use of a simple viscerotome [21,22]. 14G, 20 cm long or by doing scalpel dissections guided
MITS possibilities were substantially expanded under by US, through small incisions over the area of interest
imaging guidance [23]. In 2015, one medical institution (mainly lungs and heart). Some illustrative cases are pre-
built a minimally invasive autopsy (MIA) facility com- sented.
posed of a 7T MRI, a 16 channel CT, as well as diagnos-
tic US devices (PISA project at the Faculty of Medicine, Case reports demonstrating the use of US
Universisty of São Paulo https://pisa.hc.fm.usp.br/). Over in MIAs
time, it was noted that US became the most frequently
used instrument to guide MIAs because of its low cost Case 4
and transportability, allowing the conduction of MIAs in A 71-year-old male patient with a history of HIV di-
other institutes of the medical complex [15,24,25]. agnosed in 2014 and poor adherence to anti-retroviral

Fig 3. Postmortem echocardiography, showing signs of massive acute pulmonary embolism. Subxiphoid (a) and four-chamber view (b).
60 Thomas Thomsen et al Ultrasonography on the non-living. Current approaches.

Fig 4. Lung ultrasound showing irregular, discontinuous pleural artefact, small supleural condensations and diffuses pulmonary
infiltration (a). Focus of acute pulmonary hemorrhage (hematoxylin-eosin stain, magnification 200 X) (b). Larva of Strongyloides
stercoralis in the alveolar lumen (c) (hematoxylin-eosin stain, magnification 400 X).

therapy was admitted in 2017 to investigate an episode showed marked thickening of intestinal walls. Needle
of fever, dyspnea and diarrhea. Investigation for tuber- pulmonary tissue sampling revealed foci of pulmonary
culosis was negative, but patient received treatment for hemorrhage and the presence of larvae of Strongyloides
syphilis and hepatitis B. In late 2019 the patient com- stercoralis perforating the pulmonary capillaries in the
pletely abandoned anti-retroviral therapy. Following lungs and intestinal mucosa (fig 4). The final diagnosis
medication cessation, he lost 12 kg and in October 2020 was established as systemic angioinvasive Strongyloi-
was admitted for progressive dyspnea and diarrhea. diasis in a patient with acquired immune deficiency syn-
X-ray revealed diffuse bilateral pulmonary infiltrates and drome and COVID-19 was excluded.
CT showed ground glass infiltrates with predominance Case 5
in basal portions of the lungs. The patient’s respiratory A 52-year-old female with a history of type I diabetes
status worsened, and he was intubated requiring progres- and immunosuppression due to a kidney pancreas double
sively higher levels of inspired oxygen. The patient rap- transplantation performed in 2008, now back on hemo-
idly deteriorated with worsening hemodynamic param- dialysis after renal transplant rejection, presented to the
eters despite broad-spectrum antibiotics and vasoactive hospital with progressive dyspnea and one episode of
drugs. The patient then developed massive respiratory haemorrhagic diarrhea. She eventually developed respir-
hemorrhage, which leads to cardiac arrest refractory to atory failure and was intubated and placed on mechani-
resuscitation efforts. The autopsy service received the cal ventilation. CT scans revealed bilateral ground glass
patient’s body with evident signs of weight loss. US of opacities affecting more than 50% of the lungs. RT PCR
the lungs revealed an irregular, discontinuous pleural for Sars-CoV-2 was positive in material sampled from
artefact, small supleural consolidations and diffuse pul- her trachea. She rapidly developed multiple organ failure
monary infiltration (white lung). Bowel US examination and septic shock refractory to broad-spectrum antibiot-

Fig 5. Ultrasound image showing thickened pleural line with irregularities next to areas of lung parenchyma in which is still possible
to identify A lines. Photomicrography showing alveolar septa thickening by fibrosis (arrow, hematoxylin-eosin stain, magnification
200 X) (b). Scattered epithelial cells with nuclear alterations compatible with viral infection (arrow) and foci of fibrin thrombi in
alveolar capillaries (dashed arrow, hematoxylin-eosin stain, magnification 200 X) (c).
Med Ultrason 2023; 25(1): 56-65 61
ics. During MIA, US imaging disclosed discontinuous Postmortem US imaging to establish
thickened pleural line and small sub pleural consolida- new diagnostic approaches for US use
tions. US guided Tru-Cut tissue sampling was conducted
from different organs, evidencing acute fibrin thrombi in Dental US is a virtually non-existing field except for
alveolar capillaries, fibrotic foci suggestive of organiza- research efforts. There is no widespread clinical use of
tion of previous acute pulmonary damage and rare cells US imaging technology other than for oral surgery. Im-
with aberrant nuclei, compatible with SARS-CoV-2 cy- aging technology has recently seen an increase in center
topatic effects. Final diagnosis was COVID-19 in fibro- frequency and also an increase in point of care solutions,
proliferative phase in a patient with immunosuppression i.e., smaller and more portable systems [27]. This sets
due to pancreas kidney double transplantation (fig 5). the stage for an attempt on the initiation of facilitating
Case 6 ultrasonic imaging with proper spatial resolution, practi-
A 46-year-old male was admitted due to an episode cal scan head size and meaningful clinical applications
of loss of consciousness while in the outpatient thoracic [28]. These technological advancements could be espe-
surgery offices. Family reported severe weight loss dur- cially helpful to monitor oral wound healing and evalu-
ing the preceding 4 months (14 kilograms) and the ap- ate periodontal (gum) and peri-implant tissues longitudi-
pearance of enlarged lymph nodes in the supraclavicular nally. The presented images here were recorded in human
and cervical regions. He was immediately transported cadavers and were compared to cone-beam CT (CBCT)
to the emergency ward, where he had a sudden cardiac as well as to direct caliper measurements to validate den-
arrest refractory to resuscitative efforts. Postmortem US tal US as proof of principle studies when we piloted US
images confirmed the presence of diffuse cervical lym- imaging in dentistry a few years ago. These efforts and
phadenopathy. Pulmonary images were not adequate materials significantly enhanced our understanding of
because the massive loss of weight promoted a retrac- US imaging of various anatomical structures in the oral
tion of intercostal spaces, making proper transducer ap- cavity, enabling us to comfortably scan live humans with
position on thoracic surfaces difficult. An irregular mass an off-the-shelf US imaging system at the University of
was identified in the abdomen in the area corresponding Michigan Graduate Periodontal Clinic now. The images
to the transverse colon. US guided right pneumectomy were not taken with the intent of performing an autopsy.
was performed, through a 3 cm incision in the right in- Since dental procedures currently do not involve US, it
tercostal space. Macroscopic evaluation of the resected is not surprising that forensic investigations also do not
lung showed massive pulmonary thromboembolism and involve US.
microscopic examination showed the presence of multi- Case 7
ple foci of undifferentiated adenocarcinoma in the pul- In a study in 2015 to 2016 we have investigated the
monary lymphatics (fig 6), lymph nodes and in the mass ability of US to depict soft and hard-tissue structures in
adjacent to the transversal colon. Final diagnosis was the oral cavity [29] (fig 7). A Zonare/Mindray scanner
pulmonary thromboembolism due to diffuse carcinoma- (ZS3) with off-the-shelf imaging transducers (L14-5w
tosis secondary to advanced intestinal (probably colonic) and L14-5sp) was employed for scans in human cadaver
cancer. specimens (Study ID: HUM00107975). Findings were

Fig 6. Ultrasound image of enlarged cervical lymph node (a); macroscopic view of a pulmonary embolus in a large branch of pulmo-
nary artery (embolus shown by an arrow) (b); microscopic view of pulmonary parenchyma, showing perivascular lymphatics dilated
by the presence of emboli of neoplastic epithelial cells exhibiting atypical nucleim cellular pleomorphism, organized as rudimentary
glandular acini. hematoxylin-eosin stain, 400 X magnification) (arrows points towards neoplastic emboli (c).
62 Thomas Thomsen et al Ultrasonography on the non-living. Current approaches.

Fig 7. Example for underlying curvature of the oral hard-tissue


anatomy. Ultrasonic images are composed of scattered and
reflected waves. While soft-tissue scattering is often omnidi-
rectional, reflections from hard-tissues, such as bones, roots,
crowns, are angle dependent and may require more adjustment Fig 8. Comparison of ultrasound and cone beam CT images.
and alignment to obtain satisfactory images. A second-harmonic imaging mode SH12 was used here, with
an approximately 170 µm axial resolution and 0.5 mm lateral
compared to CBCT and photographs. The intent was to resolution, assuming a f-number of 3. Displayed is tooth #9.
The employed US scanner allows for automatic speed of sound
seek US as an additional imaging modality, i.e., to com- correction. Here a Speed Index (ZSI) of 20 was selected, i.e.,
plement CBCT, X-ray and optical scans, among others, +20 m/s.
to harness the power of US soft tissue contrast and its
spatial resolution. Soft- and hard-tissue imaging is of in-
terest. While soft-tissues mostly provide omnidirectional
visualization, due to mostly angle independent scatter-
ing, hard-tissues predominantly show strong angle de-
pendence and thus require specific spatial adjustment of
the ultrasound transducer for satisfactory visualization.
In Figure 8 tooth #9 is shown by means of CBCT and
US. The former has excellent hard-tissue contrast though
lacks soft-tissue contrast. For US a second harmonic
imaging mode, i.e., SH12, was used here. The Mindray
scanner offers an optimize function/button which adjusts
the assumed speed of sound. In the presented case a speed
of sound correction of +20 m/s resulted and is indicated
as Zonare Speed Index (ZSI): 20. The overlay of the
CBCT and US in panels (c) and (d) illustrates the spatial
resolution that can be obtained with off-the-shelf imag-
ing technology. In addition, one may appreciate the soft
tissue contrast of the gingiva in panel (b), left side of the
ultrasound scan, which is not obtainable via CBCT. The
left-most thickest gingiva is 4.4 mm from the jawbone to
the epidermis. Relevance to forensics is not straightfor-
ward. But subdermal tissue changes may be visible on Fig 9. Ultrasonic visualization of the greater palatine foramen.
ultrasound and not be apparent visually or visually evi- The arrow in panel (a) points to the foramen opening located
dent yet quantified ultrasonically, both in geometry and under a mucosal soft-tissue layer. Panel (b) is the equivalent
gray scale appearance. Figure 9, shows the greater pala- cone beam CT image, where the arrow also points to the fora-
men, yet in a different image orientation. Thus, ultrasound and
tine nerve. Morphometric parameters have been defined
cone beam CT are not co-registered.
for the dimensions of the greater palatine foramen, which
differ between male and female gender [30,31]. It may to also find either gender differences or other forensic in-
therefore be possible that similar features can be found formation. It should be noted that with the introduction
for ultrasonographic assessment of the greater palatine of the L30-8 linear array by Mindray, three classes of US
Med Ultrason 2023; 25(1): 56-65 63
transducers exist that might be helpful in the oral cavity. may need to be informed about soft-tissue, so may need
At first the forward looking endocavitary probe, second to be a forensic investigator or a forensic clinician. Fig-
the sideways looking (transducer cable in the lateral di- ure 10 demonstrates how well connective tissue, muscle,
rection), often intra-operatively used, hockey stick probe, nerve, and glands can be distinguished by US. While
as well as third, the also sideways looking but transducer such is known for medical US, it has previously been
cable in the elevational direction L30-8 array. This al- a challenge in dental due to probe dimensions and spa-
lows the transducer to image sagittal, transverse and cor- tial resolution. Of note is also the observed gas bubble
onal slices in the oral cavity (fig 8, fig 9). formation in cadaver tissues. Figure 11 shows frames re-
Case 8 corded during an elevational sweep from retro-molar to
The above mentioned soft-tissue imaging qualities molar region. A significant number of bubbles are seen,
were demonstrated in a study concerned with posterior most dominantly in the muscle tissue. These might either
mandible pertinent to clinical dentistry, e.g. oral, peri- be the result of previous freezing of the specimen or are
odontal and implant surgery [32]. While oral surgeons originating from the known postmortem gas formation
during the process of decomposition [1] (fig 10, fig 11).

Discussion

We presented the use of postmortem US under very


different conditions. Postmortem US has been compared
with CT/CBCT and MRI in forensic medicine reference.
In previous studies, US was considered to be of limited
value because of gas formation due to tissue autolysis and
the regular occurrence of pneumatosis intestinalis due to
bacterial transmission [33]. The advantages of post-mor-
tem imaging include potentially valuable findings that
may help determine cause of death at low cost [34]. In
paediatrics, there are increasing reports of post-mortem
echocardiography and US after stillbirths with meaning-
ful findings [35]. In adult medicine, too, postmortem US
can yield further findings. Advantages are the ubiquitous
availability and the low organizational and financial costs
compared to CT or MRI. Postmortem gas formation in
Fig 10. Labeled soft tissue structures demonstrating the wide the abdomen and tissue maceration present known chal-
range of possible soft-tissue imaging and their locations, i.e., lenges for US. This has been described as a major limit-
as far posterior as molar. (a) Image at right maxillary molar ing factor for use of US in forensic medicine. Fetal US,
showing muscle attachement (arrow) to jawbone. (b) Image at
on the other hand, can be performed weeks postmortem
mandibular left premolar showing the mental (nerve) foramen.
without these impediments and shows good results. We
performed the first three described examinations in the
first three hours after death and found good conditions.
The last two were performed at 20 and 10 minutes after
death and also yielded valuable information that would
have otherwise been undiscovered. It was even possible
to provoke flows in the leg veins by compression. In all
cases, sonography made it possible to clarify the cause of
death. The next two examinations were performed at 20
and 10 minutes, respectively, after death and also yielded
valuable information that would have otherwise been
lost, as neither patient would have entered the hospital
nor had an autopsy. We therefore recommend that post-
Fig 11. Gas bubble or other hyperechoic formation in cadaver mortem US be performed as soon as possible after death.
tissue. Image frames shown are picked from an elevational Developments in high-frequency US as well as minia-
sweep from the left retro-molar to molar region. turization allow for visualization of regions previously
64 Thomas Thomsen et al Ultrasonography on the non-living. Current approaches.

not of interest due to poor spatial resolution or poor ac- Conflict of interest: none
cess, such as the oral cavity. The last two cases were not
recorded with the intent of autopsy, but rather technology References
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Review Med Ultrason 2023, Vol. 25, no. 1, 66-71
DOI: 10.11152/mu-3309

Role of emergency chest ultrasound in traumatic pneumothorax.


An updated meta-analysis.
Haiyan Tian1, Tong Zhang2, Yu Zhou3, Sanjay Rastogi4, Rupshikha Choudhury4,
Jawed Iqbal5

1Department of Ultrasound, The Affiliated Hospital of Inner Mongolia Medical University, Inner Mongolia, China,
2Department of Radiology, Central Hospital Affiliated to Shandong First Medical University, Lixia District, Jinan,
Shandong Province, China, 3Department of Ultrasound, Dalian Central Hospital, Dalian, Liaoning Province, China,
4Department of Oral and Maxillofacial Surgery, Regional Dental College, Guwahati, Assam, India,
5Department of Oral and Maxillofacial Surgery, Indira Gandhi Institute of Medical Sciences, Patna, Bihar, India

Abstract
Aim: To assess chest ultrasound (US) diagnostic accuracy in pneumothorax diagnosing. Material and methods: Prospec-
tive studies related to the US pneumothorax diagnostic accuracy in trauma patients were extensively searched from 2000 up
to November 2020. The studies features and findings were gathered using a standardised form and the methodological quality
of the investigations was evaluated using the Quality Assessment of Diagnostic Accuracy Studies (QUADAS-2). Results:
Twelve articles were finally chosen for quantitative analysis. The overall sensitivity of US scan in pneumothorax diagnosis
was 89% (95%CI 86-91%). Specificity was 96% (95%CI 95-97%). The diagnostic odds ratio was 193.94 (59.009-637.40) at
95%CI, thus demonstrating high chest US accuracy in pneumothorax diagnosis. Conclusion: Despite the limitations of the
included studies, this systematic review and meta-analysis concluded that chest US is a reliable method for diagnosing pneu-
mothorax in traumatized patients.
Keywords: Chest ultrasound; diagnostic accuracy; sensitivity; specificity; pneumothorax

Introduction nique involves chest X-ray if clinical examination does


not point towards thoracostomy. However, some disad-
Traumatic injuries can result in severe health conse- vantages of this method include lesser sensitivity, radia-
quences such as premature death. Chest injuries make up tion exposure and patient mobilisation [4-6].
to 25% of all trauma-induced causalities [1,2] of which Chest ultrasonography (US) has lately gained favour
pneumothorax makes up 85% of chest trauma-related for pneumothorax diagnosis since it is fast, easy to rep-
cases. Pneumothorax results in increased morbidity and licate, does not involve radiation, and allows for real-
mortality causing extended hospital stays with increased time scanning and interpretation [4,5]. Pneumothorax is
health service expenditures and decreased productivity evaluated in the parts of the chest closest to the front and
[3]. the pleural line may be clearly visible on an US scan.
Early diagnosis of pneumothorax and chest drainage Chest US has gained popularity owing to its portability,
has lifesaving consequences. The first diagnostic tech- speed, replicability and real-time scanning without the
use of radiation. It has been successfully used in diagnos-
ing pneumothorax under emergency situations with high
Received 12.07.2021 Accepted 10.12.2021
Med Ultrason
sensitivity and specificity [7,8].
2023, Vol. 25, No 1, 66-71 The purpose of this systematic review and meta-anal-
Corresponding author: Yu Zhou, MM ysis is to assess the accuracy of chest US for the early
Department of Ultrasound, diagnosis of pneumothorax in adult trauma patients.
Dalian Central Hospital,
Dalian, Liaoning Province,
Summary metrics were calculated using data from pro-
116033, China spective diagnostic accuracy trials utilizing chest US for
E-mail: zhouyu19810516@gmail.com diverse injuries.
Med Ultrason 2023; 25(1): 66-71 67
Material and methods Statistical analysis
The DerSimonian Lair approach was used to deter-
In this investigation, we followed the Preferred Re- mine pooled sensitivity, specificity, and diagnostic odds
porting Items for Systematic Reviews and Meta-Analy- ratios based on a 2x2 table. The computed diagnostic
ses (PRISMA) normative recommendations [9]. odds ratio (DOR) demonstrates the effectiveness of the
Two separate authors picked and reviewed the re- chest ultrasound capacity test to identify pneumothorax.
search, as well as extracted data and evaluated methodo- A greater DOR value suggests that the test has a higher
logical quality. Disputes were resolved via argument un- diagnostic accuracy. The Cochran Q statistic and the I2
til a consensus was achieved. When an agreement could index were also employed to assess the heterogeneity
not be achieved, the problems were handled by a third of the included studies. Forest plots were created using
author. Meta disc software, and summary ROC (SROC) curves
Data sources and search strategy (the Moses-Littenberg technique) were visually evalu-
Eligible studies were searched in MEDLINE, Em- ated for potential sources of variability.
base, Ovid, Scopus, Web of Science, and Journals on web
databases, through EBSCO. The search was conducted Results
using MeSH phrases, and open phrases were entered
into unique search strategies. The key MeSH terms em- Literature search
ployed for the search were: 1) pneumothorax; 2) chest A total of 593 research articles were retrieved using
ultrasound; 3) specificity; 4) sensitivity; 5) diagnostic electronic scanning. By reviewing titles and abstracts,
accuracy; 6) ultrasonography; and 7) chest trauma. The 386 articles were eliminated. Due to duplication, 106
search limit for literature ranged from the year 2000 up studies were removed from the total of 207. There were
until 2020 as the concluding year and published only in 39 full-text articles for final screening, with 27 being
the English language with full text was chosen for inclu- eliminated due to inclusion requirements (main reasons
sion in the study. for the exclusion being the inappropriate comparison cri-
Selection of studies teria and insufficient evidence to produce 2x2 tables for
Studies were included if they matched the following evaluation). Finally, 12 articles [11-22] were included in
criteria: prospective studies, trauma patients attending our analysis (fig 1).
emergency departments, index test – ultrasonography, Characteristics of the studies included
target injuries - pneumothorax. The results were the num- All of the investigations were carried out in a single
ber of true and false positives, as well as the number of EDs at a single location. Table I summarises the charac-
true and false negatives. teristics of the included studies.
Extraction of data Bias risk
The following data were retrieved from the entire text Individual reports reported sensitivity ranged from
of the included publications using a standardized form: 86% to 91%, while specificity ranged from 95% to 97%.
study ID, sample size, location, criteria of the condition,
ultrasound type, machine-make, and personnel involved.
All the titles and abstracts were screened independently
by the reviewers. Following detailed analysis, data was
abstracted into a data extraction table.
Endnote X8 soft ware was used to import the search
results and remove duplicates. Abstracts were screened
for eligibility criteria, and the full text was extracted
when an article was selected.
Risk of bias in individual studies
QUADAS-2 criteria evaluated risk of bias of includ-
ed studies which is a tool for assessing study quality for
meta-analysis of diagnostic accuracy [10]. It includes pa-
tient selection - random sequencing, index test - detection
of the condition, reference evaluation – comparison with
flow and timing of the study. Any disagreements in qual-
ity review by the authors were resolved by consultation
with an expert in the field. Fig 1. Flow chart diagram for article inclusion
68 Haiyan Tian et al Role of emergency chest ultrasound in traumatic pneumothorax. An updated meta-analysis.
Table I. Characteristics of studies involved
Study ID, Number of Referred for Ultrasound Ultrasound Ultrasono-
Country patients, age type-B mode machine grapher
Corsini 2018 124, Neonates with NA Philips CX50, 10-12 Neonatologist
[11], Italy. 33±5 weeks respiratory distress MHz linear transducer
Cattarosi 2016 49, Neonates with NA Prosound 𝛼7Ultrasound, Neonatologist
[12], Italy 36±5 weeks respiratory distress 13 MHz linear transducer
Mumtaz 2016 46, Trauma patients E - FAST Philips CX50. Surgical
[13], Pakistan 25±9 years 5 MHz linear transducer residents
Raimondi 2016 42, Neonates NA Prosound 𝛼7Ultrasound, Radiologist
[14], Italy 31±3.5 weeks 10 MHz linear transducer
Balesa 2015 126, Hemodynamically stable Chest US NA Radiologist
[15], India 2 months to patients
88 years age
Ziapour 2015 45, Patients with moderate FAST NA, 9.0 MHz or 3.5 Emergency
[16], Iran NA to severe trauma Convex MHz transducer physicians
Abbasi 2013 146, Stable patients inflicted FAST NA, 7.5 MHz linear Emergency
[17], Iran 37±11 years with chest trauma transducer physicians

