Ep ssp
Ep ssp
Ep ssp
www.elsevier.com/locate/ymse
a
Center for Interdisciplinary Research in Rehabilitation and Social Integration, Quebec City, Quebec, Canada
b
School of Rehabilitation Sciences, Faculty of Medicine, Universite Laval, Quebec City, Quebec, Canada
c
La Trobe Sport and Exercise Medicine Research Centre, La Trobe University, Melbourne, Victoria, Australia
d
Research Unit in Physio – and Occupational Therapy, Department of Physio- and Occupational Therapy, Lillebaelt
Hospital - Vejle, Vejle, Denmark
e
Orthopaedic Clinical Research Unit, Maisonneuve-Rosemont Hospital Research Center, University of Montreal Affiliated
Research Center, Montreal, Canada
f
School of Rehabilitation, Faculty of Medicine, University of Montreal, Montreal, Canada
g
Therapy Department, Central London Community Healthcare National Health Service Trust, Finchley Memorial
Hospital, London, UK
h
School of Health Sciences, University of Nottingham, Nottingham, UK
i
School of Life and Health Sciences, University of Nicosia, Nicosia, Cyprus
j
Clinical Therapies, University of Limerick, Limerick, Ireland
k
Research Unit of Musculoskeletal Function and Physiotherapy, Department of Sports Science and Clinical Biomechanics,
University of Southern Denmark, Odense, Denmark
l
Orthopaedic Department, Shoulder Unit, Lillebaelt Hospital, Vejle Hospital, Vejle, Denmark
The RoCTEX trial was approved by the Regional Scientific Ethics Committee *Reprint requests: Marc-Olivier Dube, PT, PhD, Centre for Inter-
of Southern Denmark (S-20130071) and the Dube et al trial was approved by disciplinary Research in Rehabilitation and Social Integration, 525,
the Research Ethics Committee of Centre integre universitaire de sante et de Boulevard Wilfrid-Hamel, office H-0616, Quebec City, Quebec G1M
services sociaux de la Capitale-Nationale (CIUSSS-CN) (#2019-1762). 2S8, Canada.
1
Marc-Olivier Dube and Kim Gordon Ingwersen contributed equally as E-mail address: marc-olivier.dube.1@ulaval.ca (M.-O. Dube).
first co-authors.
1058-2746/Ó 2024 The Author(s). This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
https://doi.org/10.1016/j.jse.2024.03.055
Therapeutic exercises and supraspinatus tendon thickness 1919
m
Orthopaedic Department, Shoulder Unit, Aalborg University Hospital and Department of Clinical Medicine, Aalborg
University, Aalborg, Denmark
n
School of Allied Health, Faculty of Education and Health Sciences, University of Limerick, Limerick, Ireland
o
Ageing Research Centre, Health Research Institute, University of Limerick, Limerick, Ireland
Background: The mechanistic response of rotator cuff tendons to exercises within the context of rotator cuff-related shoulder pain
(RCRSP) remains a significant gap in current research. A greater understanding of this response can shed light on why individuals
exhibit varying responses to exercise interventions. It can also provide information on the influence of certain types of exercise on ten-
dons. The primary aim of this article is to explore if changes in supraspinatus tendon thickness (SSTT) ratio differ between exercise
interventions (high load vs. low load). The secondary aims are to explore if changes in SSTT ratio differ between ultrasonographic ten-
dinopathy subgroups (reactive vs. degenerative) and if there are associations between tendinopathy subgroups, changes in tendon thick-
ness ratio, and clinical outcomes (disability).
Methods: This study comprises secondary analyses of the combined dataset from two randomized controlled trials that compared high
and low-load exercises in patients with RCRSP. In those trials, different exercise interventions were compared: 1) progressive high-load
strengthening exercises and 2) low-load strengthening with or without motor control exercises. In 1 trial, there was also a third group that
was not allocated to exercises (education only). Ultrasound-assessed SSTT ratio, derived from comparing symptomatic and asymptom-
atic sides, served as the primary measure in categorizing participants into tendinopathy subgroups (reactive, normal and degenerative) at
baseline.
Results: Data from 159 participants were analyzed. Two-way repeated measures ANOVAs revealed significant Group (P < .001) and
Group Time interaction (P < .001) effects for the SSTT ratio in different tendinopathy subgroups, but no Time effect (P ¼ .63).
