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Application of Ultrasonography in Female Infertility: A Comprehensive Review

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International Journal of Reproduction, Contraception, Obstetrics and Gynecology

Okeke TC et al. Int J Reprod Contracept Obstet Gynecol. 2015 Oct;4(5):1246-1256


www.ijrcog.org pISSN 2320-1770 | eISSN 2320-1789

DOI: http://dx.doi.org/10.18203/2320-1770.ijrcog20150693
Review Article

Application of ultrasonography in female infertility: a comprehensive


review
Tochukwu C. Okeke1*, Kennedy K. Agwuna2, Cyril C. Ezenyeaku3, Lawrence C. Ikeako3

1
Department of Obstetrics & Gynecology, University of Nigeria Teaching Hospital, Enugu, Nigeria
2
Department of Radiology, University of Nigeria Teaching Hospital, Enugu, Nigeria
3
Department of Obstetrics & Gynecology, Anambra State University Teaching Hospital, Amaku, Awka, Nigeria

Received: 24 August 2015


Accepted: 09 September 2015

*Correspondence:
Dr. Tochukwu C. Okeke,
E-mail: tcokeke2014@yahoo.com

Copyright: © the author(s), publisher and licensee Medip Academy. This is an open-access article distributed under
the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial
use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

The quest for detailed evaluation of the uterus, fallopian tubes, and ovaries that is radiation free, inexpensive, readily
available, non-invasive, relatively less time consuming and easily repeatable in female infertility has resulted in
further studies. However, ultrasonography (US) remains the first line indispensable tool for gynecologic workup,
monitoring and treating infertility. The aim is to review the current knowledge regarding the application of
ultrasonography in female infertility. This was a descriptive review of ultrasonography in female infertility. We
searched several databases (Medline, Google scholar, PubMed) with keywords “ultrasonography and female
infertility”, “evaluation of female infertility”, “role of ultrasonography in female infertility:, and imaging in female
infertility”. Female infertility is multifactorial in origin. Ultrasonography is the most widely used imaging in
gynecology and has revolutionized the management of female infertility worldwide. The recognition, evaluation and
treatment of female infertility are complicated, complex, stressful and emotionally devastating for most couples. The
couple’s emotional state should be supportive, informative and well tolerated. Female infertility is an immense stress
to couples, families and relatives worldwide. The causes are multifactorial in origin with both congenital and acquired
problems of the uterus, fallopian tubes and ovaries. Ultrasound plays an important role in female infertility workup
with hysterosalpingography (HSG), sonohysterography (Sono-HSG) and magnetic resonance imaging (MRI), each
playing a complimentary role in the screening, diagnosis and/or management of female infertility.

Keywords: Female Infertility, Ultrasonography, HSG, Sono-HSG, MRI

INTRODUCTION 10-15% of all couples.5 Males and females are equally


affected.5 The physician must view the couple as a unit.
Infertility is a cause of immense stress to couples, The initial evaluation is often perceived as a stressful
families and relatives especially in sub-Saharan Africa experience. The couple is seen together. This approach is
where marriage is revered, respected and tied to child helpful and saves time. Female infertility workup is
bearing.1-3 The emotional, physiological, psychological, incomplete without the application of ultrasonography
sexual, social, and financial burden of infertility on the (US). However, it is important to note that infertility in
family, are enormous.3-6 females is multifactorial in origin.5

Infertility is the inability of a couple to achieve US is a useful and first line investigation tool available to
pregnancy after one year of regular, unprotected gynecologists to assess the causes of female infertility
intercourse. Infertility is relative. In both men and women and to institute some of the treatments used to ameliorate
the fertility process is complex. Infertility affects about infertility. US is an effective, safe, inexpensive, radiation

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Okeke TC et al. Int J Reprod Contracept Obstet Gynecol. 2015 Oct;4(5):1246-1256