Jalli 2013 197, Patients with respiratory NA NA, 7.5 MHz linear array Radiologist
[18], Iran NA problems probe
Hyacinthe 2012 119, Chest trauma patients NA NA, 2.5 MHz convex Emergency
[19], France 22±51 years suggested for CT transducer physicians
Zhang 2006 135, Multiple trauma FAST SSD-900, Emergency
[20], China 45±15 years 3.5 MHz convex and department
7.5 MHz linear transduce clinicians
Rowan 2002 27, Blunt chest trauma FAST NA, 7.0 MHz linear Radiologist
[21], Canada 42 years (17 to 83) transducer
Soldati 2006 185, Blunt chest trauma NA NA, 5.0 MHz transducer Emergency
[22], Italy 51+23 years convex physicians
CT, Computed Tomography; FAST, Focussed assessment with sonography in trauma; E-FAST Extended FAST; NA, not available

As a result, all of the included trials had a minimal risk of between visceral and parietal pleura [24]. The presence
bias, according to the QUADAS-2 tool (Table II). of sliding lung signs acts as an accurate negative predic-
Meta-analysis results tor for pneumothorax detection. Dulchavsky et al [24]
The overall sensitivity of US in diagnosing a pneu- found 100% true negative rate compared to conventional
mothorax was 89% (95% CI 86-91%) and the specificity chest radiographs in pneumothorax diagnosis, with sen-
96% (95% CI 95-97%). The diagnostic odds ratio was sitivity ranging from 90% to 100%.
193.94 (95% CI 59.009-637.40), indicating that chest US
is accurate in detecting pneumothorax. The SROC plot
displayed an assessment of sensitivity vs. specificity as
well as the area under the SROC curve (fig 2-4).

Discussion

In this metanalysis we found that chest US had good


diagnostic accuracy in pneumothorax diagnosis, with
89% sensitivity and 96% specificity
Chest US for pneumothorax diagnosis was reported
first in 1986 in a veterinary journal [23]. Several re-
searchers have explored its usage since then. The prin-
cipal method for diagnosing pneumothorax on chest US Fig 2. Sensitivity of chest ultrasound in diagnosis of pneumo-
employed an absent sliding lung sign in the air presence thorax patients.
Med Ultrason 2023; 25(1): 66-71 69
Table II. Risk of bias assessment for studies included
Study ID Random Allocation Blinding of Blinding of Incomplete Selective Other
sequence concealment participants outcome outcome data reporting bias
generation (selection bias) and personnel assessment (attrition bias) (reporting
(selection bias (performance bias) (detection bias) bias
Rowan [21] - - - - ? - -
Soldati [22] - - - - ? ? -
Hyacinthe [19] - - - + - - -
Abbas [17] + - - + - - -
Jalli [18] - - - - ? ? -
Balesa [15] + - - - - - ?
Ziapour [16] - - - - - - ?
Corsini [11] - - - - ? ? -
Mumtaz [13] + - - - - - ?
Raimondi [14] - - - - - - ?
Cattarosi [12] ? - - - - ? -
Zhang [20] + - - - - ? -
Low risk = -; High risk = +; Uncertain risk = ?

For identifying the pneumothorax the majority of findings are comparable, with a sensitivity of 0.89 and
studies utilized the focused assessment with sonography a specificity of 0.96. In contrast to our findings, Alrajab
for trauma (FAST) method. Standard FAST protocols as- et al [4] found that chest US had a pooled sensitivity of
sess four locations (pericardial, perihepatic, perisplenic 78.6% (95%CI 68.1-98.1%) and a pooled specificity of
and pelvis) and it is feasible and simple-to widen the 98.4% (95% CI 97.3-99.5%). Chest radiography’s pooled
scanned regions to assess the chest for haemothorax for- sensitivity and specificity were determined to be 39.8%
mally in an accurate and rapid manner [25,26]. (95% CI 29.4-50.3%) and 99.3% (95% CI 98.4-100%),
Pneumothorax diagnosis can be made based on respectively. Subgroup analysis showed that the sam-
physical examination and symptom presentation. Con- pling method, setting (trauma vs. non-trauma), operator
firmation is generally via radiography or CT scanning. type and probe were significant sources of heterogeneity.
Radiographs taken in the later stages pose difficulty in
diagnosing pneumothorax because of the patient’s condi-
tion, distance and other considerations. Also, chest radio-
graph reliability is questionable and a wrong diagnosis
may be expected in 30% of cases [21]. The met analytic
study of Ebrahimi et al [26] showed US accuracy in the
detection of pneumothorax, with a sensitivity of 0.87
(95%CI 0.81–0.92; I2=88.89; p<0.001) and specific-
ity of 0.99 (95%CI 0.98–0.99; I2=86.46, p<0.001). Our

Fig 4. In the primary analysis by pneumothorax, the summa-


ry-ROC curve showed the diagnostic accuracy of chest ultra-
sonography for traumatic pneumothorax. Individual studies are
shown by red dots. The AUC=0.9642, indicate high ultrasonog-
Fig 3. Specificity of chest ultrasound in diagnosis of pneumo- raphy accuracy in diagnosing pneumothorax, with Q*=09107
thorax patients. indicating that its sensitivity matches specificity.
70 Haiyan Tian et al Role of emergency chest ultrasound in traumatic pneumothorax. An updated meta-analysis.

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Review Med Ultrason 2023, Vol. 25, no. 1, 72-81
DOI: 10.11152/mu-3594

Diagnostic accuracy of ultrasonography for the confirmation of


endotracheal tube intubation: a systematic review and meta-analysis
Xuxia Li1, Jiapeng Zhang2, Monica Karunakaran3, Vishnu Shankar Hariharan4

1Department of Ultrasonography, Dingxi People’s Hospital of Gansu Province, Dingxi City, Gansu Province, China,
2Department of Emergency Treatment, Sisui People’s Hospital, Jining, Shangdong Province, China, 3Department of
Anaesthesia, SKS Hospital & Postgraduate Medical Institute, Salem, India, 4Department of Internal Medicine, Hindu
Mission Hospital, Chennai, India

Abstract
Aim: Despite several studies and reviews reporting data accuracy of ultrasonography for confirmation of endotracheal
intubation, there has been limited pooled evidence summarizing the diagnostic accuracy of this imaging modality, especially
based on recent evidence. Hence, the current study reviews the recent literature and conducts a meta-analysis to compare the
accuracy of ultrasonography for the confirmation of endotracheal tube placement. Material and methods: We conducted a
systematic search for all studies reporting the diagnostic accuracy of ultrasonography in the databases of Medline, EMBASE,
PubMed Central, ScienceDirect, Google Scholar & Cochrane library from inception till December 2021. Meta-analysis was
performed using STATA software “midas” package. Results: Thirty-eight studies with 3,268 participants were included. The
pooled sensitivity was 98% (95% CI, 97%-99%) and specificity was 95% (95% CI, 90%-98%), respectively. The AUC was
0.98 (95%CI: 0.96-1.00). The pooled DOR was 1090 (95% CI, 408-2910). Pooled LRP was 19 (95% CI, 9-39) and pooled
LRN was 0.02 (0.01-0.03). There was significant heterogeneity found in the outcome with significant chi-square tests and
I2 statistics > 75%. Conclusion: Findings from our review demonstrate promise in the applicability of ultrasonography as a
major diagnostic tool for confirming the endotracheal tube intubation.
Keywords: intubation; meta-analysis; ultrasonography; validation studies

Introduction Unrecognized esophageal intubation might lead to se-


rious complications, contributing to a significant number
Endotracheal intubation of critically ill patients is a of morbidity and deaths [2]. Traditional methods such as
commonly performed intervention in the emergency set- bilateral breath sounds or condensation in the endotra-
ting. Directly visualizing the endotracheal tube passing cheal tube for the confirmation of appropriate placement
through the cords is relied upon for the initial localiza- of the endotracheal tube have not been found to be re-
tion, followed by the confirmatory technique. Nonethe- liable enough for conclusively determining the location
less, direct visualization of the passage of the endotra- of the endotracheal tube [3]. Devices such as colorimet-
cheal tube might be limited during certain situations such ric capnography or end-tidal CO2 detection, requires at
as difficult intubations, making approximately 4% of the least five breaths for the confirmation. This can lead to a
emergency intubations esophageal [1]. higher risk of aspiration or gastric distention, if the en-
dotracheal tube is incorrectly placed in the esophagus.
Received 22.01.2022 Accepted 03.04.2022
In addition, the application of capnography is not reli-
Med Ultrason able in a certain group of patients, like those with recent
2023, Vol. 25, No 1, 72-81 ingestion of carbonated beverages, previous use of bag-
Corresponding author: Monica Karunakaran valve-mask or when there is paucity in the production
Department of Anaesthesia,
SKS Hospital & Postgraduate
of carbon-di-oxide (i.e., cardiac arrest) [4,5]. The use of
Medical Institute, Salem, India quantitative waveform capnography has been found to be
E-mail: kmonicacpt@gmail.com only 65-68% sensitive in the accurate detection of loca-
Med Ultrason 2023; 25(1): 72-81 73
tion of endotracheal tube during events such as cardiac “Diagnostic Accuracy Studies”. We restricted the search
arrest [6,7]. from inception of databases to December 2021 and the
The above-mentioned limitations, in combination language restriction to English only. References in the
with the higher availability, comfort with the point-of- full-text articles retrieved during the search process were
care ultrasound, have led to a large amount of research hand-searched for the identification of any relevant stud-
into the feasibility and use of ultrasonography for the ies missed during the search of databases. The detailed
confirmation of the placement of the endotracheal tube. search strategy is provided in Supplementary file 1.
Nonetheless, most of the studies had relatively smaller Study selection process
sample sizes, resulting in wide confidence intervals. Ul- It involved three stages:
trasonography is a helpful adjunct for the confirmation Stage 1: Two independent investigators (XL and VH)
of endotracheal tube placement, especially during seri- have screened title, abstract and keywords by following
ous events such as cardiac arrest or when the quantita- the search strategy. Full-texts were retrieved for the origi-
tive capnography is not readily available. However, be- nal research articles based on the inclusion criteria.
fore the routine implementation of ultrasonography, it is Stage 2: Retrieved studies were fully screened by
necessary to check the diagnostic characteristics of this the same two investigators (XL and VH) and evaluated
imaging technique. Hence, we conducted this review to against inclusion criteria. Studies that fully satisfy the
assess the diagnostic accuracy of ultrasonography for the criteria were included.
confirmation of endotracheal tube placement. Stage 3: Disagreements and differences during the se-
lection process were resolved with the help of the corre-
Material and methods sponding author (MK) and a final consensus was reached.
Data extraction and management
Eligibility criteria Data was extracted by the primary investigator (XL)
The eligibility criteria consist of studies investigating using a pre-defined form. The following information
the accuracy of ultrasonography for the confirmation of were obtained: author, publication year, study design,
endotracheal tube placement. There was no restriction in sample size, study setting, index test information, type of
terms of study design or type of participants. Only full- reference standard, study participants, quality related in-
text articles or abstracts were included while the unpub- formation, and accuracy parameters. Data entry process
lished data or studies were excluded. and management was double-checked by the set of sec-
Type of participants ondary investigators (VH, MK).
We have included studies conducted among adult pa- Risk of bias assessment in included studies
tients undergoing endotracheal intubation irrespective of Two independent authors (XL and VH) examined the
the medical conditions suffered by the participants and bias risk using the “Quality Assessment of Diagnostic
the settings in which the study was conducted. Accuracy Studies-2 (QUADAS-2)” tool [8]. The follow-
Index test ing keywords were used: “patient selection, index test,
Studies that used ultrasonography for the confirma- reference standard, and flow and timing of assessments”.
tion of endotracheal tube placement were included. Based on these keywords, grading was assessed as high,
Reference standards low and unclear for potential sources of bias.
Studies comparing ultrasonography with a standard Statistical analysis
endotracheal tube confirmatory test like end-tidal cap- Bivariate meta-analysis method was utilized to ob-
nography, colorimetric capnography, fibreoptic bron- tain the pooled sensitivity, specificity, positive likelihood
choscopy, direct visualization as the reference standard ratio (LRP), negative likelihood ratio (LRN) and diag-
were also included. nostic odds ratio (DOR) for Ultrasonography. Summary
Search strategy Receiver Operator Characteristic curves (sROC) were
A systematic search in the databases such as Med- constructed to produce the area under the curve (AUC).
line, EMBASE, PubMed Central, ScienceDirect, Google Diagnostic value can be considered to be better when the
Scholar & Cochrane library was conducted. We used both AUC value is closer to 1. The Fagan plot was utilized
the “medical subject headings (MeSH)” & “free-text to determine how much the findings on PET/CT change
words” while performing the search. The terms used in the probability that a suspected patient has a correct en-
our search strategy were as follows: “Endotracheal Intu- dotracheal tube placement. Heterogeneity was identified
bation”, “Validation Studies”, “Intubation”, “Ultrasonog- through a bivariate box plot graphically, using the chi
raphy”, “Ultrasound” “Diagnostic Imaging”, “Specific- square test for identifying statistical heterogeneity. We
ity”, “Sensitivity”, “Adults”, “Ultrasound Imaging”, and also calculated the I2 statistics to quantify the level of
74 Xuxia Li et al Diagnostic accuracy of ultrasonography for the confirmation of endotracheal tube intubation

inconsistency [9]. Publication bias was checked through


a funnel plot and the Deek’s test. The analysis was com-
pleted using STATA 14.2 (StataCorp, College Station,
TX, USA).

Results

Study selection process


In total, 896 records were identified through the liter-
ature search and 123 of them were relevant to our review
question and their full-texts were obtained. An additional
two full-texts were gained through the hand-search of
references in the retrieved full-texts. In the final stage
of screening, 38 studies with 3,268 participants were in-
cluded as per the eligibility criteria of the review (fig 1)
[10-47].
Study characteristics
All the included studies were prospective in nature.
The majority of the studies were conducted in Asian and
Middle Eastern countries such as India, China, Korea,
Iran and Turkey. The average age of the patients varied Fig 1. Search strategy.
between 38.9 and 71.5 years. We utilized data from 3,268
patients in our review to understand the accuracy of ul-
trasonography (samples sizes varied between 19 and 150
patients). The majority of the studies used capnography
as the gold standard criterion followed by auscultation
and direct visualization (Table I).
Risk of bias assessment
First, with respect to patient selection, 25 out of the
38 studies had a low bias risk. Regarding the index test
standards, 22 studies had a low risk of bias in its con-
duct & interpretation, while 22 studies had a low bias
risk with respect to patient flow and interval. Finally, 32
studies had a lower bias risk with respect to the conduct
& interpretation of the reference standard. Overall, 27
out of 38 studies had a lower bias risk as per QUADAS
results (figure 2).
Diagnostic accuracy of ultrasonography Fig 2. Quality assessment among the included studies using
The utility of ultrasonography for the confirmation of QUADAS-2 tool.
endotracheal tube intubation was reported in 38 studies.
The pooled sensitivity was 98% (95% CI, 97%-99%) and chi-square test (p<0.001) and very high I2 statistic (>
specificity was 95% (95% CI, 90%-98%), respectively 75%). This was graphically depicted through a bivariate
(fig 3). The AUC was 0.98 (95%CI: 0.96-1.00) (fig 4). box plot, which further confirmed the between-study var-
The pooled DOR was 1090 (95% CI, 408-2910). Pooled iability (Supplementary fig 1). The funnel plot indicates
LRP was 19 (95% CI, 9-39) and pooled LRN was 0.02 the possibility for the publication bias. It was also statis-
(0.01-0.03). LR scattergram revealed that both the likeli- tically confirmed by the significant Deek’s test (p=0.02)
hood measures (LRP and LRN) occupied the left upper (Supplementary fig 2).
quadrant (fig 5). Fagan’s nomogram revealed significant-
ly higher utility of PET/CT scan in the mediastinal nodal Discussion
metastasis of NSCLC (Positive=99; Negative=10%) dif-
fering significantly from the pre-test probability (86%) We assessed the accuracy of ultrasonography for con-
(fig 6). Wide heterogeneity was found with a significant firmation of endotracheal tube intubation. Following the
Table I. Characteristics of the included studies (N=38)
First author and Country Study Sample Reference standard Study location Mean Ultrasonic Transducer Esophageal
year design size age technique type intubation
(years) (%)
Abbasi 2015 Iran Prospective 120 Direct visualization + Auscultation + Emergency department 50 Dynamic/ Linear 11.7
Capnography Static
Abhishek 2017 India Prospective 100 Capnography Operating room 38.9 Static Linear 5
Adi 2013 Malaysia Prospective 107 Capnography Emergency department NR Static Linear 5.6
Afzalimoghadam Iran Prospective 90 Capnography Emergency department 59.2 Dynamic Linear 3.3
2019
Álvarez-Díaz 2015 Spain Prospective 105 Auscultation + Capnography + Operating room NR NR NR 32.3
Visualizing the chest wall
expansion + Perceiving lung
compliance in reservoir bag
Arafa 2018 Egypt Prospective 107 Capnography Operating room 41.4 Dynamic Linear 7.5
Arya 2018 USA Prospective 75 Capnography ICU 63.4 Dynamic Linear 16
Chen 2020 China Prospective 118 Direct visualization + Fibre optic ICU 71.5 Dynamic NR 10.2
bronchoscopy
Chou 2011 Taiwan Prospective 83 Capnography Emergency department 67.6 Static Curvilinear 15.7
Chou 2013 Taiwan Prospective 89 Capnography + Auscultation Emergency department 69.9 Dynamic Curvilinear 7.6
Chowdhury 2020 India Prospective 120 Capnography + Auscultation Operating room 39 Dynamic Linear 4.1
Hoffman 2014 USA Prospective 101 Direct visualization + Capnography Emergency department 58 Dynamic/ Linear 10
Static
Hosseini 2013 Iran Prospective 59 Direct visualization + Auscultation Emergency department 57 Static Curvilinear 21
Inangil 2018 Turkey Prospective 50 Capnography Operating room 42.9 Dynamic Linear 6
Kabil 2018 Egypt Prospective 40 Fibreoptic bronchoscopy ICU 55.7 Dynamic Curvilinear 10
Kad 2018 India Prospective 100 Auscultation Operating room NR Static Linear 2
Karacabey 2016 Turkey Prospective 85 Capnography Emergency department 67.2 Dynamic Linear 38.2
Khosla 2016 USA Prospective 20 Capnography + Auscultation ICU 70.5 Static Linear 5
Lahham 2017 USA Prospective 72 Capnography Emergency department 57.7 Dynamic Linear 4.2
Masoumi 2017 Iran Prospective 100 Capnography Emergency department 64.5 Static Curvilinear 6
Med Ultrason 2023; 25(1): 72-81
75
First author and
year
Country Study
design
Sample Reference standard
size
Study location Mean Ultrasonic Transducer Esophageal
age technique type intubation 76
(years) (%)
Xuxia Li et al