Following the interventions, SSTT ratio increased in the "Degenerative" subgroup (0.14 [95% confidence interval {CI}: 0.09-0.19]),
decreased in the "Reactive" subgroup (0.11 [95% CI: 0.16 to 0.06]), and remained unchanged in the "Normal" subgroup
(0.01 [95% CI: 0.04 to 0.02]). There was no Time (P ¼ .21), Group (P ¼ .61), or Group Time interaction (P ¼ .66) effect for
the SSTT ratio based on intervention allocation. Results of the linear regression did not highlight any significant association between
the tendinopathy subgroup (P ¼ .25) or change in SSTT ratio (P ¼ .40) and change in disability score.
Conclusion: Findings from this study suggest that, over time, SSTT in individuals with RCRSP tends to normalize, compared to the
contralateral side, regardless of the exercise intervention. Different subgroups of symptomatic tendons behave differently, emphasizing
the need to potentially consider tendinopathy subtypes in RCRSP research. Future adequately powered studies should investigate how
those different tendinopathy subgroups may predict long-term clinical outcomes.
Level of evidence: Level II; Randomized Controlled Trial; Treatment Study
Ó 2024 The Author(s). This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Keywords: Supraspinatus; ultrasound; shoulder; tendinopathy; thickness; rotator cuff-related shoulder pain
Shoulder pain affects up to 56% of the population Doppler ultrasound (US) imaging.8,34,42,52 One model of
yearly.17,35 A vast proportion of shoulder pain complaints tendon pain and pathology, known as the continuum model
may be labeled as rotator cuff-related shoulder pain of tendinopathy, classifies tendinopathy as reactive (char-
(RCRSP).57 Based on the definition of the International acterized by tendon thickening, and hypoechoic areas), or
Scientific Tendinopathy Symposium Consensus, RCRSP degenerative (characterized by tendon thinning and/or
may be defined as persistent pain and loss of function tearing).5,6,31,38
related to mechanical loading on the rotator cuff tendons.50 Many nonsurgical interventions have been suggested as
RCRSP leads to decreased function and quality of life29 as surgical management of RCRSP has not proven to be more
well as increased healthcare usage55 especially since 40%- effective than nonsurgical ones.22 Therapeutic exercise
50% of individuals with shoulder pain experience persistent being one of the advocated nonsurgical option, with sup-
or recurrent pain within the 12 months after initial porting evidence that it is associated with moderate effect
onset.7,13,26 sizes for pain and disability reduction when compared to a
Our understanding of RCRSP has evolved from a bio- placebo or no intervention.51 One aim of therapeutic ex-
logical model,28,43 to one that also includes psychosocial ercise is to induce beneficial mechanical stress to induce
factors that are likely to contribute to the persistence of changes in the rotator cuff tendons, notably decreased
pain.3,4 Although these psychological factors can play a tendon thickness in those whose tendinopathy can be
crucial role, it is important not to discard the biological classified as reactive and increased tendon thickness in
factors that may contribute to the onset and persistence of those whose tendinopathy can be classified as degenera-
pain. Structural pathology is commonly observed in tive.2,23 In healthy tendons, higher loads have been asso-
RCRSP, with changes such as tendon thickening or thin- ciated with an increased cross-sectional area,1,27 while the
ning, neovascularization, decreased tendon stiffness, and opposite seems to happen in pathological reactive tendons
hypoechoic appearance visible on greyscale or power where higher loads such as heavy-slow resistance exercise
1920 M.-O. Dube et al.
program have been associated with a decrease in cross- external rotation). Patients with other shoulder-related diagnoses
sectional area.25 There is no evidence regarding the not relating to RCRSP (eg, capsulitis, instability), bilateral
behavior of degenerative rotator cuff tendons following shoulder complaints, competing diagnoses, full-thickness rotator
loading in vivo in a symptomatic population. Trials of ex- cuff tears, large calcifications, or corticosteroid injection within
the past six weeks were excluded. Eligibility criteria were
ercise for reactive patellar and Achilles tendinopathy have
verified by a physiotherapist and participants were recruited
shown a decrease in tendon thickness in response to 12-
from shoulder units within the outpatient clinics of orthopedic
week exercise programs, with positive associations departments of 3 hospitals in the western part of Denmark for
between structural changes and patient-reported out- Ingwersen et al, and through advertisements in local physio-
comes.24,25,44 This could also apply for RCRSP, as the therapy clinics (Quebec, Canada), electronic mailing lists of
majority of cross-sectional studies evaluating tendon Universite Laval (Quebec, Canada) as well as social media for
thickness in symptomatic populations have mostly high- Dube et al.