Men 2019 China Prospective 68 Auscultation + Operating room 60.4 Static Curvilinear 17.6
Fibre optic bronchoscopy
Milling 2007 USA Prospective 40 Auscultation + Capnography Operating room 52.5 Dynamic Curvilinear 12.5
Muslu 2011 Turkey Prospective 150 Auscultation + Capnography Operating room 40.5 Dynamic Linear 50
Noh 2012 Korea Prospective 19 Capnography Emergency department NR Dynamic Linear 15.7
Parab 2019 India Prospective 100 Fibre optic bronchoscopy Operating room 48.8 NR Linear 38.3
Park 2009 Korea Prospective 30 Auscultation + Capnography Emergency department 59.6 Dynamic Linear 10
Patil 2019 India Prospective 91 Capnography ICU NR Dynamic Linear 2
Rahmani 2017 Iran Prospective 75 Direct visualization Emergency department 61.1 Dynamic Linear 4
Ramsingh 2016 USA Prospective 42 Fibre optic bronchoscopy Operating room 45 NR Linear 35.7
Saglam 2012 Turkey Prospective 69 Capnography Emergency department NR Static Linear 7.2
Sim 2012 Taiwan Prospective 115 Chest radiography Emergency department 67.5 Dynamic NR 7.8
Sun 2014 Taiwan Prospective 96 Auscultation + Capnography Emergency department 68.8 Dynamic Curvilinear 7.3
Thomas 2017 India Prospective 100 Capnography Emergency department 50.8 Static Linear 5
Werner 2007 USA Prospective 66 Capnography + Direct visualization Operating room 38.9 Dynamic Linear 57.6
Yang 2017 China Prospective 93 Auscultation + Capnography Operating room 53.5 Static Linear 9.7
Zadel 2015 Slovenia Prospective 124 Capnography Emergency department 62.9 Static Curvilinear 2.4
Zamani 2018 Iran Prospective 100 Capnography Emergency department 57.5 Dynamic Linear 6
Zamani 2017 Iran Prospective 150 Auscultation + Direct visualization Emergency department 58.5 Static Linear 11.3
Diagnostic accuracy of ultrasonography for the confirmation of endotracheal tube intubation
Med Ultrason 2023; 25(1): 72-81 77

Fig 3. Forest plot showing pooled sensitivity and specificity

literature search, we found 38 prospective studies report-


ing the accuracy of ultrasonography. We discovered that
ultrasonography had a high level of sensitivity (98%) and
specificity (95%) for confirmation of endotracheal tube
intubation. This indicates that this imaging technique can
be used for both confirmation and exclusion of intuba-
tion among adult patients. This was further confirmed by
the findings in the LR scattergram, as both the likelihood
measures (LRN & LRP) were placed in the left upper
quadrant. The utility for clinical practice was signifi-
cantly better as the Fagan’s nomogram showed that there
was a significant increase in the post-imaging probability
compared to the pre-imaging probability.
Based on the literature available till date, it is pos-
sible to recommend ultrasonography as even the first
line tool for confirmation of endotracheal tube intubation
compared to gold standard techniques such as end-tidal
capnography, colorimetric capnography, fibreoptic bron-
choscopy, direct visualization. Previous meta-analysis
assessing the accuracy of ultrasonography revealed simi-
lar accuracy parameters compared to our review [48-52].
This shows that ultrasonography has a high amount of
applicability in the clinical practice, as it has excellent
performance with a very high specificity. Fig 4. SROC Curve
However, the application of ultrasonography or any
other alternate method as the sole technique for the de- in the endotracheal tube [52]. The confirmation of the
tection of esophageal intubation or confirmation of en- placement of endotracheal tube during intubation can be
dotracheal tube placement is not recommended. This is made either by directly scanning the anterior neck during
mainly because of the grave consequences of malposition the endotracheal tube intubation, or by indirectly looking
78 Xuxia Li et al Diagnostic accuracy of ultrasonography for the confirmation of endotracheal tube intubation

tivity with suboptimal specificity, especially among the


patients having a cardiac arrest or the low level of pul-
monary blood flow [54,55]. However, ultrasonography
has three main advantages for the airway assessment and
confirmation of endotracheal tube placement. First, the
use of ultrasonography can be done in real time, as the
endotracheal tube is passed via either the trachea or es-
ophagus. The mistakes during intubation can be easily
identified even before any ventilation begins. The second
advantage is that ultrasonography has a very high speci-
ficity for confirming the placement of endotracheal tube.
Hence, it can be used when the capnography results are
equivocal. This can reduce the unnecessary attempts for
Fig 5. Likelihood scatter gram intubation amongst the critically ill patients. Finally, the
ultrasonography can be performed even during the car-
diopulmonary resuscitation (CPR) without interrupting
the chest compressions [56].
However, future research is required to identify the
best non-invasive imaging modality that can improve
the assessment of endotracheal tube intubation and rule
out the esophageal intubation. Till all the longitudinal
research studies demonstrate a high amount of accuracy
(both sensitivity and specificity) for evaluating an intu-
bation attempt on a consistent basis, it can never replace
the AHA guidelines and become the gold standard tech-
nique. However, use of this imaging modality has been
evolving and expanding across multiple clinical facets
and might soon be integrated into a routine examination
across various areas of clinical practice.
Our review has certain strengths. Though a similar
review exists, we included a greater number of studies
and performed an updated meta-analysis with the most
recent evidence, making it the most up to date review in
the field. The majority of the studies had a lower risk of
bias, adding to the credibility of the evidence. However,
the review has certain limitations. First, significant het-
erogeneity found in our analysis might limit the ability to
infer the obtained pooled results. Secondly, the accuracy
of ultrasonography depends on several factors such as the
experience and skill of the clinicians, and the severity of
Fig 6. Fagan nomogram the condition and risk factors associated with the patients.
But, the influence of these factors cannot be assessed.
for the ventilation at pleural or diaphragmatic level, or by Despite these limitations, our review provides impor-
the combination of these techniques [52]. The commonly tant information and valuable implications for the evalu-
used methods to confirm the endotracheal tube placement ation of endotracheal tube intubation amongst adult pa-
are the observation of chest wall with chest auscultation. tients and informs that ultrasonography has the ability to
Based on the recent American Heart Association (AHA) be used as an important tool in ruling out esophageal in-
guidelines, capnography is still the gold standard crite- tubation especially in resource constrained settings. The
rion for the assessment of endotracheal intubation [53]. use of this imaging modality can aid patients by reducing
Previous reviews have also reported that the detec- significantly the time and money spent during these pro-
tion of the esophageal intubation, capnography along cedures. Another important implication is that the early
with the chest auscultation have a high level of sensi- assessment of suspected patients can help in engaging
Med Ultrason 2023; 25(1): 72-81 79
the diagnosed patients early in the effective therapeu- for emergency medicine residents to confirm tracheal tube
tic management. Further large-scale research, that have placement by ultrasound. Crit Care Shock 2019;22:1–8.
specific and longitudinal settings in nature are necessary 13. Zamani M, Esfahani MN, Joumaa I, Heydari F. Accuracy of
real-time intratracheal bedside ultrasonography and wave-
to ascertain it as a useful non-invasive modality and its
form capnography for confirmation of intubation in multi-
applicability in the standard protocol for endotracheal in-
ple trauma patients. Adv Biomed Res 2018;7:95.
tubation. 14. Kad N, Sikarwar A, Kumar V, Kumari D. A study to con-
firm the position of endotracheal tube using ultrasonogra-
Conflict of interest: none phy and standard auscultation method. Int J Contemp Med
Res 2018;5:L12–L16.
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Sirine Dehmani, Nadine Penkalla

Review Med Ultrason 2023, Vol. 25, no. 1, 82-92


DOI: 10.11152/mu-3538

Scoping Review: Ultrasonographic evidence of intraabdominal


manifestations of COVID-19 infection
Sirine Dehmani1*, Nadine Penkalla1*, Ernst Michael Jung2, Chiara De Molo3, Carla Serra3,
Beatrice Hoffmann4, Cheng Fang5, Christoph F. Dietrich1
* the authors share the first authorship

1Department Allgemeine Innere Medizin (DAIM), Kliniken Hirslanden Beau Site, Salem und Permanence, Bern,
Switzerland, 2Department of Radiology, University Medical Center Regensburg, Germany, 3Interventional,
Diagnostic and Therapeutic Ultrasound Unit, Department of Medical and Surgical Sciences, IRCCS, Azienda
Ospedaliero-Universitaria Sant’Orsola Malpighi Hospital, Bologna, Italy, 4Beth Israel Deaconess Medical Center
Boston, Harvard Medical School, Boston MA, USA, 5Department of Radiology, King’s College Hospital, London,
United Kingdom

Abstract
COVID-19 is an infectious disease caused by the novel SARS-CoV-2 coronavirus that in the majority of patients will only
cause mild symptoms. The most common serious complication is COVID-19 pneumonia, however, gastrointestinal (GI) COV-
ID-19 is also a frequent presentation and likely due to the high expression of the ACE2 receptor in the GI tract. As diagnostic
ultrasound has been frequently used in the management of this patient cohort, we conducted a literature search with the aim to
present and review the currently published evidence of using ultrasound examinations in the management of intraabdominal
manifestations of COVID-19. Our analysis showed that sonographic abnormalities of the hepatobiliary system are the most
commonly reported findings in adults, while gastrointestinal abnormalities are the most common findings in children. The
most severe complications are related to thromboembolic complications in the intensive care unit.
Keywords: SARS-COV-2; COVID-19; gastrointestinal; liver; spleen; kidney

Introduction been infected and over 3 million people have died from
COVID-19 by the end of 2021 [2]. Typical symptoms
We are confronted with of a global pandemic caused of the disease include dry cough and dyspnea, as well
by the severe acute respiratory syndrome coronavirus as fever and fatigue [3-5]. Severe infection of the lungs,
2 (Sars-CoV-2). The clinical manifestation from Sars- which progresses to ARDS, occurs in up to 12% of hos-
CoV-2 infection known as COVID-19 disease may be pitalized patients and most cases require intensive care
asymptomatic or mild, but can lead to severe form COV- [6]. In this population, lung ultrasound (US) has been
ID-19 with multi-organ involvement and death [1]. Since frequently used because it is readily available at bedside,
the beginning of its outbreak in Wuhan, China, in De- and has high diagnostic accuracy for a number of condi-
cember 2019, over 170 million people worldwide have tions without the use of intravenous iodinated contrast
agent [5,7-13]. Typical US signs of pneumonia and acute
respiratory distress syndrome (ARDS) in the course of
Received 29.09.2021 Accepted 11.11.2021
Med Ultrason
COVID-19 were described. These included thickened and
2023, Vol. 25, No 1, 82-92 irregular pleural lines, B-lines as well as sub pleural con-
Corresponding author: Prof. Dr. med. Christoph F. Dietrich solidations with or without air bronchogram [7,14,15].
Department Allgemeine Innere Medizin (DAIM), Pathophysiological mechanisms of COVID-19 appear to
Kliniken Hirslanden Beau-Site,
Salem und Permancence, Bern, Switzerland
involve immunological, vascular and prothrombotic fac-
Phone: +41 76 440 81 50 tors which lead to endothelial damage and thrombosis in
E-mail: c.f.dietrich@googlemail.com the context of a cytokine storm, accompanied by remod-
Med Ultrason 2023; 25(1): 82-92 83
eling of the vascular tissue and resulting hypoperfusion Results
play a crucial role [16-18].
However, COVID-19 is not limited to the respiratory The review comprised a total of 39 publications in-
tract with emerging evidences suggest it rather represents cluding two prospective and four retrospective studies,
a systemic disease with a variety of clinical manifestations as well as several single or multiple case reports. In to-
[19]. Up to 50% of children as well as adults have been tal, data of 175 patients were analyzed. The diagnosis of
shown to experience gastrointestinal (GI) symptoms, COVID-19 was confirmed in all patients with reverse-
which include diarrhea, nausea, vomiting, anorexia, and transcription polymerase chain reaction (RT-PCT). The
abdominal pain [20]. GI symptoms might precede other mean age was 27 years (range: 2 months - 78 years) and
symptoms or even be the only manifestation of the dis- about 90% of patients were male. All patients received an
ease, and thus can complicate the diagnostic process [21- abdominal US. Out of 138 patients with available infor-
23]. Involvement of the hepatobiliary system in COV- mation, 96 patients (70%) showed abdominal symptoms.
ID-19 may lead to abnormal liver function testing in up Notably, multiple patients experienced these prior to any
to 76% of hospitalized patients, regardless of preexisting respiratory complaints. In single and multiple case stud-
hepatic conditions. It can be accompanied by symptoms ies, there was a correlation of symptoms and US find-
of hepatitis or acute hepatic failure, especially during in- ings. In the prospective and retrospective trials, a clear
tensive care therapy [24,25]. Furthermore, involvement correlation between US and clinical findings was not as
of the pancreas has been reported in up to 17% of cases clearly found.
ranging from asymptomatic elevation of serum amylase Gastrointestinal tract
to fulminant pancreatitis [26,27]. Moreover, acute or Overall we found that unspecific GI abnormalities
acute on chronic failure of renal function was observed detected by US were frequently reported, especially for
in both children and adults in up to 46% of cases [28,29]. children. We found 8 cases of ileocolic intussusception in
Symptoms comprise hematuria, proteinuria, but also ol- infants up to ten months of age, hereof one with necrosis
iguria and anuria and are most likely the result of immu- of the intestine. US examinations showing ileocolic in-
nological and micro thrombotic phenomena [29]. Final- tussusception reported typical findings such as “telescop-
ly, the lymphatic tissue and spleen may also be affected ing of bowl into bowl”, “doughnut sign” or a “swirl” of
causing unspecific abdominal complaints and has been the intestines with layers of different echogenicity [33-
detected in children diagnosed with COVID-19 [30,31]. 39] (fig 1). One case of pediatric intestinal necrosis pre-
While US is usually a well-established imaging meth- sented with a significant amount of free intraperitoneal
od for abdominal complaints, data concerning abdominal fluid on examination [40].
manifestation of COVID-19 appear scarce [7,32]. There- A single center study enrolling 44 patients with mul-
fore, our aim is to review and summarize the results of tisystem inflammatory syndrome in children (MIS-C) re-
existing published data and to identify specific sono- lated to COVID-19 described US findings of thickened
graphic findings facilitating the diagnosis of abdominal
COVID-19.

Methods

The Electronic Databases PubMed, Cochrane library


and Google scholar were systematically searched. The
MeSH key words used were “SARS-COV-2”, “COV-
ID-19”, “ultrasound”,”ultrasonography”, “extrapulmo-
nary”, “abdominal”, “gastrointestinal”, “hepatic”, “bil-
iary”, “pancreatic”, “splenic” and “renal” to identify
publications related to gastrointestinal and abdominal
(extra pulmonary) ultrasonographic findings of COV-
ID-19. We included all types of clinical prospective and
retrospective studies and single or multiple case studies.
There was no restriction on age or gender for the search. Fig 1. A 42 years old man diagnosed with SARS-CoV2 and se-
vere respiratory symptoms, abdominal pain and diarrhea treated
Clinical symptoms and results of US had to be stated in in the intensive care unit. “Doughnut sign” or a “swirl” of the
the article; otherwise we excluded the publication from intestines with layers of different echogenicity typical of transi-
the analysis (table 1). tory intussusception often seen in diarrhea.
84 Sirine Dehmani, Nadine Penkalla et al Scoping Review: US evidence of intraabdominal manifestations of COVID-19 infection

Overview of ultrasonographic and clinical findings concerning abdominal manifestation of COVID-19


Publication N Age Results of ultrasonography Clinical Diagnosis
symptoms
Abd. Resp.
Gastrointestinal tract
Ahtamnah [33] 1 2 mo Target sign of bowl Yes No Ileocolic intussusception
Bazuaye-Ekwuyasi [38] 1 9 mo Concentric alternating echogenic and hypoechoic Yes Yes Ileocolic intussusception
bands (target sign)
Cabrero-Hernández [45] 3 9-12 y Signs of ileitis and colitis, intestinal inflammation Yes Yes PIMS-TS
Cai [40] 1 10 mo Free intraperitoneal liquid Yes Yes Ileocecal intussusception
with necrosis
Carducci [44] 2 13 y Widespread thickening of distal small intestine, Yes Yes PIMS-TS
14 y small amount of ascites
Ekbatani [41] 2 10 y Acute appendicitis, multiple reactive mesenteric Yes Yes Acute appendicitis
4y lymph nodes
Gutierrez-Jimeno [42] 1 13 y Thickened appendix with destructured layers Yes No MIS-C with acute
appendicitis
Hameed [31] 18 1-17y 37% echogenic expanded mesenteric fat Yes Yes MIS-C
21% bowl wall thickening
Ibrahim [47] 1 33 y Dilatated fluid-filled intestinal loops in left lower Yes Yes Paralytic Ileus of large
quadrant intestine
Kangas-Dick [46] 1 74 y Free intraperitoneal liquid Yes Yes Upper gastrointestinal
perforation
Makrinioti [35] 2 10 mo Signs of ileocolic intussusception not further Yes Yes Ileocolic intussusception
specified
Martinez-Castano [36] 1 8 mo “Swirl” of intestines with alternating hyper- and Yes Yes Ileocolic intussusception
hypoechogenic layers
Miller [30] 12 NA 16.7% thickened intestine in right upper quadrant Yes Yes MIS-C
8.3% prominent appendix vermiformis
Moazzam [37] 1 4 mo Telescoping of bowl into bowl with doughnut Yes Yes Ileocolic intussusception
sign in right upper quadrant
Morparia [43] 1 11 y Non-compressible, dilated appendix Yes No MIS-C with acute
appendicitis
Rajalakshmi [39] 1 6 mo Signs of ileocolic intussusception not further Yes No Ileocolic intussusception
specified
Hepatobiliary tract
Abeysekera [60] 1 42 y No flow detectable in portal vein Yes Yes Thrombosis of portal
vein
Bhayana [58] 37 NA 54% dilatation of gallbladder with sludge NA NA NA
5.4% thickening of gallbladder wall
2.7% liquid in gallbladder base
2.7% gas in portal vein
Blumfield [49] 8 1-20y 75% Hepatomegaly, ascites Yes Yes MIS-C
Culver [51] 1 71 y Massive amount of free intraperitoneal liquid Yes Yes Acute hepatic
decompensation, Ascites
Sars-CoV-2-positive
Dane [59] 1 NA Thrombosis of portal vein tree NA NA Hypercoagulability
Effenberger [54] 32 NA 50% increased liver stiffness in elastography Yes Yes Acute hepatitis
Hameed [31] 18 1-17y 53% ascites Yes Yes MIS-C
16% periportal echogenicity, pericholecystic
edema, mild gallbladder wall thickening and
gallbladder sludge
11% mild hepatomegaly
Hassani [57] 1 65 y Increased gallbladder wall thickness Yes Yes Acute cholecystitis

Lamazou [53] 1 35 y Sludge in gallbladder with no signs of inflamma- Yes Yes Liver cytolysis
tion
Mieczkowska [52] 1 43 y Hepatomegaly, hepatic steatosis and trace per- Yes Yes Multisystemic
icholecystic fluid inflammation syndrome
Med Ultrason 2023; 25(1): 82-92 85
Publication N Age Results of ultrasonography Clinical Diagnosis
symptoms
Abd. Resp.
Miller [30] 12 NA 25% thickened gallbladder wall Yes Yes MIS-C
25% sludge in gallbladder
25% ascites
8.3% heterogenous coarse parenchyma of liver
without focal lesion
8.3% hepatomegaly with normal parenchyma and
vascularity
Paz [62] 1 14 y Biliary sludge, distended gallbladder with diffuse Yes No Acute pancreatitis
wall thickening, surrounding free fluid, meteorism
Tirumani [55] 4 NA 50% signs of hepatitis not further specified NA NA NA
25% sludge in gallbladder
Ying [56] 1 68 y Ultrasound-guided percutaneous transhepatic Yes Yes Acute cholecystitis
gallbladder drainage PCR negative from bile
Alloway [63] 1 7y Diffuse pancreatic enlargement and Yes No Necrotizing pancreatitis
heterogeneous pancreatic echogenicity
Pancreas
Dietrich [21] 1 72 y Cholecystolithiasis without signs of obstruction, Yes Yes Acute pancreatitis
inhomogeneous pancreas
Hadi [64] 2 47y Diffuse increase in pancreatic volume without Yes Yes Acute pancreatitis
68 y focal lesions or gallstones
Signs of acute pancreatitis not further specified
Samies [61] 1 16 y Mild hepatomegaly, one gallstone, prominent Yes No Acute pancreatitis
pancreatic head, tail and duct
Renal and urinary tact
Berteloot [65] 7 3-17 y Spectral Doppler: stenosis of renal artery, No No Immune postviral vas-
increased peak systolic velocity culitis in renal graft after
transplant
Blumfield [49] 8 1-20y 63% hyperechogenic kidneys Yes Yes MIS-C
13% urinary bladder wall thickening
Fogagnolo [66] 15 55-69 Doppler: increased renal resistance index, Yes Yes Acute kidney injury in
y 71% not continuous venous flow 53%
Gopalakrishna [70] 1 49 y Slightly echogenic kidneys Yes Yes Acute kidney injury
Jung [67] 5 51-74 Color Doppler: increased renal resistance index Yes Yes Acute or acute on
y CEUS: segmental infarction 20%, partially chronic kidney disease
reduced cortical microcirculation
Hameed [31] 18 1-17y 5.5% echogenic kidneys Yes Yes MIS-C
Tancredi [69] 1 38 y Increased renal parenchymal echogenicity Yes Yes Acute kidney injury
Color Doppler: decreased global signal, elevated
resistance indices
Tirumani [55] 1 38 y 25% increased renal cortical echogenicity Yes Yes NA
Tuma [68] 1 78 y Echo-dense and enlarged kidneys with high Yes Yes Acute kidney injury
resistance indices (>0.8)
CEUS: delayed renal perfusion
Spleen and lymphatic system
Blumfield [30] 8 1-20 y 13% splenomegaly Yes Yes MIS-C
Hameed [31] 18 1-17 y 47% enlarged lymph nodes Yes Yes MIS-C
11% borderline splenomegaly, subcortical and
hypoechoic splenic lesions
Harwood [71] 2 14 y Mesenteric adenitis Yes Yes PIMS-TS
Miller [30] 12 NA 16.7% mesenterial lymphadenopathy in right Yes Yes MIS-C
hemiabdomen
N: Number of cases; Abd.: Abdominal; Resp.: Respiratory; PIMS-TS: Pediatric Inflammatory Multisystem Syndrome temporally associated
with SARS-CoV-2-infection; MIS-C: Multisystemic inflammatory syndrome in children; NA: not available
86 Sirine Dehmani, Nadine Penkalla et al Scoping Review: US evidence of intraabdominal manifestations of COVID-19 infection

Fig 2. A 39 years old patient with severe symptoms of a COVID-19 infection. Slight thickening of the descending colon (a), mesen-
terial lymphadenopathy (b) and pronounced appendix (c) are shown.

intestinal walls within the right upper quadrant in 16.7% and ascites and 38% presenting with a thickened gall-
and a prominent appendix vermiformis in 8.3% of their bladder wall [49]. Meanwhile, evidence of hepatobiliary
participants [30] (fig 2). US evidence of appendicitis in manifestation of COVID-19 is frequently reported in
three more cases was reported in children with non-spe- adult patients. A retrospective study of 30 ICU patients
cific malaise due to COVID-19 [41-43]. revealed solitary hepatomegaly in 56% of their patients
More general signs of inflammation concerning the [50]. Acute hepatic decompensation was found to be
small and large intestines, such as bowel wall thickening diagnosed in cases with and without preexisting liver
or fluid surrounding the loops were reported in children conditions. However, one single case study of an elderly
presenting with generalized illness, abdominal symptoms male patient with liver cirrhosis Child-Pugh-B showed
or acute abdomen as a part of the Pediatric Inflamma- massive new ascites and RT-PCR of the fluid was posi-
tory Multisystem Syndrome temporally associated with tive for Sars-CoV-2 [51]. Particularly in cases of severe
SARS-CoV-2 infection (PIMS-TS) [31,44,45]. Two case COVID-19, the risk of acute liver injury appears to be
reports showed US findings of gastrointestinal involve- increased [52,53]. As acute liver injury is associated with
ment in critically ill adult males with COVID-19. One increasing liver stiffness and elevated liver enzymes,
case showed a significant amount of free intraperitoneal an association between these two measures and disease
fluid that was later identified as enteric content due to severity could be found in COVID-19 [54]. Moreover,
upper GI perforation [46]. The other case showed signs several investigators reported patients with US signs of
of an ileus such as dilatation of multiple fluid-filled bowl hepatobiliary tract inflammation. A retrospective study on
loops in a patient requiring intensive care [47]. 73 patients with COVID-19 described non-specific signs
Hepatobiliary tract of hepatitis in 50% and gallbladder sludge in 25% of the
Hepatic laboratory anomalies are often observed in patients. Interestingly, the bowel abnormalities were the
SARS-CoV-2 infection [48]. Hepatobiliary abnormalities most frequent finding in the abdomen, but the majority
on US of children were so far only described in MIS-C. of patients had no abdominal complaints. GI findings ap-
According to Miller et al, 25% of children with MIS-C peared independent of the severity of pulmonary involve-
presented with a thickened gallbladder wall and sludge ment or laboratory markers [55]. Two other case reports
on US. Another 8.3% showed either parenchymatous ab- of US findings of acute cholecystitis showed increased
normalities of the liver without specific lesions or liver gallbladder wall thickness and one required percutane-
enlargement with normal liver echo texture and vascu- ous transhepatic gallbladder drainage with uS guidance
lature. Presence of any abdominal symptoms was docu- [56,57]. Gallbladder dilatation and sludge were further
mented in 84% of the included cases [30]. Hameed et al reported in 54% of patients of a retrospective cross-sec-
revealed significant ascites in 53% of the included chil- tional study of 134 patients. Within the same population,
dren with MIS-C and 16% were reported to have biliary 27% of participants presented with a fatty liver and 2.7%
abnormalities such as gallbladder sludge or wall thick- revealed a thickened gallbladder wall or fluid surround-
ening, pericholecystic edema and increased periportal ing the gallbladder, or signs of gas in the portal vein
echogenicity. In 11% of the cases, the liver was enlarged [58]. Venous thrombosis of abdominal vasculature, such
on US [31]. A retrospective study of the same popula- as thrombosis of the portal vein, has also been reported
tion reported even higher odds of hepatobiliary involve- [59,60]. One patient was a middle-aged man with both
ment, with up to 75% of patients showing hepatomegaly abdominal and respiratory symptoms, while the other
Med Ultrason 2023; 25(1): 82-92 87
case was described as part of a larger retrospective trial to COVID-19 is thought to be multifactorial, including
without additional information. from micro thrombi formation leading to tissue ischemia,
Pancreas virus-mediated cytokine storm and direct viral effects on
Three cases of acute pancreatitis associated with renal parenchyma as ACE-2 expression in urinary organs
COVID-19 in children and two cases in adults were iden- are nearly 100-fold higher than in respiratory organs [68].
tified. In a 14 year old boy, US revealed prominence of Spleen and lymphatic system
the whole pancreas as well as its duct, associated with Splenic manifestations detected on US were reported
mild hepatomegaly and a solitary gallstone [61]. In the in children with MIS-C due to COVID-19. Two studies
other case, an adolescent male patient had a distended of 35 and 16 pediatric patients found an enlarged spleen
gallbladder with thickened walls, biliary sludge and a in 11-13% of the included patients, in one case even with
small amount of free fluid, but no pancreatic abnormali- focal hypoechoic splenic lesions [31,49]. Lymphadenop-
ties [62]. In another young and otherwise healthy 7 year athy was frequently described on abdominal US of chil-
old girl, US revealed diffuse pancreatic enlargement and dren with COVID-19. Miller et al found prominent lym-
heterogeneous pancreatic echogenicity [63]. Moreover, phatic tissue in the right hemi abdomen in 16.7% of their
the three children with COVID-19 associated pancreati- 40 included patients [30]. Mesenterial lymphadenitis was
tis did not present with any respiratory manifestation of further reported in two girls with PIMS-TS [71]. More-
the disease [62,63]. over, Hameed et al revealed enlarged intraabdominal
In adult patients, a case series reported acute pan- lymph nodes in 47% of their patients, with 37% showing
creatitis in two of three family members with severe echogenic expansion of the mesenteric tissue [31].
COVID-19. Here, US revealed an increased pancreatic CEUS for abdominal imaging of COVID-19 infection
volume without signs of necrosis, focal lesions, or gall- CEUS offers the possibility to analyze dynamic mi-
stones [64]. crocirculatory disturbances in real time dynamically
Kidneys and urinary tract without any risk for kidneys and thyroid gland even in se-
US renal abnormalities in children and adults were vere progressing disease bedside. Based on severe COV-
mostly related to disturbances of the renal perfusion ID-19 infections, first experiences with abdominal CEUS
going along with acute or acute on chronic kidney dis- examinations are presented. In the stage of an imminent
ease. In children with MIS-C, the main US findings organ failure with significantly reduced kidney and liver
were echogenic kidneys in up to 63% in one study, but function, CEUS can be used to show a narrowing of the
only reported in 5% in another [31,49]. Berteloot et al organ-supplying arteries, as well as a delayed capillary
performed US in children after kidney transplantation, filling of vessels near the capsule, a regional reduced
which were diagnosed with immune post viral graft vas- parenchymal perfusion or an inflammatory hyperemia
culitis related to COVID-19. They found stenosis of the with capillary hyper circulation. It is possible to quickly
renal artery with increased peak systolic velocity using rule out organ infarction and to dynamically record the
spectral Doppler US [65]. Furthermore, a thickened wall mesenteric arterial and venous blood flow [67]. The first
of the urinary bladder was described in a child with MIS- results on abdominal diagnostics confirm the assessment
C [49]. Similar results were obtained in adult patients that CEUS can also detect peripheral reduced blood flow,
with COVID-19. A prospective study found an increased embolisms in the context of pulmonary artery embolism,
renal resistance index measured with Doppler US in all micro infarctions and reactive hyperemia in the case of
their patients and additionally a not continuous pattern consolidations and pleural irritation in the periphery of
of venous flow in 71% of their study sample of 15 pa- the lungs. In this way, CEUS can contribute to improving
tients [66]. The same result was reported by Jung et al, follow-up checks in the event of severe infection constel-
who also performed contrast enhanced US (CEUS) in 5 lations and embolisms in the case of COVID-19 infec-
COVID-19 patients, which additionally revealed a seg- tions [9,12,13,72] (fig 3).
mental renal infarction with reduced cortical microcir- In the case of COVID-19, CEUS is restricted in the
culation in one patient [67]. Elevated resistance indices event of severe disease progression by the fact that the
were also reported in one case where US discovered de- use of Sulfur hexafluoride Microbubbles (SonoVue®)
creased global perfusion of the enlarged and echogenic as US contrast agent can lead to right heart stress with
kidney on CEUS [68,69]. Echogenic kidneys on US were pulmonary hypertension. A restricted right heart func-
found in one retrospective study of 73 patients and one tion is often part of the serious course of the disease with
case report described a previous healthy young adult COVID-19 infections. For a seriously ill COVID-19
male progressing to acute kidney injury in the setting of patient, examinations with computed tomography (CT)
worsening COVID-19 [55,70]. Acute kidney injury due also meant complex repositioning and transport with a
88 Sirine Dehmani, Nadine Penkalla et al Scoping Review: US evidence of intraabdominal manifestations of COVID-19 infection

Fig 3. A 55 years old patient with severe symptoms of a COVID-19 infection. CEUS shows micro infarctions and reactive hyperemia
in the case of consolidations and pleural irritation in the periphery of the lungs (a, b). The spleen shows homogenous enhancement.

high level of personnel care. In addition, the contrast controls, which does not appear to be a consequence of
agent used in CT imaging can pose a not inconsiderable right or left heart dysfunction. A reno-vascular pathogen-
risk for the kidneys, which are often already function- esis of COVID-19 AKI seems likely [73].
ally impaired. This would be one of the starting points Point of care US
for CEUS, since the use of SonoVue® does not impair Due to its easy application and its high diagnostic re-
kidney function. In preliminary investigations, the po- liability, point-of-care US systems of the latest genera-
tential of CEUS for dynamic recording of organ micro tion represent a valuable imaging method for the primary
perfusion in the case of a severe course of a COVID-19
infection with regard to abdominal US could be shown.
Our initial experience indicate reactive changes with hy-
peremia, peripheral mosaic perfusion, peripheral micro
embolism, infarcts and vascular thrombosis (fig 4-6).
This enables a targeted control with CEUS in correlation
to the CT. In addition, CEUS also enables the dynamic
assessment of organ micro perfusion, especially of the
liver, spleen and kidneys. Here, hypoperfusions are com-
mon in severe infectious to septic clinical pictures and,
as with COVID-19 patients, may require the use of an
ECMO treatment.
The use of CEUS for lung diagnostics is reserved for
individual cases. However, especially in the stage of in-
Fig 4. A 69 years old patient with severe symptoms of a
creasing kidney function restriction, CEUS can open up COVID-19 infection: thrombosis of the inferior caval vein
new diagnostic possibilities with regard to changes in mi- with echo-inhomogeneous material inside of the lumen without
crovascularisation. These must be examined multicentri- contrast enhancement (arrow).
cally before a final assessment is possible. Acute kidney
injury (AKI) is a common complication of COVID-19
critical illness but the pathophysiology is uncertain. CE-
US-derived parameters were reduced in COVID-19 as-
sociated AKI compared with healthy controls (perfusion
index 3.415 vs. 548, p=0.001; renal blood volume 7.794
vs. 3.338, p=0.04). Renal arterial flow quantified using
time averaged peak velocity was also reduced compared
with healthy controls (36.6 cm/s vs. 20.9 cm/s, p=0.004)
despite cardiac index being similar between groups (2.8
l/min/m2 vs. 3.7 l/min/m2, p=0.07). Patients with septic
Fig 5. A 65 years old patient with severe symptoms of a
shock had more heterogeneous perfusion variables. Both COVID-19 infection: echo-inhomogeneous parenchymal kid-
large and small vessel blood flow was reduced in patients ney structures, partial edema, local inflammatory reaction by
with COVID-19 associated AKI compared with healthy micro-embolic changes (arrow).
Med Ultrason 2023; 25(1): 82-92 89
mised and thus limiting the functional capacity of the
organ [66,67]. This might be due to hyper inflammation
promoting a prothrombotic state not only affecting the
kidneys but also other organ systems [16]. Hypercoagu-
lability might eventually lead to end organ ischemia due
to the resulting micro- and macroangiopathy, as well as
manifest as thrombosis and embolism [17,18]. Although
similar phenomena are known in sepsis, the mechanisms
involved in COVID-19 might be particular because of
their linkage to the ACE-2 receptor, which contributes
to the widespread endothelial dysfunction [18]. These
mechanisms might also have an impact on changes in the
lymphatic organs and the spleen. However, due to their
role in immune response, they might also experience
unspecific alterations linked to the state of infection in
general [49].
While rather specific signs of pneumonia and ARDS
Fig 6. A 54 years old female patient with severe symptoms due to COVID-19 could be identified using lung US, the
of a COVID-19 infection: inflammatory reaction of the small results concerning the abdomen do not appear to offer
bowel with edema in B-mode (a) and hyperemia with enlarged
enhancement in CEUS (b, arrows). the same specificity [7,14,15]. Nevertheless, they often
reflect the general clinical state and correspond to certain
assessment of abdominal and thoracic findings, especial- symptoms, e.g. an edematous pancreas in Sars-CoV-2-in-
ly in patients on geriatric and intensive care units or in duced pancreatitis [61]. Hence, US provided valuable
emergency situations [74-77]. information for the clinician, often relevant for further
therapy and course of the disease. To determine poten-
Discussion tially more specific intraabdominal US findings linked to
COVID-19, larger cohort studies are required.
This review identified 39 studies reporting US find-
ings of intraabdominal manifestations of COVID-19. We Conclusion
structured these findings according to the corresponding
anatomy of GI, hepatobiliary, kidneys, and the lymphatic Intraabdominal manifestations of COVID-19 are
system. If available, additional clinical information was common and end organ abnormalities can be readily
provided. Although according to the current literature, diagnosed on multiparametric US examinations at bed-
children and adults suffer similarly from GI symptoms side. COVID-19 specific US findings within the abdo-
due to COVID-19, we found more results were reported men have not yet been reported, but the reported results
concerning children. Pathologies such as intussusception often correlated with the clinical presentation. Thus, US
in infants seem to be of great clinical relevance and can has the potential to impact a patient’s clinical course and
readily be detected using US. Avoidance of ionizing ra- therapy, and is therefore of great value.
diation and potentially harmful contrast agents are im-
portant factors to consider in this population [32]. On the Conflict of interest: none
contrary, hepatic and biliary abnormalities appear to be
more common findings in adults. However, the clinical Acknowledgements: The work was kindly support-
importance of findings such as gallbladder sludge is not ed by Bad Mergentheimer Leberzentrum e.V.
clear, as it may not necessarily be linked to COVID-19.
Remarkably, many hepatobiliary pathologies were de- References
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Pictorial essay Med Ultrason 2023, Vol. 25, no. 1, 93-97
DOI: 10.11152/mu-3858

Preoperative ultrasound study of differentiated thyroid cancer:


relevant aspects for its optimal performance. Pictorial essay.
Michael Hirsch1,2, Javiera Matus1,3, Constanza Orellana1,3, Karin Krauss4

1Programa de Radiología, Departamento de Especialidades Médicas, Universidad de La Frontera, 2Departamento de


Imágenes, Clínica Alemana de Temuco, 3Servicio de Radiología, Hospital Hernán Henríquez Aravena, 4Servicio de
Imagenología, Complejo Asistencial Padre Las Casas, Temuco, Chile.

Abstract
Differentiated thyroid cancer has an increasing incidence in recent years, but its mortality remains low. In this context, a
preoperative ultrasound study is fundamental; it makes a difference due to its ability to adequately characterize local involve-
ment, the presence of extrathyroidal extension and lymphatic metastases. A preoperative study can help to decide the best
therapeutic measures and thus avoid adding greater morbidity to patients. In this article we present the relevant aspects to
consider in the preoperative ultrasound evaluation of differentiated thyroid cancer and representative images of the main find-
ings that can be found.
Keywords: cancer; thyroid; ultrasound; metastasis; lymph nodes

Introduction In this pictorial essay we present relevant aspects in


the preoperative US evaluation of DTC and representa-
The incidence of thyroid cancer has increased in last tive images from our experience.
years, the differentiated thyroid carcinoma (DTC) being
the most frequent type. Up to 95% of DTC are papillary Ultrasound technique
thyroid carcinoma (PTC) [1]. Dissemination to regional
lymph nodes is present in 30-80% of cases, mainly at A multi-frequency linear transducer (8-15 MHz) is
cervical level VI (fig 1) [2,3], being the greatest risk fac- preferable for the correct evaluation of the deep paratra-
tor for thyroid cancer recurrence, suggesting that many of cheal areas and the tracheoesophageal grooves (TEG),
the lymphatic metastases detected in the first post-treat- which are references for the trajectory of the recurrent
ment years are residual disease [4]. Due to the greater laryngeal nerves (fig 2) [5].
risk of complications related to the surgical reinterven- The neck must be hyperextended. The patient should
tion, the interest for more accurate preoperative studies be asked to turn their neck to the right or left to facilitate
has increased, cervical ultrasound (US) being the most the study of level VI lymph nodes and better expose the
sensitive study, modifying the surgical approach in up to TEG (fig 3) [5].
23% of cases [4]. The cervical region must be explored from the chin
to the suprasternal region, looking for remnants of the
thyroglossal duct, which are frequently close to the hyoid
Received 25.08.2022 Accepted 17.12.2022 bone (fig 4), presence of pyramidal lobes and intrathorac-
Med Ultrason
2023, Vol. 25, No 1, 93-97
ic extension [5].
Corresponding author: Michael Hirsch, MD
Departamento de Imágenes, Characterization of thyroid lesions
Clínica Alemana de Temuco
Senador Estébanez 645, 4810297 Temuco,
Región de La Araucanía, Chile
Although the aim of this work is not to review the
Phone: 56-45-2201167 features of thyroid nodules to allocate risk of malignan-
E-mail: michael.hirsch@ufrontera.cl cy, it must be remembered that the nodules at greatest
94 Michael Hirsch et al Preoperative US study of differentiated thyroid cancer & its optimal performance

risk of malignancy are solid, hypoechogenic, taller than


it is wide, with irregular edges, microcalcifications, inter-
mittent ring-shaped calcifications and with extrathyroidal
extension (ETE) [6].