lighted an increased tendon thickness.18,41,52 However, no
published trials have evaluated the changes in tendon Interventions
thickness in response to different exercise programs for
RCRSP. Both trials compared an exercise regimen with higher loads to an
Thus, this article presents secondary analyses of pooled exercise regimen with lower loads. More details about the in-
data from two randomized controlled trials10,21 looking at terventions are presented below and can be found in the respective
the effect of different exercise regimens on pain, disability, articles.11,10,19,21 In both trials, the low-load interventions
and supraspinatus tendon thickness (SSTT) in adults with included a larger number of repetitions (>15) and no significant
RCRSP. The primary aim of the current article is to explore external load. On the other hand, the high-load interventions
included in both trials aimed to increase strength by inducing a
if changes in SSTT differ between interventions (high load
sufficient load on the musculotendinous unit. In those in-
vs low load exercises). Based on previous findings in the
terventions, the number of repetitions was smaller (4-8 RM), and
lower limb literature, our hypothesis was that high load the external load applied was larger. Although not identical, the
exercises would lead to a greater reduction in tendon shared attributes of the interventions in both trials prompted us to
thickness compared to low load exercises. The secondary consider their integration to achieve the study’s objectives.
aims are to explore if changes in SSTT differ between ul-
trasonographic tendinopathy subgroups (reactive vs. RoCTEx trial
degenerative) and if there are associations between ten- In the RoCTEx trial, patients were randomly assigned to follow
dinopathy subgroups, changes in tendon thickness, and either the intervention program consisting of 12 weeks of pro-
clinical outcomes (disability). gressive high load exercises (PHLE) (gradually increasing the
load from 15 repetitions maximum (RM) in week 1, to 6 RM in
weeks 9 to 12) (n ¼ 28), or the control group consisting of
Materials and methods 12 weeks of low load exercises (LLE) (20-25 RM from weeks
1-12) (n ¼ 40).
In general, both groups received the same 6 exercises, spe-
Study design
cifically addressing the scapular and rotator cuff muscles. The
program consisted of 2 exercises for strengthening the rotator cuff
Results presented in this article are derived from secondary ana- muscles (push-up plus exercise and low row exercise), 2 exercises
lyses of pooled results from two randomized controlled trials for the scapulothoracic muscles (scaption and side-lying external
comparing high and low-load exercise for RCRSP.10,21 Both trials rotation), and 2 stretching and mobilizing exercises (posterior
obtained informed consent from participants. The RoCTEX trial capsule stretch and scapula retraction). The program was designed
was approved by the Regional Scientific Ethics Committee of to generate the same total load and time under tension in both
Southern Denmark (S- 20130071) and the Dube et al trial was groups. Further, attention and basic information about ergonomic
approved by the Research Ethics Committee of Centre Integre corrections related to daily use of the upper extremity were pro-
Universitaire de Sante et de Services Sociaux de la Capitale- vided. Both groups were recommended to perform home-based
Nationale (CIUSSS-CN) (#2019-1762). exercises 3 times per week and were offered 6 follow-up one-to-
one sessions at the physiotherapy department. Exercise
Participants instructions follow-up sessions were performed by trained phys-
iotherapists, following the standardized exercise regime described
Participants included in this study were adults with persistent in a previous article.19 Patients were blinded toward the specific
RCRSP who were included in either the Dube et al or Ingwersen difference regarding load adjustments in the 2 groups and were
et al (RoCTEx) trials.10,21 Detailed information about eligibility merely told that 2 different active treatment approaches were
criteria, which were similar in both trials, are presented in the compared.
respective articles.11,10,19,21 In summary, eligible participants One thing to note is that 34 participants (17 in both groups)
were adults aged 18-65 years with shoulder complaints lasting received a corticosteroid injection at baseline before starting their
for at least three months, presenting with a combination of 12-week exercise program. There was a significant interaction
positive clinical tests (painful arc, Neer and/or Hawkins Ken- between corticosteroid injection and type of exercise. This inter-
nedy and/or Jobe, and painful resisted isometric abduction or action highlighted a nonsignificant disability decrease in favor of
Therapeutic exercises and supraspinatus tendon thickness 1921
PHLE for patients receiving a corticosteroid injection. This is plane of the supraspinatus tendon just anterior to the acromion
relevant as both corticosteroid and anesthetic (eg, lidocaine) have with tuberculum major visible in the lateral part of the image.