Fig 2. Left tracheoesophageal groove (dotted lines) between


the trachea (asterisk) and the esophagus (arrow), through which
the recurrent laryngeal nerve passes together with echogenic
fatty tissue (arrowhead).

Evaluation of extrathyroidal extension


The interruption of the capsule, bulging of structures,
involvement of the TEG, contact of the tumor with the
capsule, and tracheal invasion suggest ETE [7,8]. Inter-
Fig 1. Neck lymph node levels. Level I: submental (IA) and
ruption of the capsule appears as a loss of the hypere-
submandibular (IB). Level II: upper internal jugular chain. chogenic interface of the capsule [8]. The protrusion of
Level III: middle internal jugular chain. Level IV: lower inter- a nodule towards the TEG is associated with an invasion
nal jugular chain. Level V: posterior triangle. Level VI: central of the recurrent laryngeal nerve [8]. Contact between the
(anterior) compartment. Level VII: superior mediastinal nodes. tumor and the adjacent capsule higher than 25% of the
Sublevel IA and IB are separated by anterior bellies of both
digastric muscles, level I and II by the vertical plane defined nodule circumference have a positive predictive value of
by the posterior border of the submandibular gland, sublevel 70.7% and a specificity of 85.7% for microcarcinomas
IIA and IIB by the posterior border of the internal jugular vein, (fig 5, fig 6) [7]. The formation of an obtuse angle be-
level II and III by the horizontal plane defined by the inferior tween the tumor and the trachea is suggestive of tracheal
border of the hyoid bone, level III and IV by the horizontal invasion (fig 7) [8].
plane defined by the inferior border of the cricoid cartilage as
well as sublevel VA and VB, level VI and levels III-IV by the It is also useful to evaluate the vocal cords and their
medial borders of both common carotid arteries, and level VI adequate excursion; asymmetric displacement or absence
and VII by superior border of manubrium. of displacement of the affected side [9].

Fig 3. US that shows how to improve the visualization of the right tracheoesophageal groove (TEG) (a). Turning the head to the left
(b), the esophagus slides to the right, better exposing the TEG (dotted line) and its contents (arrowhead). Asterisk: trachea.
Med Ultrason 2023; 25(1): 93-97 95

Fig 4. US in the sagittal plane, midline, demonstrating a thy- Fig 6. Papillary thyroid carcinoma (between calipers) that pre-
roglossal duct cyst (between calipers) with anechogenic con- sents protrusion towards the esophageal groove (arrowhead)
tent and a fine septum, immediately caudal to the hyoid bone without involving it completely. Asterisk: trachea, arrow: es-
(arrow). Asterisk: mylohyoid muscle, arrow heads: epiglottis. ophagus.

Fig 5. Different cases of papillary thyroid carcinoma (PTC) that present progressive involvement of the capsule up to the marked
extrathyroidal extension: a) PTC completely surrounded by healthy parenchyma (arrow heads); b) PTC that comes in contact without
involving the capsule (arrow heads), which presents a linear hyperechogenic appearance: c) PTC that involves the capsule (white ar-
row heads), becoming hypoechogenic unlike the linear hyperechogenic appearance of the normal capsule (black arrow heads). There
is no extension towards the infrahyoid muscles; d) PTC with marked extension towards the infrahyoid muscles (arrows), and towards
the trachea with loss of definition of its cartilages and membrane (arrow heads). Asterisk: trachea.

Assessment of the lymph nodes peripheral vascularization is the criterion of malignancy


The presence of microcalcifications and cystic chang- with a better sensitivity-specificity ratio (fig 8) [5].
es have a proven specificity of up to 100%, but low sen- The loss of hyperechogenic hilum has shown a speci-
sitivity for lymph node metastasis [10]. The presence of ficity of only 29%. However, due to the high sensitivity

Fig 7. Different cases of papillary thyroid carcinoma (PTC): a) PTC that presents an acute angle in relation to the trachea (asterisk),
unlike b), which presents an obtuse angle, with this one being of greatest risk for tracheal invasion.
96 Michael Hirsch et al Preoperative US study of differentiated thyroid cancer & its optimal performance

of this finding (100%), the presence of the fatty hilum present involvement of some lymphatic groups difficult
makes it possible to exclude the presence of a malignan- to visualize with routine preoperative US [12].
cy with some certainty [10]. Staging of DTC
Hyperechogenicity of the parenchyma and rounded In the 8th edition of the American Joint Committee on
morphology has shown specificity of only 18% and 54%, Cancer (AJCC) from 2018, significant changes for the
respectively, to determine malignancy; therefore, it is staging of patients with DTC were reported (23-35% of
recommended that these criteria to be used with other down-staging) [13]. These changes are meant to avoid
auxiliary criteria such as increased size or those previ- the overtreatment of patients at low risk of malignancy
ously mentioned [10,11]. [14,15].
Limitations of US Active surveillance
Preoperative computed tomography (CT) or magnet- Active surveillance is considered a safe option for
ic resonance imaging (MRI) are recommended as a com- managing patients with low-grade asymptomatic DTC
plement to US for patients with a clinical suspicion of <1 cm and with no high-risk factors such as the presence
advanced disease [12] (fig 9, fig 10). Patients who pres- of metastatic lymph nodes, distant metastasis, a fine-nee-
ent voluminous or widely distributed adenopathies could dle biopsy with findings of high-grade malignancy or

Fig 8. Different cases of lymphatic metastasis of papillary thyroid carcinoma: a) adenopathy (arrowheads), with solid component
of heterogeneous echogenicity and peripheral vascularization in color Doppler mode and anechogenic cystic component (arrow); b)
adenopathy with loss of echogenic hilum, heterogeneous echostructure and microcalcifications; c) adenopathy with heterogeneous
echostructure, loss of echogenic hilum and penetrating peripheral vessels in color Doppler mode; d) adenopathy of heterogeneous
echostructure, loss of echogenic hilum, with presence of calcifications (arrow heads) and small peripheral cystic areas (arrows); e)
adenopathy (arrow heads) of heterogeneous echostructure, with loss of echogenic hilum, isolated microcalcifications, emphasizing
greater overall echogenicity than the adjacent sternocleidomastoid muscle (asterisk); f) adenopathy (arrow heads) with small cystic
area, similar in appearance to a thyroid colloid cyst (arrow).

Fig 9. Papillary thyroid carcinoma (arrowheads) that at the time of the study with ultrasound (a) presented an extension towards
the mediastinum (arrows), which limited the complete assessment; b) CT of the same patient demonstrates the great intrathoracic
involvement not visualized by ultrasound. White asterisk: trachea, black asterisk: sternum.
Med Ultrason 2023; 25(1): 93-97 97

Fig 10. Papillary thyroid carcinoma (arrowheads) that at the time of the study with ultrasound (a) presented an extension towards
the trachea (asterisk), difficult to characterize; b) CT of the same patient better demonstrates the tracheal invasion (arrow heads).
Asterisk: trachea.

tumors that invade the trachea or the recurrent laryngeal sensus statement and recommendations. Korean J Radiol
nerve [16]. 2011;12:1–14.
7. Kwak JY, Kim EK, Youk JH, et al. Extrathyroid extension
Conclusions of well-differentiated papillary thyroid microcarcinoma on
US. Thyroid 2008;18:609–614.
Nowadays, US is the best tool to conduct an adequate 8. Chung SR, Baek JH, Choi YJ, et al. Sonographic assess-
preoperative study of DTC. Whoever does the preopera- ment of the extent of extrathyroidal extension in thyroid
tive study must be familiar with the relevant aspects of the cancer. Korean J Radiol 2020;21:1187–1195.
technique, important findings that must be assessed and 9. Leboulleux S, Girard E, Rose M, et al. Ultrasound crite-
added to the report, as well as an in-depth understanding ria of malignancy for cervical lymph nodes in patients
of anatomy and ultrasound signs that can differentiate followed up for differentiated thyroid cancer. J Clin Endo-
conditions that will mark the prognosis and therapeutic crinol Metab 2007;92:3590–3594.
10. Yeh MW, Bauer AJ, Bernet VA, et al. American thyroid
approach. Emphasis must be placed on the evaluation of
association statement on preoperative imaging for thyroid
ETE and lymphatic involvement and complemented with
cancer surgery. Thyroid 2015;25:3–14.
additional studies in cases where US is insufficient. 11. Zhao H, Li H. Meta-analysis of ultrasound for cervical
lymph nodes in papillary thyroid cancer: Diagnosis of cen-
Conflict of interest: none tral and lateral compartment nodal metastases. Eur J Radiol
2019;112:14–21.
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lymph node metastases in the central compartment. Eur Ra- Cancer: The American Thyroid Association Guidelines
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4. Kumbhar SS, O’Malley RB, Robinson TJ, et al. Why thy- Node-Metastasis Staging System for Differentiated Thy-
roid surgeons are frustrated with radiologists: Lessons roid Cancer. Thyroid 2017;27:1149–1155.
learned from pre- and postoperative US. Radiographics 15. Tuttle RM, Haugen B, Perrier ND. Updated American joint
2016;36:2141–2153. committee on cancer/tumor-node-metastasis staging system
5. Yeh MW, Bauer AJ, Bernet VA, et al. American thyroid for differentiated and anaplastic thyroid cancer (Eighth Edi-
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Continuing education Med Ultrason 2023, Vol. 25, no. 1, 98-103
DOI: 10.11152/mu-3810

Ultrasound guided Interpectoral, Pectoserratus and Serratus


anterior plane blocks
Geraldine Armissoglio, Paschalitsa Serchan, Laura Griseto, Gabriella Iohom

Department of Anaesthesiology and Intensive Care Medicine, Cork University Hospital, Cork, Ireland

Abstract
Interpectoral, Pectoserratus and Serratus anterior plane blocks are relatively recent fascial plane blocks performed with
ultrasound guidance to provide analgesia of the anterior thoracic wall. They have been mainly used in breast surgery and are
both safe and easy to perform. This review will focus on the technique of ultrasound guided Interpectoral, Pectoserratus and
Serratus anterior plane blocks.
Keywords: Interpectoral plane block; Pectoserratus plane block; Serratus anterior plane block; ultrasound; breast surgery

Introduction they appear to be safe, simple and effective [10]. Not only
do they provide excellent analgesia compared to general
Breast cancer is the most common cancer diagnosed anaesthesia alone [11–13], but they also allow a reduc-
globally in 2020 accounting for 11.7% of new annual can- tion in overall opioid consumption, postoperative nausea
cer cases worldwide [1]. Most women with breast cancer and vomiting [9,14–17] and chronic postoperative pain
will have some type of surgery as part of their treatment [18]. Some studies suggest the role of regional anesthesia
[2]: tumor resection, mastectomy, sentinel lymph node in the overall survival in breast cancer [19,20].
biopsy or axillary dissection. Blanco et al first described The popularity of these blocks has led to multiple
the pectoralis nerve block (Pecs I) in 2011 [3], and later techniques and given names resulting in heterogeneity
a second version, “the modified Pecs block or Pecs II”, and a difficulty in comparing them. A recent consensus
adding a second injection, in order to extend the analgesia regarding the nomenclature has been established [21].
coverage to the intercostal nerves [4]. He later described The Pecs I should now be referred to as the Interpectoral
a further modification the “Serratus anterior plane (SAP) block and the second injection of Pecs II became the Pec-
block” [5,6]. These interfascial blocks were developed as toserratus plane block. The Serratus anterior plane (SAP)
alternatives to thoracic epidural, paravertebral, intercos- block will be referred to as Superficial or Deep SAP
tal, and intrapleural nerve blocks for perioperative anal- block depending on the site of injection. This paper will
gesia of anterior thoracic surgeries, mainly breast surgery focus on the technique of ultrasound guided Interpecto-
[7–9]. They have gained popularity for breast surgery as ral, Pectoserratus and Serratus anterior plane blocks.

Anatomy
Received 13.07.2022 Accepted 06.09.2022
Med Ultrason
2023, Vol. 25, No 1, 98-103
The pectoral region is located in the anterior chest
Corresponding author: Dr Geraldine Armissoglio wall. It contains four muscles separated by fascias: the
Department of Anaesthesiology pectoralis minor and major innervated by the lateral and
and Intensive Care Medicine, medial pectoral nerves which run between these muscles,
Cork University Hospital,
Wilton, Cork, Ireland
the serratus anterior innervated by the long thoracic nerve
Phone/fax: +353214922135/+353214546434 (C5, C6, and C7), and the subclavius muscle innervated
E-mail: g.armissoglio@gmail.com by the upper trunk of the brachial plexus (C5 and C6).
Med Ultrason 2023; 25(1): 98-103 99
The pectoralis major originates from a clavicular to VI, the intercostobrachial nerves, and the long thoracic
head and a sternocostal head; the distal attachment of nerve.
both heads is into the intertubercular sulcus of the hu- The Serratus anterior plane block consists of an injec-
merus. Underneath the pectoralis major lies the pectora- tion of local anaesthetic in the axillary region, at a more
lis minor. This muscle originates from the 3rd to the 5th lateral and posterior location than the above nerve blocks,
rib near their costal cartilages and extends superolaterally between the serratus anterior muscle and latissimus dorsi
to form a flat tendon, which inserts into the medial bor- muscle, targeting the lateral cutaneous branches of the
der and coracoid process of scapula. The serratus anterior thoracic intercostal nerves. Deep and superficial virtual
is located more laterally in the chest. It consists of sev- spaces surround the serratus anterior muscle lending the
eral strips which originate from the 1st to the 8th rib and name to deep and superficial SAP block depending on
which insert at the costal surface of the medial border of the location of the local anaesthetic solution. Either plane
the scapula. block will achieve analgesia to the anterolateral chest
The axillary region is the area that lies underneath wall with reportedly similar efficacy and an equivalent
the glenohumeral joint, at the junction of the upper limb area of cutaneous sensory loss [5,6,23,24]
and the thorax. At the axillary fossa, the intercostobra-
chial nerve, lateral cutaneous branches of the intercostal Ultrasound anatomy/ internal landmarks
nerves (T3–T9), the long thoracic nerve, and the thora-
codorsal nerve are located in a compartment between the These fascial blocks are ideally suited for ultrasound
serratus anterior and the latissimus dorsi muscles, be- guidance with a high frequency linear probe. The patient
tween the posterior and midaxillary lines. At the level of is in supine position with the arm next to the body or
the fifth rib, a superficial plane forms between the anteri- abducted 90 degrees. For the Interpectoral and Pectoser-
or aspect of the serratus anterior and the posterior aspect ratus blocks, the linear probe is placed perpendicular to
of the latissimus dorsi muscle. The deep plane is situated the middle of the clavicle at the level of the 3nd rib. From
between the posterior aspect of the serratus anterior and superficial to deep, the pectoralis major is first encoun-
the external intercostal muscles and ribs. tered, then the pectoralis minor. The thoracoacromial ar-
Most of the breast consists of glandular (milk-pro- tery runs in the fascia between the pectoralis muscles; it
ducing) and fatty tissues. The sensory innervation of the may be identified in some cases and should be avoided.
breast is derived from the anterior and lateral branches of The pleura is easily identified as a bright echogenic line
the second to the sixth intercostal nerves. These intercos- between the ribs. The probe is then moved down and
tal nerves leave the spinal cord and run anteriorly under laterally to the level of the 4th and 5th rib. The Serratus
the corresponding rib, then they divide into lateral and anterior muscle can be seen appearing on the top of the
anterior branches. Since these nerves run underneath the rib (fig 1-3).
corresponding ribs, they are located in close proximity
to the serratus muscle. Other nerves that supply sensory
innervation include the lower cervical plexus; sensation
to the nipple is derived from the lateral cutaneous branch
of the fourth thoracic nerve [22].

Applied anatomy

The Interpectoral block consists of an interfascial in-


jection of local anaesthetic between the pectoralis ma-
jor and pectoralis minor muscles at the level of the third
rib to block both the medial and lateral pectoral nerves
which are responsible for the motor innervation of the
pectoral muscles. As a result, the Interpectoral block has
no direct analgesic effect.
By adding a Pectoserratus plane block, achieved us-
ing the same single needle entry point at skin, local an- Fig 1. Ultrasound scout of pectoral region at the level of 3rd
rib. From superficial to deep, the pectoralis major muscle (PM),
aesthetic is deposited between the pectoralis minor and pectoralis minor muscle (Pm), and the thoracoacromial artery
the serratus anterior muscle. The intention is to block the (TAA) are identified. The pleura appears as a bright echogenic
anterior cutaneous branches of the intercostal nerves III line.
100 Geraldine Armissoglio et al Ultrasound guided Interpectoral, Pectoserratus and Serratus anterior plane blocks

Fig 2. Ultrasound scout for Pectoserratus plane block: the pec-


toralis major (PM) and minor (Pm) muscles, and the Serratus Fig 3. Ideal injection site for the deep and superficial Serratus
anterior muscle (Sm) appearing above the 4th rib anterior plane (SAP) block on top of the 4th and 5th ribs. The
thoracodorsal artery (TDA) runs in the fascial plane between
the serratus anterior (Sm) and the latissimus dorsi (LD) mus-
Technique with ultrasound guidance cles. The ribs, pleura, and intercostal muscles can also be seen.

The operator stands at the patient’s side. The blocks kg of local anaesthetic and for Serratus anterior plane
are performed under aseptic conditions with standard block 0.4 ml/kg of local anaesthetic.
monitoring and intravascular access in situ. They can be The needle is inserted parallel to the long axis of the
carried out before or after induction of anaesthesia, using probe, perpendicular to the middle of the clavicle at the
a 22G short bevelled needle (50 or 100 mm), a high fre- level of 3rd rib, medially with a posterolateral direction
quency linear probe and a long-acting local anaesthetic for the Interpectoral and Pectoserratus plane blocks (fig
(bupivacaine 0.25%, ropivacaine 0.2%, or levobupiv- 4), using the same entry point at the skin.
acaine 0.25%). General precaution should be exercised The Serratus anterior plane block can be performed
when injecting the local anaesthetic solution. These both anteriorly or laterally. Figure 5 illustrates the ante-
blocks are fascial blocks and not targeting a specific rior approach. The needle is inserted at the level of the 4th
nerve, thus a relatively large volume of local anaesthetic and 5th ribs. Figures 6-9 illustrate the in-plane approach
will be needed [3–5]: for Interpectoral block- 0.2 ml/kg to these fascial plane blocks with the appropriate needle
of local anaesthetic, for Pectoserratus plane block 0.4ml/ tip position and pattern of the local anaesthetic spread.

Fig 4. a) Ideal position of the probe and b) needle for Interpectoral and Pectoserratus plane blocks. The clavicle has been marked.
The probe is placed perpendicular to the middle of the clavicle at the level of the 3rd rib. In the plane needling technique, the needle
is inserted from the medial to posterolateral direction; c) The operator stands on the patient’s side. The ultrasound machine is ideally
placed above the patient’s head.
Med Ultrason 2023; 25(1): 98-103 101

Fig 6. Interpectoral block: in plane needle injection of local


Fig 5. a) Position of the probe and b) needle for Serratus an- anaesthetic (LA) between the pectoralis muscles, major (PM)
terior plane block (anterior approach) in the axillary fossa and minor (Pm)
at the level of the 4th and 5th ribs. The arm is abducted at 90
degrees. The needle is inserted from the anterior to posterior
direction.

Indications

The main indication of Interpectoral, Pectoserratus


and Serratus anterior plane blocks is analgesia of the
anterolateral thoracic wall under circumstances summa-
rized in Table I.

Discussion

Both Pectoserratus and SAP blocks may be per-


formed for the analgesia of breast surgery. It appears that
the Pectoserratus block might be superior to the SAP Fig 7. Pectoserratus plane block: following the interpectoral
block for this indication especially when breast surgery is block, the needle is advanced deeper between the pectoralis mi-
associated with an axillary dissection [25,26]. However, nor (Pm) muscle and the serratus anterior muscle (Sm) at the
a recent meta-analysis suggests that there were few dif- level of the 3rd and 4th rib.
ferences between the analgesic techniques for breast sur-
gery regarding their effectiveness [30]; pectoralis nerve
blocks, serratus anterior block, erector spine block or
paravertebral block, but they were all superior to general
anaesthesia alone (control group) or local infiltration.
Pectoserratus and SAP blocks may be associated with an
ultrasound guided parasternal block to extend medially
the analgesia of the anterior thoracic wall.
Any regional analgesia technique should ideally be
performed before surgery with ultrasound guidance, with
no or little sedation [31] or after induction of anaesthesia.
In some cases, the surgery can be performed exclusively
under regional anaesthesia [31].
Even though these blocks were primarily developed
for the analgesia after surgery on the hemithorax, mainly Fig 8. Superficial Serratus anterior plane block: in plane nee-
breast surgery, case reports have also described their use dle, superficial injection above the serratus muscle at level of
for the analgesia following thoracotomy or rib fractures 4/5th rib.
102 Geraldine Armissoglio et al Ultrasound guided Interpectoral, Pectoserratus and Serratus anterior plane blocks
Table I. Main indications of Pectoserratus and Serratus anterior plane blocks
Pectoserratus plane block SAP block
Breast surgery [3,4] + +
Sentinel lymphe node and axillary dissection [25,26] + +
Breast expander /submuscular prosthesis + +
Implantation of cardiac device (pacemaker and defibrillator) or ports [27] + +
Anterior thoracotomy[28] + +
Rib fractures [29] - +
Thoracoscopy [24] - +

associated with a catheter insertion for prolonged anal-


gesia [29,32], as well as arteriovenous fistula of the up-
per limb [33]. Finally, as they are considered superficial
blocks amenable to external compression, they could be
considered in the case of an ongoing anticoagulation [34-
36] when paravertebral block and thoracic epidural are
contraindicated [37].

Conclusion

The practice of regional anaesthesia has increased


over the past years, especially with the wide availability
of ultrasound machines. We described two different anal-
gesic blocks as alternatives to paravertebral and thoracic
epidural blocks, still considered the gold standard for an-
Fig 9. Deep Serratus anterior plane block, injection below the
algesia of the anterior thoracic wall. serratus muscle

Conflict of interest: none 8. Hussain N, Brull R, McCartney CJL, et al. Pectoralis-II


Myofascial Block and Analgesia in Breast Cancer Surgery:
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Transcatheter aortic valve implantation & cardiac tamponade of
unclear etiology

Case report Med Ultrason 2023, Vol. 25, no. 1, 104-106


DOI: 10.11152/mu-2706

Transcatheter aortic valve implantation in a patient with


interventricular membranous septal aneurysm resulted in cardiac
tamponade of unclear etiology
Mihaela Ioana Dregoesc1, Dan Ion Bindea2, Mădălin Constantin Marc3, Vasile Săsărman2,
Adrian Corneliu Iancu1

1Cardiology Department, “Iuliu Hațieganu” University of Medicine and Pharmacy, 2Cardiovascular Surgery Depart-
ment, “Iuliu Hațieganu” University of Medicine and Pharmacy, 3“Niculae Stăncioiu” Heart Institute, Cluj-Napoca,
Romania

Abstract
An 86-year-old lady with severe aortic stenosis and interventricular membranous septal aneurysm underwent transfemoral
transcatheter aortic valve implantation (TAVI). A balloon-expandable valve was deployed after a difficult native valve cross-
ing. Transesophageal echocardiography showed a rapidly accumulating pericardial effusion, with pericardial thrombus and
subsequent cardiac tamponade. The angiographic views raised suspicion of aortic root perforation. Median sternotomy was
performed because of sudden hemodynamic collapse.
The report presents the uncommon association between severe aortic stenosis and interventricular membranous septal
aneurysm in an octogenarian and discusses its impact on the development of a post-TAVI major complication.
Keywords: transcatheter aortic valve implantation; cardiac tamponade; intrapericardial thrombus; aortic root injury

Introduction cidence and an incompletely understood etiology [2]. It


has been rarely diagnosed as an isolated finding and it
Transcatheter aortic valve implantation (TAVI) has is usually associated with other congenital heart defects
become the standard treatment for patients with symp- [3]. Patients with AMS are usually asymptomatic, possi-
tomatic severe aortic stenosis and increased surgical risk ble complications related to the AMS presence including
[1]. Due to the infrequent association, little is known arrhythmic and thromboembolic events [3,4].
about specific procedural steps and outcomes in the pres- The presence of structural defects in the sub-annular
ence of concurrent congenital heart defects. area could cause prosthesis malposition resulting in sig-
An aneurysm of the interventricular membranous nificant paravalvular leaks or device embolization. There
septum (AMS) is a rare condition with an unknown in- are only three previous reports about the association be-
tween AMS and transfemoral TAVI [5-7].
Received 20.07.2020 Accepted 26.09.2020
Med Ultrason Case report
2023, Vol. 25, No 1, 104-106
Corresponding author: Adrian C. Iancu, MD, PhD
Professor of Cardiology
An 86-year-old lady with severe aortic stenosis and
“Iuliu Hațieganu” University of Medicine and NYHA class III heart failure was proposed for transfem-
Pharmacy, Department of Cardiology oral TAVI. Echocardiography showed a hypertrophic
19-21 Calea Moților, left ventricle, with a 36% ejection fraction. Moderate
400001, Cluj-Napoca, Romania
E-mail: adrianiancu56@gmail.com
mitral regurgitation and severe pulmonary hypertension
Phone: +40744751027 were noticed. The aortic valve area measured 0.6 cm2.
Fax: +40264595090 An AMS was identified both on echocardiography and
Med Ultrason 2023; 25(1): 104-106 105

Fig 1. Aneurysm of the interventricular membranous septum.


Panel a – Transthoracic echocardiography five-chamber view
showing the presence of an aneurysm of the membranous sep-
tum (asterisk). Panel b – Cardiac computed tomography trans-
verse view which confirms the presence of the sub-annular Fig 2. Intraprocedural transthoracic echocardiography modi-
congenital anomaly (asterisk). IVS = interventricular septum; fied two-chamber view identifies the pericardial thrombus
LA = left atrium; LV = left ventricle; RA = right atrium; RV = in contact to the left ventricular posterior wall (asterisk) and
right ventricle. shows the presence of pericardial effusion. LA = left atrium;
LV = left ventricle; PE = pericardial effusion; PW = posterior
computed tomography, but no interventricular shunting left ventricular wall.
was present (fig 1). A balloon-expandable 26 mm Ed-
wards Sapien 3 valve (Edwards Lifesciences Corp., CA, short limited aortic sinus perforation (fig 3), the finding
USA) was implanted under general anesthesia. Predila- was not identified on the transesophageal echocardio-
tation was avoided because of the unknown impact of graphic examination.
this procedural step on the sub-annular structural anom- Median sternotomy was performed because of the
aly. The native valve was crossed with difficulty. The sudden hemodynamic collapse and 800 ml of arterial
Edwards Commander Delivery System was retracted in blood and fresh thrombus were evacuated. A posteri-
the ascending aorta several times and the flex wheel was or aortic root hematoma was identified, but no active
used to change the angle of annulus approach. After sev- bleeding was noticed. Surgicel Absorbable Hemostat
eral pushing maneuvers the prosthesis was successfully (Johnson&Johnson, NJ, USA) was applied. Two units
positioned and deployed. Following deployment, trans- of packed red blood cells were administered and the pa-
thoracic and transesophageal echocardiography showed tient left the operating room with stable hemodynamics.
a rapidly accumulating pericardial effusion, with cardiac Postoperative evolution was influenced by the develop-
tamponade. Pericardial thrombus was identified next to ment of a large left plural effusion. Thoracentesis was
the left ventricular posterior wall (fig 2, Video 1, on the attempted but the procedure was complicated by a mas-
journal site). Although the angiographic views showed a sive pneumothorax, which required emergency drainage.

Fig 3. Angiographic views. Panel a – Angiography view showing the initial integrity of the aortic walls. Panels b-d – Angiography
views showing the development of aortic root injury. Contrast extravasation is seen following native valve crossing (arrows). The
aneurysm of the membranous septum is filled with contrast (asterisk).
106 Mihaela Ioana Dregoesc et al Transcatheter aortic valve implantation & cardiac tamponade of unclear etiology

The patient made a slow recovery and after a four weeks aortic root injury. Three previous reports offered data on
hospitalization she was discharged home. At the one-year this uncommon association in TAVI patients. Concerns
follow-up she was in good clinical condition. about the procedure were raised in all three cases, but
valve deployment was uneventful [5-7].
Discussion Despite significant improvements in technology and
operator experience, TAVI remains a complex and techni-
Aortic dissection and perforation are rare complica- cally demanding procedure that requires advanced skills
tions of TAVI, with an incidence of 0.2% [8]. Several and intensive training. Major complications like cardiac
mechanisms are incriminated in the development of an tamponade negatively influence the procedural outcome
aortic tear: stiff wire maneuvering in the ascending aorta, and need to be further reduced. The etiology of the peri-
balloon valvuloplasty injury, valve catheter injury to the cardial effusion may sometimes be uncertain, but quick
aortic wall, system retraction in balloon-expandable de- decision making is mandatory in case of hemodynamic
vices, or postdilatation balloon interaction with the aorta instability. When perforation of the left-side structures is
[9,10]. In our case, the aortic tear was most probably pro- suspected open surgical exploration is the preferred ap-
duced by the leading edge of the prosthesis pusher dur- proach.
ing the prolonged native valve crossing maneuvers. Pre-
dilatation would have probably prevented the event by References
facilitating prosthesis advancement through the calcific 1. Baumgartner H, Falk V, Bax JJ et al. 2017 ESC/EACTS
native valve. However, the avoidance of this procedural guidelines for the management of valvular heart disease.
step was related to the presence of the AMS and to the Eur Heart J 2017;38:2739-2791.
negative impact it might have had on the anomalous sub- 2. Choi M, Jung JI, Lee BY, Kim HR. Ventricular septal an-
annular structures. eurysms in adults: findings of cardiac CT images and cor-
The management of an aortic perforation depends on relation with clinical features. Acta Radiol 2011;52:619-
the patient’s clinical status and on the site of the perfora- 623.
3. Carcano C, Kanne JP, Kirsch J. Interventricular membra-
tion [8]. In our case, the aortic injury occurred at the level
nous septal aneurysm: CT and MR manifestations. Insights
of the non-coronary sinus and was incriminated in the eti-
Imaging 2016;7:111-117.
ology of the pericardial effusion. Although the presence 4. Jain AC, Rosenthal R. Aneurysm of the membranous ven-
of pericardial thrombus in close proximity to the left ven- tricular septum. Br Heart J 1967;29:60-63.
tricular posterior wall could have raised suspicion of an 5. Banga S, Barzallo MA, Nighswonger CL, Mungee S. Tran-
earlier, guidewire induced left ventricular wall perfora- scatheter aortic valve replacement in membranous inter-
tion, the angiographic images suggestive of an aortic root ventricular septum aneurysm with left ventricular outflow
lesion led to an invasive, surgical approach. During TAVI tract extension. World J Cardiol 2018;10:1-5.
procedures, the incidence of cardiac tamponade reach- 6. Hawa ZA, Hawa A, Mitchell J, Allen K. TAVR in a patient
es 4.3%, the most common cause being right ventricular with a membranous ventricular septal aneurysm identified
perforation due to pacemaker leads [9]. Perforations of during cardiac CT. BMJ Case Rep 2019;12:pii:e231215.
7. Kadoya Y, Zen K, Matoba S. Bicuspid Aortic Valve Ste-
the left-sided structures are almost equally divided be-
nosis With Membranous Interventricular Septal Aneurysm
tween annular/supra-annular ruptures and left ventricular Treated Using Transcatheter Aortic Valve Replacement.
wall perforations [9]. Although less common, tamponade Circ Rep 2019;1:540-541.
caused by arterial perforations is associated with higher 8. Langer NB, Hamid NB, Nazif TM, et al. Injuries to the Aor-
mortality rates [8,9]. In the frail, high-risk TAVI patients, ta, Aortic Annulus, and Left Ventricle During Transcatheter
pericardiocentesis is the preferred strategy, surgery be- Aortic Valve Replacement Management and Outcomes.
ing restricted to the rare cases of aortic root injury [8]. Circ Cardiovasc 2017:10:e004735.
Although better outcomes were recorded in patients who 9. Rezq A, Basavarajaiah S, Latib A, et al. Incidence, manage-
underwent percutaneous pericardial drainage, the pres- ment, and outcomes of cardiac tamponade during transcath-
ence of hemodynamic instability mandates open surgical eter aortic valve implantation: a single-center study. J Am
Coll Cardiol Intv 2012;5:1264-1272.
exploration and repair [8].
10. Eggebrecht H, Vaquerizo B, Moris C, et al. European Reg-
Last but not least, the presence of the AMS had an istry on Emergent Cardiac Surgery during TAVI (EuRECS-
indirect role in the development of the complication Pre- TAVI). Incidence and outcomes of emergent cardiac surgery
dilatation was avoided in order to prevent trauma to the during transfemoral transcatheter aortic valve implantation
sub-annular interventricular septum. As a result, native (TAVI): insights from the European Registry on Emergent
valve crossing became a challenging step of the proce- Cardiac Surgery during TAVI (EuRECS-TAVI). Eur Heart
dure and a major factor involved in the development of J 2018;39:676-684.
Case report Med Ultrason 2023, Vol. 25, no. 1, 107-110
DOI: 10.11152/mu-3614

The “starry night” (diffuse microcalcific myopathy) – thousands


of muscle microcalcifications after 30 years of Trichinella infection
detected by ultrasound
Daniela Fodor1,2, Carmen Georgiu2,3, Michael Pelea1,2, Oana Serban1,2, Alexandru Micu2,
Mihaela C. Micu4

12nd
Internal Medicine Department, 2”Iuliu Hatieganu” University of Medicine and Pharmacy 3Pathological Anatomy
Department, 4Rheumatology Division, Rehabilitation Clinical Hospital Cluj-Napoca, Romania

Abstract
Trichinellosis, a parasitosis transmitted through consumption of raw or undercooked meat from pigs and game animals, is
responsible for a specific myositis. The calcifications of infected myocytes and larva can be detected during many years postin-
fection. We present the case of a male patient with a history of severe trichinellosis with disease onset 30 years ago, presenting
with generalized muscle microcalcifications detected during musculoskeletal ultrasound evaluation. The ultrasound aspect of
the muscles was indeed spectacular; hence, the comparison with a ”starry night”.
Keywords: calcific myositis; trichinellosis; ultrasound

Introduction presenting with generalized muscle microcalcifications


detected during ultrasound (US) evaluation.
Trichinellosis is a parasitic infection caused by nema-
todes of the genus Trichinella – Trichinella spp. being Case report
most frequently encountered in humans. Hosts such as
pigs and game animals are the major sources of human A 67-year-old male patient was admitted for inves-
infection. The transmission of the parasite is related to tigation of small hyperechoic spots detected inside the
the consumption of raw or undercooked meat. The dis- muscles during a routine musculoskeletal US examina-
ease has an acute stage (weeks) followed by a chronic tion. The patient was diagnosed with tophaceous gout 10
stage (years) and its severity may vary from asympto- years priorly, with frequent acute episodes of arthritis or
matic to severe forms. The calcification of the host cells tendinitis. No myalgia or impaired muscle function was
(myocytes of the striated muscle tissue) and of the larva detected. Laboratory findings revealed muscle enzymes,
can be detected after 6 months postinfection [1-3]. leukocyte number and C-reactive protein in normal range
We present the case of a male patient with a history and increased serum levels of uric acid (8.5 mg/dl, nor-
of severe trichinellosis with disease onset 30 years ago, mal range 4-6 mg/dl).
Musculoskeletal US (LOGIQ™ S7 Ultrasound/GE
Healthcare, United States, 6-15 and 18 MHz linear trans-
Received 14.01.2022 Accepted 08.02.2022
Med Ultrason
ducers) evaluation was first performed on the muscles of
2023, Vol. 25, No 1, 107-110 the upper arm, afterwards examining the muscles of the
Corresponding author: Mihaela Cosmina Micu thorax, abdomen and lower part of the arms. The same
Rheumatology Division, US aspect/pattern was detected in all examined muscles:
Rehabilitation Clinical Hospital
46-50 Viilor street
small hyperechoic spots (0.2-1 mm) diffusely distributed
400306, Cluj- Napoca, Romania inside the muscles. In some of the larger spots, the comet
E-mail: mcmicu@yahoo.com tail artifact was observed. No posterior acoustic shadow-
108 Daniela Fodor et al Thousands of muscle microcalcifications after 30 years of Trichinella infection detected by US

ing was detected and dynamic examination (in contrac- The anatomopathological exam found in hematoxylin
tion/relaxation) was normal. No pathological findings re- eosin stain a small, isolated, cystic structure lying within
lated to muscles vascularization or fascia were found. No the striated muscle fibres, slightly larger in diameter than
pathological lymph nodes were identified (fig 1-3, movie a normal muscle fibre. Inside the cyst, an intensely baso-
1-3, on the journal site). philic, most likely calcified material, was detected. The
Taking into consideration the patient’s history of thick hyaline capsule excluded an idiopathic or second-
gout, the preliminary assessment of the hyperechoic ary calcification, raising the possibility of a biological
spots was of urate deposition myopathy. For this reason, structure, calcified and encapsulated. Masson’s trichrome
an US guided biopsy (using Bard Magnum system, 16G stain highlighted the collagenous nature of the capsule
biopsy needle) of the left pectoralis major muscle was and the outline of a curved, non-viable tubular structure
performed. We chose this specific muscle mainly due to inside the cyst. The anti-desmin immunohistochemistry
the increased number of visible spots in this area. stained only in the muscle and no inflammatory infiltrate

Fig 1. Transversal (a) and longitudinal (b) grey scale ultrasound of the extensor part of the forearm. Small hyperechoic spots dif-
fusely distributed inside the muscles can be observed.

Fig 2. Transversal (a) and longitudinal (b) grey scale ultrasound of the thenar eminence. Small hyperechoic spots with comet tail
artifact diffusely distributed inside the muscles are detected.