the potential to reduce tenocyte numbers that may reduce the From the most lateral part of the insertion of the supraspinatus on
amount of proteoglycan which will reduce water content and lead the tuberculum major, a 20 mm line was drawn medial to a point
to a reduction in tendon thickness.32,30 where the line crosses the humeral head. From this point, a
perpendicular line from the caput was drawn to the superior
Dub
e et al trial border of the supraspinatus tendon, corresponding to the thick-
In the other trial, participants were allocated to an intervention ness of the supraspinatus tendon. Inter-rater reliability is excel-
comprising progressive high-load strengthening exercises com- lent (ICC: 0.85-0.90) for this standardized procedure.20 In the
bined with an education component or low-load motor control Dube et al trial, US measurements of supraspinatus tendon
exercises combined with an education component. In addition, thickness were obtained with the medial aspect of the wrist
there was a third group that only received the education compo- against the ipsilateral anterior superior iliac spine. Measures
nent without being instructed on any specific exercises. were obtained with the transducer perpendicularly, 1 cm behind
The strengthening exercises program was a 12-week progres- to the anterolateral aspect of the surface of the acromion. The
sive high-load exercises program that targeted humeral internal/ thickness of the SS tendon borders was defined inferiorly as the
external rotators, abductors, and the scapular muscles through 7 first hyperechoic region above the anechoic articular cartilage of
different exercises. Number of repetitions was 1 set of the the humeral head, and the hyperechoic superior border of the
maximum number of repetitions until muscular fatigue. The load tendon before the anechoic subdeltoid bursa. These US tendon
was 90% of 1 RM, which is the weight with which the participant measures are reliable (intraclass correlation coefficient [ICC] >
could only complete 1 repetition of the exercise. At each of the 6 0.92).37 Using ratio instead of the absolute value of supraspinatus
follow-up intervention sessions, shoulder strength was reassessed, tendon thickness measurement allowed us to pool US measure-
and the program was progressed accordingly. ment data obtained with 2 different methods. This prevented
As for the 12-week low-load motor control program, each of systematic differences that could have been observed between
the 6 follow-up sessions started with different shoulder symptom the 2 methods to influence our results.
modification procedures to alleviate symptoms during upper Participants were categorized into 3 subgroups of tendinop-
limb movements.33 If a technique reduced pain, that technique athy according to their ratio of baseline US measurements of
was then used during elevation exercises in 3 planes (flexion, SSTT in relation to the continuum model5,31: ‘‘degenerative’’
abduction, scaption) and incorporated into the participant’s tendinopathy for those with a ratio below 0.9, ‘‘reactive’’ ten-
everyday functional movements.49 Once participants had reached dinopathy for those with a ratio above 1.1 and ‘‘normal’’ tendons
pain-free execution, the program was progressed into re- for those that fell in-between 0.9 and 1.1. We considered a 10%
education exercises involving the whole body and mirroring cut-off value to divide the groups to account for measurement
the different functions performed by the shoulder. Participants error (minimal detectable change [MDC] ¼ 0.33 mm)20 and
performed around 6 different low-load motor control exercises within-subject variability between both sides.
with the number of repetitions varying from 1 to 3 sets of 15
repetitions.
Statistical analyses
Finally, the education component of the interventions included
2 30-minute face-to-face education sessions with a physiothera-
pist. During the first one, participants received oral and written Descriptive values were presented as mean standard deviation
advice and information related to the shoulder (anatomy and (SD) or median (range) per tendinopathy subgroup. Comparison
function), basic pain science, advice on pain management (night in tendon thickness ratio from baseline to 12-week follow-up
and day), activity modification (when to increase and decrease), between allocated interventions and tendinopathy subgroups
and on the importance of physical activity, sleep, healthy eating were performed with two-way repeated measures analysis of
habits, and managing stress. They were also instructed to watch a variance (ANOVAs). Those ANOVAs could reveal potential
series of 6 videos that addressed topics discussed during the initial Time (significant difference in the dependent variable between
session. both measurement timepoints [baseline and 12-week follow-up])
and/or Group (significant difference in the dependent variable
between groups [either the allocated intervention or the tendin-
Outcomes opathy subgroup]) effects as well as Time Group interaction
(significant difference between groups in the change in the
In this article, the primary outcome was the change in the SSTT dependent variable over time). In addition, a linear regression
ratio from baseline to 12 weeks follow-up, calculated by dividing was used to explore the association between the baseline sub-
the measurement on the symptomatic side by the measurement group of tendinopathy and mean disability (DASH or Quick-
on the asymptomatic side. We did so using the supraspinatus DASH) score change, with disability change score acting as the
tendon thickness measurements obtained in millimeters dependent variable. Tendinopathy subgroup, exercise modality,
following standardized procedures on US-captured images.20,37 baseline disability score, and concomitant administration of
In both trials, only 1 investigator, blinded to exercise modality, corticosteroid injection (since it was a possible cointervention
captured all US images and performed all measurements of included in the RoCTEx trial) were imputed as variables in the
tendon thickness. In the RoCTEx trial, US examinations were model. Baseline disability, exercise modality, and corticosteroid
performed with the patient sitting and the shoulder positioned in were selected specifically to test for potential confounding of the
internal rotation by placing the dorsal side of the hand on the results from these variables. Baseline disability was considered
opposite gluteal region. Images were obtained in the longitudinal relevant, as it influences the amount of possible change the