Fig 3. Longitudinal grey scale ultrasound of the distal part of soleus muscle (a) and Achilles’ tendon, proximal third. The small
hyperechoic spots observed in muscles are different compared to tendon urate deposits (tophi) (arrows).
Med Ultrason 2023; 25(1): 107-110 109

Fig 4. Histologically, a round to ovoid, non-viable, calcified cyst of Trichinella spiralis is identified: a) hematoxylin eosin stain
presenting a cyst within muscle fibers, with a hyalin thick peripheral capsule around a basophilic material, basophilia suggesting
calcification of the parasite (200x); b) Masson trichrome stain with a positive green collagenous cyst capsule and inside the cyst the
outline of a curved tubular structure, representing a non-viable parasite (200x); c) anti-desmine immunohistochemical staining – the
capsule and the interior of the cyst is negative, unlike the positive, brown stained, striated muscle fibers (400x).

was detected. The final interpretation was of longstand- post infection (first the capsule followed by the nurse cell
ing, encysted and calcified larvae of Trichinella spiralis and the larva). The process may lead to the death of the
(fig 4). larvae, but some larvae may survive for years in the same
When confronting the patient with the histological host [2,5]. In a study on 128 patients, 10 years after in-
result of the biopsy, he admitted to having been hospital- fection, no calcifications of residual larvae were detected
ized 30 years anteriorly for a severe form of trichinel- by mammography or muscle biopsy [6]. Muscle calci-
losis. We completed the laboratory workups with IgG- fications were described in the pectorialis muscle using
specific antibodies which were negative mammography [6-8] and in extraocular muscles using
The final interpretation was of diffuse (generalized) computed tomography [9]. We found no report regarding
chronic microcalcific myopathy due to chronic trichinel- the follow-up and the persistence of muscle calcifications
losis. We concluded that no treatment or follow-up was after more than 10 years postinfection.
required. We used the term of “diffuse (generalized) chronic
microcalcific myopathy” for the pathological findings
Discussion in our patient, although PubMed search results did not
retrieve any publication pertaining to this topic. Similar
Trichinellosis has a 2-stage evolution. After 1-4 weeks terms related to the muscle calcifications included “my-
of incubation, the acute-stage trichinellosis develops, ositis ossificans” (heterotopic ossification of muscular
with fever and gastrointestinal manifestations followed tissue, divided into two entities: myositis ossificans pro-
by muscle phase of infection. Myalgia can be severe and gressiva – an autosomal dominant disease, and myositis
associate tenderness, swelling and weakness, sometimes ossificans traumatica) [10,11], “calcinosis” (the abnor-
urticaria, symmetrical periorbital or facial edema and mal deposition of calcium in skin, subcutaneous tissue,
shivering [2,3]. Myocarditis, thromboembolic disease myofascia and muscle related to systemic scleroderma
or encephalitis may complicate the disease course [2,4]. or dermatomyositis) [12] and simple “muscle calcifica-
The chronic stage of disease starts 3-4 weeks later and tion”. Tawfeeq et al [13] used the term calcific myositis
can persist for months or even years [2]. The presence in 2 cases related to COVID-19 infection (streaky cal-
of leucocytosis, eosinophilia and elevated serum muscle cification of the muscles around the shoulders) as they
enzymes are nonspecific findings, thus requiring the use reported the appearance of muscular calcifications during
of the more specific diagnostical procedures for disease the acute phase of myositis. Calcifications found in mus-
confirmation: serologic tests and/or muscle biopsy (rare- cles can also be vascular calcifications associated with
ly needed) [1,2]. arteriosclerosis, chronic renal failure or chronic hyper-
Once the Trichinella larvae enter the myocytes, they calcemia [14]. Muscle calcifications have been also de-
induce a significant inflammatory reaction responsible scribed in other parasitic infections such as cysticercosis
for the myositis. The host cell transforms into a new phe- [15].
notype called “nurse cell”; the sarcomere myofibrils dis- We found no report about the use of US in neither
appear and the larva becomes encapsulated. The progres- acute nor chronic trichinellosis. Indeed, there is no role
sive calcification of larvae may take place after 6 months for imaging techniques in the diagnostic work-up of this
110 Daniela Fodor et al Thousands of muscle microcalcifications after 30 years of Trichinella infection detected by US

parasitosis, but musculoskeletal US has proven a great 5. Machnicka B, Dziemian E, Dabrowska J, Walski M. Cal-
capacity in identifying the small calcification and may cification of Trichinella spiralis larval capsule Parasitol
have an important role in patient follow-up, especially in Res 2005;97:501-504.
6. Harms G, Binz P, Feldmeier H, et al. Trichinosis: a prospec-
long-term symptomatic patients.
tive controlled study of patients ten years after acute infec-
Our first suspected diagnosis was urate myopathy but
tion. Clin Infect Dis 1993;17:637-643.
the generalised microcalcifications coupled with the lack 7. Lahlou H, Gagnon JH, Mesurolle B. Quiz case. Trichi-
of clinical symptoms and, more importantly, the una- nosis associated muscular calcifications. Eur J Radi-
wareness about this specific disease entity, determined us ol 2003;48:220-223.
to perform muscle biopsy. The histopathological result 8. Valdes PV, Prieto A, Diaz A, Calleja M, Gomez JL. Mi-
was indeed unexpected. The US aspect of the muscles crocacification of pectoral muscle in trichinosis. Breast J
was really spectacular; hence, the comparison with the 2005;11:150.
”starry night”. To our knowledge this US aspect of the 9. Behrens-Baumann W, Freissler G. Computed tomo-
pathological muscles has not been previously described graphic appearance of extraocular muscle calcification in
in the literature. a patient with seropositive trichinosis. Am J Ophthalmol
1990;110:709-710.
In conclusion, US detection of muscular calcifica-
10. Aoki T, Naito H, Ota Y, Shiiki K. Myositis ossificans
tions can be a challenge in situations in which the clini- traumatica of the masticatory muscles: review of the
cal aspect is not suggestive for diagnosis. Although rare, literature and report of a case. J Oral Maxillofac Surg
trichinellosis should be taken into consideration when 2002;60:1083‐1088.
assessing the differential diagnosis pertaining to these 11. Folpe AL, Inwards CY. Bone and Soft Tissue Pathology E‐
cases. Book: A Volume in the Foundations in Diagnostic Pathol-
ogy Series: Elsevier Health Sciences; 2009.
References 12. Chander S, Gordon P. Soft tissue and subcutaneous calcifi-
cation in connective tissue diseases. Curr Opin Rheumatol
1. Bruschi F, Chiumiento L. Trichinella inflammatory myo- 2012;24:158-164.
pathy: host or parasite strategy? Parasit Vectors 2011;4:42. 13. Tawfeeq H, Witham F, Dulay GS. COVID-19 related cal-
2. Gottstein B, Pozio E, Nöckler K. Epidemiology, diagnosis, cific myositis cases. BJR Case Rep 2021;7:20200120.
treatment, and control of trichinellosis. Clin Microbiol Rev 14. Singh A, Tandon S, Tandon C. An update on vascu-
2009;22:127-145. lar calcification and potential therapeutics. Mol Biol Rep
3. Kociecka, W. Trichinellosis: human disease, diagnosis and 2021;48:887-896.
treatment. Vet Parasitol 2000;93:365-383. 15. Bustos JA, Garcia HH, Dorregaray R, et al; Cysticercosis
4. Nunes MC, Guimarães Júnior MH, Diamantino AC, Gelape Working Group in Peru. Detection of muscle calcifications
CL, Ferrari TC. Cardiac manifestation of parasitic diseases. by thigh CT scan in neurocysticercosis patients. Trans R
Heart 2017;103:651-658. Soc Trop Med Hyg 2005;99:775-779.

Captions for the movies uploaded to the journal site


Movie 1. Ultrasound examination of the left pectoralis muscles
Movie 2. Ultrasound examination of the right thenar eminence
Movie 3. Ultrasound examination of the extensor part of the
right forearm
Letter to the Editor Med Ultrason 2023, Vol. 25, no. 1, 111-121

Echocardiography in the detection of lead-related infective


endocarditis
Tina Bečić, Vedran Carević, Ružica Perković-Avelini, Damir Fabijanić

Department of Cardiology, University Hospital of Split, Split, Croatia

To the Editor,

A 70-year-old man with a permanent pacemaker (PM)


implanted 10 years ago was admitted because of a febrile
state. During the 7 months period before admission, he
was febrile four times up to 39°C, lasting several days
with general weakness, pain in the back and legs, and
accelerated erythrocyte sedimentation rate and elevated
C-reactive protein recorded, while blood and urine cul-
tures were sterile. Each time he was treated empirically
with antibiotics with short-term improvement.
Two-dimensional transthoracic echocardiography
(2DTTE) indicated a possible mass in the right atrium
(fig 1a). Two and three-dimensional transoesophageal
echocardiography (2DTEE and 3DTEE) revealed mass
on the atrial segment of ventricular lead (fig 1b,c); the
segment of the lead which passes through the tricuspid
valve and surrounding cardiac structures were free of the Fig 1. 2DTTE indicates a possible mass in the right atrium (a);
infection (fig 1d). Staphylococcus aureus was isolated 2DTEE reveals a hypoechoic mobile mass on the atrial segment
from the blood culture. After 4 weeks of antibiotic treat- of the ventricular lead (b); 3DTEE confirmed large vegetations
on the atrial segment of the ventricular lead (c); the lead seg-
ment, the patient underwent a successful extraction of the ment passing through the tricuspid valve and the surrounding
PM system. cardiac structures were free of infection (d).
Lead-related infective endocarditis (LRIE) is a seri-
ous infectious disease developing in patients with cardiac and specificity for their diagnosis and evaluation of the
implantable electronic devices (CIED) [1]. Its specific spread of infection to surrounding cardiac structures [2].
sign is vegetation, a mobile oscillating mass attached to Therefore, 2DTEE is indicated in all patients with suspi-
the CIED lead, which in combination with positive blood cion of LRIE [1]. A 2DTEE probe which directs the ul-
cultures meet a major Duke criterion [1]. trasound plane through a 180-degree arc effectively pro-
2DTTE is the primary imaging technique in the case vides a panoramic image of 360-degree heart structures.
of suspected lead vegetation(s), but with poor sensitivity However, a detailed 2DTEE inspection is hampered by
reverberations and artifacts generated by the electrodes
Received 11.12.2022 Accepted 15.01.2023
which make identification of vegetation(s) near these
Med Ultrason structures difficult [2]. 3DTEE provides a clear, fast and
2023, Vol. 25, No 1, 111-112, DOI: 10.11152/mu-4002, detailed anatomical image in real time providing addi-
Corresponding author: Damir Fabijanic tional information about the appearance of the electrode
Department of Cardiology,
University Hospital of Split,
and its passage through the tricuspid orifice. Compared
21000 Split, Croatia to 2DTEE, 3DTEE enables a better visualization of the
E-mail: damirfabijanic62@gmail.com lead(s) and surrounding cardiac structures and the detec-
112 Tina Bečić et al Echocardiography in the detection of lead-related infective endocarditis

tion of additional vegetations that are often overlooked References


using 2DTEE [2]. Most importantly, 3DTEE allows a de-
1. Polewczyk A, Jachec W, Tomaszewski A, et al. Lead-relat-
tailed anatomical description of the location, size, shape, ed infective endocarditis: factors influencing the formation
and consistency of the vegetation, necessary to evaluate of large vegetations. Europace 2017;19:1022-1030.
the possibility and the best time for lead extraction, as a 2. Almomani A, Siddiqui K, Ahmad M. Echocardiography in
mandatory therapeutic intervention in patients with LRIE patients with complications related to pacemakers and car-
[1]. diac defibrillators. Echocardiography 2014;31:388-399.

EUS-guided drainage for pancreatic duct stone combined with


main pancreatic duct stenosis after pancreaticoduodenectomy:
a case report

Hongfei He, Tingting Yu, Yaoting Li, Senlin Hou, Lichao Zhang

Biliopancreatic Endoscopic Surgery Department, The Second Hospital of Hebei Medical University, Shijiazhuang,
China

To the Editor, stone become complex. We placed a fully covered metal


stent to connect the pancreatic duct and the intestinal lu-
The incidence of pancreaticojejunostomy anasto- men for drainage and expand the narrow pancreatic duct,
motic stricture has been reported in about 5% after pan- a double pigtail plastic stent being placed in the fistula.
creaticoduodenectomy [1], but the main pancreatic duct The patient was discharged after the abdominal pain dis-
stenosis is extremely rare in such cases. appeared. The patient was hospitalized again 4 months
An 81-year-old woman was admitted with epigastric later. We used duodenoscopy to find the double pigtail
pain for two weeks, and the patient had undergone pan- plastic stent, and the guidewire was inserted into the pan-
creaticoduodenectomy for ampullary cancer 8 years ago. creatic duct through the fistula. Fluoroscopy showed that
MRCP showed abnormal small nodules in the pancre- the narrow pancreatic duct had been dilated. After the
atic duct and peripancreatic inflammatory exudation. We stents were removed with forceps, the antegrade inter-
prepared ERCP using balloon-assisted enteroscopy but vention for the stone was successfully performed through
pancreaticojejunostomy anastomotic could not be found. the fistula with a balloon (fig 1).
So, we chose endoscopic ultrasound and the scan showed Faced with patients of pancreaticojejunostomy anas-
that the pancreatic duct in the body of the pancreas was tomotic stricture, the rendezvous technique or ERCP us-
dilated and with strong echoes in the interior. A punc- ing balloon-assisted enteroscopy is preferred, but the ab-
ture needle was inserted into the dilated pancreatic duct solute requirement for both techniques is that endoscopy
and fluoroscopy was performed showing the stone and can always advance to the anastomosis site [2]. For this
the narrow pancreatic duct at the site of the stone incar- case, unobstructed drainage of the pancreatic duct was
ceration, which made the antegrade intervention for the the most important. The elastic tension of the fully cov-
ered metal stent could expand the stenosis and provide
operation space for the antegrade intervention.
Received 21.11.2022 Accepted 15.01.2023
Med Ultrason References
2023, Vol. 25, No 1, 112-113, DOI: 10.11152/mu-3960,
Corresponding author: Lichao Zhang 1. Fujigaki S, Shiomi H, Atalla H, et al. EUS-guided drain-
Biliopancreatic Endoscopic Surgery
Department, The Second Hospital of Hebei
age for a non-dilated pancreatic duct using a re-puncture
Medical University, CN050000, technique in a patient with stricture-related pancreatitis
Shijiazhuang, Hebei province, China (with video). J Hepatobiliary Pancreat Sci 2021;28:e54-
E-mail: zhang.lichao@163.com e55.
Med Ultrason 2023; 25(1): 111-121 113

Fig 1. A. Endoscopic ultrasound showed the pancreatic duct stone in the body of the pancreas; B. Measurement of pancreatic duct
diameter and puncture distance under endoscopic ultrasound; C. The puncture needle was inserted into the dilated pancreatic duct;
D. Fluoroscopy showed the stone and the narrow pancreatic duct at the site of the stone incarceration; E. A fully covered metal stent
and a double pigtail plastic stent was placed; F. Removing the stents with forceps; G. The antegrade intervention for the stone was
successfully performed through the fistula with a balloon.

2. Katanuma A, Hayashi T, Kin T, et al. Interventional endo- anatomy: Techniques and literature review. Dig Endosc
scopic ultrasonography in patients with surgically altered 2020;32:263-274.

Right atrial thrombosis and lymphoblastic leukemia


Fenglin Jiang1, Caijun Han2

1Department of Medical Ultrasound, 2Department of Clinical Laboratory, Yanbian University Hospital, Yanji, Jilin,
China

To the Editor,

A 44-year-old man was diagnosed with acute Ph+


B-lymphocyte leukemia for 3 years. Two years ago, he re-
ceived umbilical cord blood stem cell transplantation and
CD19/CD22 bi-target CAR-T therapy. He was treated
with oral dasatinib since then. This time, the patient came

Received 22.12.2022 Accepted 06.02.2023


Med Ultrason
2023, Vol. 25, No 1, 113-114, DOI: 10.11152/mu-4017,
Corresponding author: Fenglin Jiang
Department of Medical Ultrasound,
Yanbian University Hospital,
#1327 Juzi St.
Yanji 133000, China Fig 1. Echocardiography, four-chamber section showed a
Phone: +86-433-2660056 39.5x28.3 mm hypoechoic mass in the right atrium,and a large
E-mail: jiangfenglin@sina.com amount of pericardial effusion.
114 Fenglin Jiang et al Right atrial thrombosis and lymphoblastic leukemia

to the hospital with chest tightness, with white blood cell Right atrial thrombosis is a rare, but potentially seri-
count of 12.53x109/L and neutrophil count of 8.91x109/L. ous complication of acute lymphoblastic leukemia treat-
Neutrophils 71.10%, lymphocytes 17.5%, monocytes ment. In the Jarvis et al study, 11 (2.7%, 95%CI 1.4-4.9)
11.30%, hemoglobin 106 g/L, platelets 237x109/L. of 406 patients had asymptomatic right atrial thrombosis,
Echocardiography showed a large amount of pericardi- ranging from 10 to 25 mm at detection [1]. Bonanni et al
al effusion. A 39.5x28.3mm weak echo light mass was believed that the right atrial mass in patients with T-cell
seen in the right atrium, and thrombus was considered chronic lymphoblastic leukemia was an abnormal mech-
(fig 1). anism of thrombosis [2].
The main research fields of OncoCardiology include
common risk factors and interventions of cardiovascu- Reference
lar diseases and tumors, cardiovascular complications
1. Jarvis KB, Andersson NG, Giertz M, et al. Asymptomatic
caused by anti-tumor treatment, cardiac tumors and tu-
Right Atrial Thrombosis After Acute Lymphoblastic Leu-
mors combined with cardiovascular diseases. Cardiovas-
kemia Treatment. J Pediatr Hematol Oncol 2021;43:e564-
cular disease and tumors have become the two diseases e566.
with the highest incidence rate. Hematologic diseases oc- 2. Bonanni L, Adami F, Angelini A, et al. Images in cardio-
cur in a series of diseases around hemorrhage and throm- vascular medicine. Right atrial mass in a patient with T-cell
bosis. The common symptoms of leukemia are fever, in- chronic lymphocytic leukemia: an unusual mechanism of
fection and hemorrhage. thrombus formation. Circulation 2007;116:e569-e572.

Evaluation and subsequent treatment for superficial peroneal


entrapment and hypertrophic scar using high-resolution ultrasound

Chia-Yu Kuo1, Kuo-Chang Wei1,2

1Department of Physical Medicine and Rehabilitation, Cathay General Hospital, 2Department of Physical Medicine
and Rehabilitation, National Taiwan University Hospital, Taipei, Taiwan

To the Editor, SPN entrapment neuropathy. A linear transducer was


firstly placed 5 cm proximal to the lateral malleolus to
A 31-year-old healthy female presented with a left an- localize the SPN at the horizontal plane between the per-
kle hypertrophic scar and paresthesia after exposure to a oneus brevis and extensor digitorum longus (EDL) (fig
traffic accident. In addition, the patient also experienced 1a). The transducer was subsequently moved caudally,
paresthesia at the left anterolateral ankle, innervated by and a gradual approximation of the SPN and scar tis-
the superficial peroneal nerve (SPN). sue was noted. The scar tissue was a hypoechoic ovoid
High-resolution ultrasonography (HRUS) was per- mass located superficially to the crural fascia. Eventu-
formed to investigate the integrity of SPN and possible ally, the SPN was compressed underneath the scar tis-
sue (fig 1b). US-guided hydrodissection and nerve block
were performed on the SPN at the site where the SPN
Received 11.12.2022 Accepted 15.01.2023 was about to go beneath the scar (fig 1c). After waiting
Med Ultrason
2023, Vol. 25, No 1, 114-115, DOI: 10.11152/mu-3997,
for 5 min to allow the local anesthetic to work, echo-
Corresponding author: Kuo-Chang Wei, MD guided steroid injection with 10 mg of triamcinolone
Department of Physical Medicine and was performed at the longitudinal plane of the scar
Rehabilitation, Cathay General Hospital (fig 1d).
280, Renai Rd., Da-an Dist.,
Taipei City 106, Taiwan (R.O.C.)
This report showed the value of HRUS in the diag-
E-mail: gordon80446@gmail.com nosis of peripheral nerve pathologies. Although electro-
Phone: 886-972278198 diagnostic studies may provide important physiological
Med Ultrason 2023; 25(1): 111-121 115
information, they are painful and incapable of providing additional morphological information on the injured
structural information. HRUS on the other hand provides nerve [1]. In this case, the hypertrophic scar made the re-
cording of the sensory nerve action potential of the SPN
inaccurate. Therefore, we used HRUS to perform nerve
tracking for the SPN to check the integrity of the nerve
and possible entrapment site.
Currently, intralesional steroid injection is common-
ly used as first-line therapy for hypertrophic scars. Be-
cause significant procedural pain is often reported, and
repeated injections are often required; methods to reduce
pain are important [2]. In this case, HRUS-guided nerve
block prior to intralesional steroid injection completely
relieved the pain of steroid injections. In addition, un-
wanted neurovascular injuries during steroid injection
were avoided under ultrasonography guidance.

References
Fig 1. Ultrasound nerve tracking of the left superficial peroneal
nerve (SPN) (a, b). Note the left SPN was compressed by the 1. Hsueh HW, Wei KC, Fan SP, Wu CH. Ultrasound imaging
scar (b). After nerve tracking was performed, US-guided hydro- and treatment in a rare case with bilateral supinator syn-
dissection and nerve block was performed to the left SPN near
drome. Med Ultrason 2022;24):250-251.
the compression site (c). Subsequent ultrasound-guided intral-
esional steroid injection to the hypertrophic scar was performed 2. Morelli Coppola M, Salzillo R, Segreto F, Persichetti
at the longitudinal plane of the scar (d). Again, note that the P. Triamcinolone acetonide intralesional injection for
SPN run right underneath the hypertrophic scar. Arrow, SPN; the treatment of keloid scars: patient selection and per-
arrowhead, needle; asterisk, anechoic dextrose solution; circled spectives. Clin Cosmet Investig Dermatol 2018;11:387-
area, hypertrophic scar; LM, lateral malleolus. 396.