1922 M.-O. Dube et al.
Table II Mean tendon thickness ratio at baseline and 12-week follow-up based on allocated intervention
Baseline 12 Weeks Within group change
Mean (SD) Mean (SD) Mean (95%CI)
No exercises (n ¼ 33) 1.04 (0.14) 1.03 (0.13) 0.01 (0.06 to 0.04)
Low-load exercises (n ¼ 70) 1.02 (0.17) 1.01 (0.16) 0.01 (0.05 to 0.03)
High-load exercises (n ¼ 56) 1.04 (0.13) 1.01 (0.13) 0.03 (0.08 to 0.01)
SD, standard deviation; CI, confidence interval.
No significant between-group differences.
Table III Mean tendon thickness ratio at baseline and 12-week follow-up based on tendinopathy subgroup
Baseline 12 Weeks Within group change
Mean (SD) Mean (SD) Mean (95% CI)
Degenerative tendinopathy (n ¼ 26) 0.80 (0.08) 0.94 (0.15) 0.14 (0.09 to 0.19)
Normal (n ¼ 84) 1.01 (0.06) 0.99 (0.12) 0.01 (0.04 to 0.02)
Reactive tendinopathy (n ¼ 49) 1.19 (0.08) 1.08 (0.15) 0.11 (0.16 to 0.06)
SD, standard deviation; CI, confidence interval.
At baseline, between-group differences were all lower than P < .001.
At 12 weeks, significant difference between reactive and degenerative (P < .001) and between reactive and normal (P ¼ .002).
For within-group change, between-group differences are all lower than P < .001.
increased, while the thickness of ‘‘Reactive’’ tendons This may serve as a caution for researchers investigating
significantly decreased, and no significant change changes in tendon morphology related to interventions. Our
occurred for tendons subgrouped as ‘‘Normal.’’ Results findings suggest comparing subgroups of RCRSP (ie,
were similar no matter the intervention the participants reactive, degenerative) may lead to very different findings
were allocated to, regardless of whether they performed than grouping all presentations under 1 blanket term. This
exercises or not. is not current common practice for RCRSP research, but it
is gaining popularity in studies looking at subgroups of
Structural changes in tendons patients presenting with Achilles tendinopathy with early
beneficial findings.16,15 Indeed, Achilles tendinopathy
Our findings indicate that over time SSTT normalize subgroups were associated with different recovery trajec-
compared to the contralateral unaffected tendon, in patients tories, which suggests the value of identifying patient
within a ‘‘Degenerative’’ or ‘‘Reactive’’ subgroup of subgroups in the management of tendinopathy.15
RCRSP, irrespective of the exercise modality they were Due to the small number of studies on the subject and the
allocated to. These results may illustrate how different small sample size of these studies, it is rather difficult to
subgroups of ‘‘symptomatic’’ tendons behave over time. compare our results with previous findings for RCRSP. A
1924 M.-O. Dube et al.
Table IV Mean change in tendon thickness ratio in each exercise group, from baseline to 12-week follow-up based on tendinopathy
subgroup
No exercises High-load exercises Low-load exercises Between-group difference
Mean (95% CI) Mean (95% CI) Mean (95% CI) between both exercise
(n ¼ 33) (n ¼ 56) (n ¼ 70) groups
Mean (95% CI)
Degenerative 0.12 (0.02 to 0.26) 0.18 (0.04 to 0.31) 0.13 (0.07 to 0.19) 0.04 (0.10 to 0.18)
tendinopathy (n ¼ 3) (n ¼ 7) (n ¼ 16)
(n ¼ 26)
Normal (n ¼ 84) 0.01 (0.04 to 0.06) 0.03 (0.07 to 0.02) 0.01 (0.06 to 0.04) 0.01 (0.09 to 0.07)
(n ¼ 23) (n ¼ 28) (n ¼ 33)
Reactive tendinopathy 0.12 (0.32 to 0.07) 0.11 (0.18 to 0.04) 0.11 (0.19 to 0.02) 0.01 (0.14 to 0.13)
(n ¼ 49) (n ¼ 7) (n ¼ 21) (n ¼ 21)
CI, confidence interval.
No significant between-group differences.
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