EUS-guided fine needle biopsy for hepatocarcinoma of the right liver


lobe as a rescue diagnostic technique after a negative percutaneous-
guided liver biopsy
Alina Ioana Tantau1, Teodor Zaharie2

14th
Medical Clinic, Gastroenterology Department, 23rd Medical Clinic, Histopathology Department, ”Iuliu Hațieganu”
University of Medicine and Pharmacy, Cluj-Napoca, Romania

To the Editor, decade, endoscopic ultrasound (EUS)-tissue acquisition


using fine needle aspiration (FNA) or fine needle biopsy
Transjugular and percutaneous approaches are the (FNB) from left and, more recently, right lobe of the liver
most common techniques for liver biopsy [1]. In the last has been developed [2-4]. EUS-liver biopsies were com-
pared with other techniques such as computed tomogra-
Received 06.12.2022 Accepted 15.01.2023 phy or ultrasound (US) in terms of diagnostic accuracy
Med Ultrason of hepatic tumors [5]. The majority of the studies found
2023, Vol. 25, No 1, 115-116, DOI: 10.11152/mu-3993, similar results between those techniques with a high di-
Corresponding author: Alina Ioana Tantau
CF Hospital, 18, Republicii street,
agnostic accuracy varying between 90-100% [5]. Recent
400015, Cluj-Napoca studies reported the utility of EUS-FNA or FNB on right
E-mail: alitantau@gmail.com liver masses [2-3]. Adequate specimen is significantly
116 Alina Ioana Tantau et al EUS-guided fine needle biopsy for hepatocarcinoma of the right liver lobe

higher in the left lobe versus right lobe but technical suc- The width of tissue fragments measured 0.5-0.8 mm. The
cess and diagnostic accuracy for liver masses were simi- positivity of MCK (citokeratin, multi), GLY (glypican-3)
lar in both lobes [2-4]. (fig 1b), HAS (hepatocyte specific antigen) markers and
We present the case of a man of 77 years old, com- the lack of mCEA (monoclonal carcinoembryonic anti-
plaining of nausea and weight loss. Physical examination gen), CD34, CD56 markers brought us to the final di-
revealed a large painless liver. Abdominal US examina- agnosis of fibrolamellarhepatocarcinoma associated with
tion detected a large right liver mass, more probably a virus B infection.
hepatocarcinoma (HCC). A US-guided liver biopsy was The EUS-guided tissue acquisition can be a suitable
performed with inconclusive histological examination. technique in either cirrhotic or non-cirrhotic patients
Therefore, we decided to perform liver biopsy guided by with suspected HCC in order to provide an accurate his-
EUS. We used 22 gauge FNB needle (22-G Franseen-tip topathological diagnosis [1].
needle, Acquire, Boston Scientific Incorporated, Boston,
Massachusetts, United States). Two passes of FNB with References
at least ten ”back and forward” procedures per pass was
1. European Association for the Study of the Liver. EASL
performed. There were 2 tissue fragments per pass (fig
Clinical Practice Guidelines: Management of Hepatocel-
1a). Size of fragments ranged from 30-100 mm in length.
lular carcinoma. J Hepatol 2018;69:182-236.
2. Oh D, Seo DW, Hong SM, et al. Endoscopic ultrasound-
guided fine-needle aspiration can target right liver mass. En-
dosc Ultrasound 2017;6:109–115.
3. Zhang L, Cai Z, Rodriguez J, Zhang S, Thomas J, Zhu H.
Fine needle biopsy of malignant tumors of the liver: a retro-
spective study of 624 cases from a single institution experi-
ence. Diag Pathol 2020;15:43 .
4. Chen F, Bao H, Deng Z, Zhao Q, Tian G, Jiang TA. En-
doscopic ultrasound-guided sampling using core biopsy
needle for diagnosis of left-lobe hepatocellular carcinoma
in patients with underlying cirrhosis. J Cancer Res Therap
Fig 1. a) EUS-FNB liver. Macroscopic on-site evaluation. 2020;16:1100-1105.
Visible core optain after EUS-FNB. The bleu arrow indicates 5. Pineda JJ, Diehl DL, Miao CL, et al. EUS-guided liver bi-
a ten-pink core, the red arrow indicates a hemorrhagic core; opsy provides diagnostic samples comparable with those
b) Immunohistochemistry. Diffusely positive glypican 3 (GLY-3) via the percutaneous or transjugular route. Gastrointest En-
staining (blue arrow), multiple 40x dosc 2016;83:360–365.

Flexor hallucis brevis’ trigger point and dry needling treatment:


a myofascial pain syndrome perspective on big toe pain
Mustafa Hüseyin Temel1, Elif Özyiğit2

1Physical
Medicine and Rehabilitation Clinic, Üsküdar State Hospital, 2Physical Medicine and Rehabilitation Clinic,
Kanuni Sultan Süleyman Training and Research Hospital, İstanbul, Turkey

To the Editor,
Received 14.12.2022 Accepted 15.01.2023
Med Ultrason
2023, Vol. 25, No 1, 116-117, DOI: 10.11152/mu-3987, One of the most common areas of the foot to experi-
Corresponding author: Mustafa Hüseyin Temel ence pain is the big toe joint, also known as the first meta-
Clinic of Physical Medicine and Rehabilitation,
Üsküdar State Hospital, İstanbul, Turkey
tarsophalangeal joint. Pain frequently manifests gradual-
Phone: +90 216 474 79 00 ly over a period of years, but it can also strike suddenly as
E-mail: mhuseyintemel@gmail.com a result of an injury [1]. The pain in the big toe negatively
Med Ultrason 2023; 25(1): 111-121 117
tect the joints, nerves and vessels in the application area
from possible damage. The ultrasound probe is placed
perpendicular to the plantar axis. Needling is performed
using the out of plane technique. A 0.25x25 mm needle
is used (fig 1). The muscle is needled with the peppering
method. Although there is no consensus in the literature,
dry needling treatment is recommended to be performed
once a week for a total of 3 sessions. It should also be
noted that MPS can be a condition that can cause pain
on its own, or it can be an entity accompanying another
Fig 1. Positioning of the ultrasound probe and ultrasound-guid- pathology.
ed needling of the flexor hallucis brevis muscle: a) positioning
of the utrasound probe; b) ultrasound-guided needling of the References
flexor hallucis brevis muscle (FHB: Flexor Hallucis Brevis,
MTH: Metatarsal Head, ADHO: Adductor Obliquus Hallucis) 1. Gilheany MF, Landorf KB, Robinson P. Hallux valgus and
hallux rigidus: a comparison of impact on health-related
affects quality of life, regardless of the underlying pathol- quality of life in patients presenting to foot surgeons in Aus-
ogy [2]. Myofascial pain syndrome (MPS) is one of the tralia. J Foot Ankle Res 2008;1:1-6.
most frequent and overlooked causes of musculoskeletal 2. Abhishek A, Roddy E, Zhang W, Doherty M. Are hallux
pain, which is a result of the myofascial trigger points valgus and big toe pain associated with impaired quality
(MTrPs) that are located in muscle tissue [3]. The flexor of life? A cross-sectional study. Osteoarthritis Cartilage
hallucis brevis is an essential muscle that may have MTrP 2010;18:923-926.
when examining patients with big toe pain [4,5]. It is dif- 3. Graff-Radford SB: Myofascial pain: diagnosis and manage-
ment. Curr Pain Headache Rep 2004;8:463-467.
ficult to diagnose when the MTrP of this muscle, which
4. Travell JG, Simons DG. Myofascial pain and dysfunction:
should be considered in the differential diagnosis of big
the trigger point manual. Lippincott Williams & Wilkins,
toe pain, are not viewed from the perspective of MPS. 1992.
In ultrasound-guided dry needling of the flexor hallu- 5. Yıldızgören M, Bağcıer F. Miyofasiyal ağri sendromu ve
cis brevis muscle; the patient is placed in a supine posi- kuru iğneleme Kas, Tendon, Ligament ve Fasyaların Ma-
tion with the hip in external rotation and the knee in 90º nuel Palpasyon Tekniğiyle ve Ultrason Rehberliğinde Kuru
flexion. It is important to use ultrasound guidance to pro- İğnelemesi 2022.

Intramural ectopic pregnancy at 21 weeks of gestation


Yuting Wei, Jin Wang, Hong Luo

Department of Ultrasound, West China Second University Hospital, Sichuan University, Key Laboratory of Birth
Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Chengdu, China

To the Editor, patient had a laparoscopic myomectomy (9x8 cm) eight


years earlier. A previous ultrasound (US) that the pa-
A 25-year-old woman (G1P0), at 21 6/7 weeks gesta- tient underwent showed an intrauterine pregnancy with
tion, presented with severe lower abdominal pain. The no acute abnormalities. Urgent US demonstrated a large
volume of hemoperitoneum. About 20 ml of incoagula-
Received 04.01.2023 Accepted 29.01.2023
Med Ultrason ble blood was extracted from her right middle abdomen.
2023, Vol. 25, No 1, 117-118, DOI: 10.11152/mu-4033, The patient was consented for emergency laparotomy
Corresponding author: Prof. Hong Luo, Department of Ultrasound, and rupture of the posterior uterine wall was observed
West China Second University Hospital,
No. 20, Section 3, South Renmin Road,
intraoperatively. The pregnancy was not communicated
Chengdu, Sichuan Province 610041, China with the endometrial cavity and fallopian tubes, which
E-mail: luohongcd1969@163.com was consistent with intramural ectopic pregnancy. A still-
118 Yuting Wei et al Intramural ectopic pregnancy at 21 weeks of gestation

birth was removed and uterine-conserving surgery was


performed. The patient went home in stable condition on
postoperative day 7.
Retrospective review of US images of the patient
was performed. Ultrasonography at 6 1/7 weeks gesta-
tion showed the gestational sac was located within 5 mm
of the uterine serosa (fig 1a). Ultrasonography at 12 0/7
weeks gestation presented the loss of clear zone under
the placental bed, which was a sign of placenta accreta
spectrum (fig 1b). Color Doppler ultrasonography at 21
5/7 weeks gestation presented retroplacental hypervas-
cularity and thin myometrium between the endometrium
and the amniotic sac (fig 1c). The postoperative pathol-
ogy reported that villi invaded posterior myometrium
(fig 1d).
Intramural ectopic pregnancy is the rarest form of ec- Fig 1. a) Greyscale and color Doppler ultrasonography images
topic pregnancy, accounting for less than 1% of ectopic at 6 1/7 weeks of gestation. Gestational sac (white arrow), lo-
pregnancies. It refers to a gestational sac surrounded by cated within 5 mm of the uterine serosa (red arrow). b) Ultra-
the uterine wall without connection to the endometrial sonography image at 12 0/7 weeks gestation presented the loss
of clear zone under the placental bed. (P) placenta. c) Color
cavity and fallopian tubes [1]. The risk of rupture of in- Doppler ultrasonography at 21 5/7 weeks gestation showed thin
tramural pregnancy increases with the increase of the myometrium between the endometrium (red arrow) and the
gestational age. Uterine trauma caused by surgical pro- amniotic sac (white arrow). d) Postoperative pathology showed
cedures including myomectomy, dilatation and curettage that villi invaded posterior myometrium.
are predisposing factors for intramural ectopic pregnancy
[2]. The treatment depends on the location and size of the References
gestational sac, the extent of myometrial involvement,
gestational age at diagnosis and future fertility inten- 1. Zhang Q, Xing X, Liu S, et al. Intramural ectopic preg-
tions [3]. Although intramural pregnancy is a rare form nancy following pelvic adhesion: case report and lit-
of ectopic pregnancy, early diagnosis is essential for the erature review. Arch Gynecol Obstet 2019;300:1507-
prevention of severe hemorrhage and loss of reproduc- 1520.
2. Chaikof M, Hobson S, Sobel M. Fundal intramural ectopic
tive function.
pregnancy. CMAJ 2020;192:E1211.
3. Shen Z, Liu C, Zhao L, et al. Minimally-invasive manage-
Acknowledgement: this work was supported by the ment of intramural ectopic pregnancy: an eight-case series
Sichuan Science and Technology Plan Project (Grant No. and literature review. Eur J Obstet Gynecol Reprod Biol
2022YFS0086) 2020;253:180-186.
Med Ultrason 2023; 25(1): 111-121 119

Ultrasound imaging and guided intervention for the middle cluneal


nerve

Wei-Ting Wu1,2, Yu-Chun Hsu1, Kamal Mezian3, Vincenzo Ricci4, Ke-Vin Chang1,2,5,
Levent Özçakar6

1Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Bei-Hu Branch, Taipei,
Taiwan,2Department of Physical Medicine and Rehabilitation, National Taiwan University College of Medicine,
Taipei, Taiwan, 3Department of Rehabilitation Medicine, First Faculty of Medicine and General University Hospital,
Charles University in Prague, Prague, Czech, 4Physical and Rehabilitation Medicine Unit, Luigi Sacco University
Hospital, ASST Fatebenefratelli- Sacco, Milan, Italy, 5Center for Regional Anesthesia and Pain Medicine, Wang-Fang
Hospital, Taipei Medical University, Taipei, Taiwan, 6Department of Physical and Rehabilitation Medicine, Hacettepe
University Medical School, Ankara, Turkey

To the Editor, ina, piercing [1] or running superficial to [2] the LPSL
between the posterior superior and posterior inferior il-
A 55-year-old female suffered from right lower back iac spines. They supply the cutaneous sensation of the
and gluteal pain for the last year. Her symptoms aggra- medial aspect of gluteus maximus muscle. The average
vated after prolonged sitting and walking. Physical ex- width of the MCNs in cadaveric specimens is 1.6 mm [3]
amination revealed tenderness with tingling sensation when traveling into the LPSL. There are three common
over the right sacroiliac joint (SIJ). Plain pelvic radiog- causes of MCN injury: LPSL sprain, iatrogenic injury
raphy showed normal bony alignment. As the pain could during SIJ injection, and overstretching of the gluteus
not be relieved by physical therapy, oral medication, and maximus.
corticosteroid injection in the SIJ, she was referred for ul- In patients with MCN entrapment, pain can devel-
trasound-guided middle cluneal nerve (MCN) block (fig op around the SIJ with possible radiation to the lower
1A). The transducer was first placed on the right SIJ par- back, gluteus, and lower extremity [4]. Tenderness can
allel to the 2nd sacral foramina (fig 1B). Then the medial be reproduced when pressure is applied inferolateral to
end of the transducer was pivoted caudally toward the the LPSL or 35 mm caudal to the posterior superior iliac
lateral sacral crest (fig 1C). The MCN could be seen axi- spine [5]. Since the MCNs can be identified using the
ally, inside the long posterior sacroiliac ligament (LPSL). high-frequency transducer placed between the posterior
Betamethasone (1 ml, 4 mg) mixed with lidocaine (2 ml, superior iliac spine and lateral sacral crest, whereas ultra-
1%) was administered using the in-plane approach to tar- sound-guided injection can be used for a diagnostic/ther-
get the nerve branches (fig 1D, Video 1, on the journal apeutic block. Lastly, if synovitis/arthritis of the SIJ is
site). The second injection was given two weeks later, present, the underlying disease should also be thoroughly
and she described total pain relief thereafter. managed to avoid recurrent entrapment.
The MCNs are derived from the dorsal rami of the
sacral nerves S1-S3. The nerves exit the sacral foram- Acknowledgment: The study was made possible by
(1) the research funding of the Community and Geriatric
Medicine Research Center, National Taiwan University
Received 01.04.2022 Accepted 29.01.2023 Hospital, Bei-Hu Branch, Taipei, Taiwan; (2) Ministry of
Med Ultrason
Science and Technology (MOST 106-2314-B-002-180-
2023, Vol. 25, No 1, 119-120, DOI: 10.11152/mu-4032,
Corresponding author: Ke-Vin Chang MY3, 109-2314-B-002-114-MY3 and 109-2314-B-002-
Department of Physical Medicine and 127), and (3) Taiwan Society of Ultrasound in Medicine.
Rehabilitation, National Taiwan University
Hospital Bei-Hu Branch, No. 87, Nei-Jiang Rd., References
Wan-Hwa District, Taipei 108, Taiwan
E-mail: kvchang011@gmail.com 1. Aota Y. Entrapment of middle cluneal nerves as an unknown
Phone: +886223717101-5309 cause of low back pain. World J Orthop 2016;7:167-170.
120 Wei-Ting Wu et al Ultrasound imaging and guided intervention for the middle cluneal nerve

Fig 1. The schematic drawing shows the course of the middle cluneal nerves (A). The transducer is first placed on the sacroiliac
joint (B), and then its medial end is pivoted 90 degrees caudally, toward the lateral edge of the sacral crest (C). The needle is inserted
using the in-plane approach to target the middle cluneal nerves in the short-axis (D). Yellow line and white arrowheads: branches of
the middle cluneal nerve; black arrows: needle; green shade and green dashed lines: long posterior sacroiliac ligament. S: sacrum; I:
ilium; LPSL: long posterior sacroiliac ligament; SPSL: short posterior sacroiliac ligament; PSIS: posterior superior iliac spine; LSC:
lateral edge of the sacral crest.

2. Tubbs RS, Levin MR, Loukas M, Potts EA, Cohen-Gadol 4. Karri J, Singh M, Orhurhu V, Joshi M, Abd-Elsayed A. Pain
AA. Anatomy and landmarks for the superior and mid- Syndromes Secondary to Cluneal Nerve Entrapment. Curr
dle cluneal nerves: application to posterior iliac crest Pain Headache Rep 2020;24:61.
harvest and entrapment syndromes. J Neurosurg Spine 5. Matsumoto J, Isu T, Kim K, Iwamoto N, Morimoto D,
2010;13:356-359. Isobe M. Surgical treatment of middle cluneal nerve en-
3. Konno T, Aota Y, Saito T, et al. Anatomical study of middle trapment neuropathy: technical note. J Neurosurg Spine
cluneal nerve entrapment. J Pain Res 2017;10:1431-1435. 2018;29:208-213.

Ultrasonographic and pathological findings of a secretory carcinoma


of the parotid gland
Xiaowei Zhang1, Dandan Wu1, Jun Chen2

1Department of Pathology, 2Department of Imaging Medicine, Affiliated Dongyang Hospital of Wenzhou Medical
University, Dongyang, Zhejiang, P.R. China

Dear Editor, tient 2 months prior to admission as a broad, bean-sized


mass. The patient did not report associated pain or fa-
A 48-year-old male patient was admitted because of a cial numbness. A 1.0×1.0 cm mass was found behind the
posterior right ear mass, which was first noted by the pa- right ear; it was mobile with clear boundaries and was not
associated with redness or tenderness. No swelling was
Received 21.11.2022 Accepted 29.01.2023 noted in the lymph nodes of the neck.
Med Ultrason Ultrasonography revealed a hypoechoic nodule in the
2023, Vol. 25, No 1, 120-121, DOI: 10.11152/mu-3962,
right parotid gland, approximately 14×11×11 mm in size,
Corresponding author: Jun Chen
Department of Imaging Medicine, Dongyang with a well-defined border and an uneven internal echo.
Hospital Affiliated with Wenzhou Medical An irregular dark liquid area was present. Color Dop-
University, No. 60 West Wuning Road, pler flow imaging detected a few blood flow signals (fig
Dongyang, Zhejiang, 322100, P.R. China
Phone/fax: +86 18868579300
1a, 1b). Postoperative pathology after surgical resection
+86 057989605211 confirmed the diagnosis of secretory carcinoma of the
E-mail: 547635310@qq.com right parotid gland with immunohistochemistry: CK7+,
Med Ultrason 2023; 25(1): 111-121 121
CK19+, S-100+, CK20+, SMA-, Desmin-, P63-, DOG-1-, Parotid secretory carcinomas are salivary gland tu-
Mammaglobin+, and Ki-67 (+, 5%) (fig 1c, 1d). mors morphologically similar to those seen in breast se-
cretory carcinomas and harbor a specific ETV6-NTRK3
fusion [1]. Secretory carcinomas of the parotid gland are
usually characterized by occurring singularly, with dif-
ferent lesion locations and poor blood supply. They have
been misdiagnosed as benign tumors of the parotid gland,
as they present as a solid hypoechoic nodule that lacks
the sonographic characteristics of typical parotid gland
malignancy.
Parotid secretory carcinomas are usually low-grade
malignancies and have relatively good prognoses. Local
recurrence and local lymph node metastasis may occur,
but distant metastasis is rare [2]. The first-line treatment
option is the complete surgical resection of the tumor,
followed by local radiotherapy.

References
Fig 1. a) A hard hypoechoic nodule is visible in the right parot-
1. Min FH, Li J, Tao BQ, et al. Parotid mammary analogue
id gland. b) A few blood flow signals are seen on color Doppler
flow imaging; c) The tumor displays a microcystic and pap- secretory carcinoma: a case report and review of literature.
illary structure, with small to medium-large cells containing World J Clin Cases 2021;9:4052-4062.
abundant and eosinophilic cytoplasm (Hematoxylin and Eosin 2. Forner D, Bullock M, Manders D, et al. Secretory carcino-
stain ×200); d) Tumor cells are positive for S100 (Immunohis- ma: the eastern Canadian experience and literature review.
tochemistry ×200). J Otolaryngol Head Neck Surg 2018;47:69.
Guidelines for Authors
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references, tables, legend. Do not insert here the name of the of obtaining free fluid. Radiology 1982;142:163-164.
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ordering reprints. Ultrasonography. Oslo, The Nicer Year Book 1996:55-82.

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