free, non-invasive tool, readily available, easy to use and of the pelvis, but transvaginal ultrasound offers several
easily repeatable approach to evaluate female infertility advantages in gynaecology.10
worldwide.6 It improves the quality of care provided in
female infertility workup by facilitating rapid diagnosis The ultrasound of the female pelvis and the morphologic
and the visualization of changes in female reproductive changes in the uterus and ovaries in relation to the
physiology required to direct therapy. menstrual cycle was described by Kratochwil et al in
1972.11 Later in 1977 Hackerloer et al described the
US is the most widely used method of imaging in ultrasonic measurement of follicular size after
gynecology and has revolutionized the management of gonadotropin stimulation by means of the transabdominal
female infertility worldwide.7 technique with full bladder.12 Hackerloer with other co-
workers demonstrated the linear relation between
Ultrasonographic limitations include limited field of follicular growth and serum concentration of oestradiol in
view, subjective errors, interference by obesity or by the spontaneous menstrual cycle.13 This finding was
gaseous bowel loops, suboptimal visualization of confirmed by Kerin et al for timing of oocyte retrieval in
fallopian tubes and broad ligament, failure to delineate natural cycle in invitro fertilization (IVF).14 These
small ovaries, and inability to obtain images in the observations were made by means of static ultrasound
surgical plane.5,6 scanning. O’Herlithy et al demonstrated that real-time
sector scanning yielded similar results.15 This technique
The recognition, evaluation and treatment of female gradually replaced static scanning in monitoring the
infertility are complex and stressful for most couples. spontaneous or induced cycle. The validity of
However, the clinician should not ignore the couple’s transabdominal measurements of follicular size and
emotional state. Information should be supportive, number was confirmed with laparoscopic findings.16
informative and well tolerated. Seibel et al established the role of ultrasound in ovulation
induction.17 The most important advancement in
The aim of this review is to provide clinicians with the infertility care was the introduction of transvaginal
role of ultrasonography in the evaluation of female ultrasonography (TVS). This was reported by Gleicher et
infertility and management of women who want to al in 1983 after successful imaging of ovaries by
achieve pregnancy. transvaginal sector probe and oocyte retrieval for invitro–
embryo transfer (IVT-ET) – through culdocentesis. In
METHODOLOGY 1984 Dellenbach et al described transvaginal
ultrasonically guided oocyte retrieval by means of
This was a 6-month descriptive review of the application follicular puncture.18 Later Schwimer and Lebovic in the
of US in female infertility. Relevant literature search on mid-1980s introduced the technical improvements that
this topic was from January 1st to June 30th 2015. A provided TVS with its powerful diagnostic and
search of literature on application of US in female therapeutic properties.19,20 They used 3.5MHz
infertility published in English was conducted. Relevant transabdominal transducers via the transvaginal route.
materials were selected. We searched several databases This technique did not gain wide acceptance because it
on application of US in female infertility from inception did not result in substantial improvement in image
to January 1st 2015 with keywords “ultrasonography and resolution. It was later that TVS gained popularity after
female infertility”, female infertility workup, female technical advances in instrumentation and imaging.
infertility investigations, imaging in female infertility and Images of better axial and lateral resolution and enhanced
evaluation of female infertility and role of ultrasound in quality were developed as a result of proximity of the
female infertility. We also searched references in vaginal probe to pelvic structures, avoidance of
retrieved articles, book chapters, review articles, attenuation caused by intestinal gas or abdominal wall
conference papers, technical reports, abstracts and muscle and fat with development and incorporation of
internet articles using Medline, Google scholar and probes with higher frequencies. The use of high
PubMed database. These materials were critically frequency (5 to 7.5MHz), high resolution transvaginal
reviewed and the inclusion of individual articles was probes and improvements in magnification imaging and
based on scientific merit and clinical relevance. signal processing provided the opportunity for
investigating of the female reproductive system.
Historical perspective
Recently, TVS has developed and expanded as one of the
Ultrasound was first used in obstetrics and gynecology by most powerful tools for the investigation and
Ian Donald and his colleagues in Scotland in 19588. Ian management of female infertility. It is well accepted by
Donald was Regius Professor of Midwifery at the patients and sonographers because it eludes the
University of Glasgow.9 Ultrasound has undergone discomfort inherent in the need for a full and distended
several developments since introduction. Both bladder. TVS also provides the clinician the ability to
transabdominal ultrasound (TAS) and transvaginal visualize the pelvic organs within a millimeter range.
ultrasound (TVS) are used in gynecology. This ability helps in the definitive diagnosis of pelvic
Transabdominal approach gives a more panoramic view abnormalities with even greater accuracy than the routine

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Okeke TC et al. Int J Reprod Contracept Obstet Gynecol. 2015 Oct;4(5):1246-1256

bimanual pelvic examination.21 Comparative studies have divided into two parts: the medulla, where the blood
proved the superiority of TVS over TAS in monitoring supply enters and exits the ovary and the cortex, which
ovulation induction.22,23 contains multiple follicles in varying stages of
development. Before puberty, the ovaries are smooth, but
Further improvements in technology and instrumentation they get progressively scared with age. Postmenopausal
have made TVS feasible as an office procedure.24 A ovaries are shrunken and have a surface pitted with scars.
recent incorporation in the investigation of female The ovaries are the ovum-producing organs and they also
infertility is the use of Doppler Velocimetry of the pelvic produce female sex steroids.25
organs. This has increased our understanding of
reproductive physiology and pathology. Causes of female infertility

Anatomy of female genital organs Pelvic causes of female infertility are varied and
range from ovarian to tubal and peritubal abnormalities,
The internal organs of reproductive system include: the uterine and cervical disorders.26,27
vagina, the uterus, the fallopian tubes and the ovaries.
1. Ovarian Factors
The vagina is a distensible fibromuscular tube extending  Polycystic ovarian syndrome (PCOS)
from the vulva to the uterine cervix. It is about 9cm long  Hypothalamic amenorrhea
with its upper half above the pelvic floor and lower half  Luteinized unruptured follicle
within the perineum.6,7 The recess between the cervix and  Ovarian infections or tumors
the vagina is called the fornix. Anterior to the vagina, sit 2. Tubal factors
the urinary bladder and urethra; posterior to it is the  Ectopic pregnancy
rectum and anal canal. Laterally, it is bounded by the  Endometriosis
levator ani and pelvic fascia.  Pelvic inflammatory disease (PID)
3. Uterine factors
 Developmental anomalies
The uterus is a hollow, pear-shaped organ with a thick-
walled fibromuscular structure that measures about 8cm x  Adhesions (Asherman’s syndrome)
 Infections
5cm x 2.5cm in a nulliparous young adult.7 However, the
 Tumors
size and shape of the uterus depend on the woman’s age
4. Cervical Factors
and parity. The uterus is divided into the body and the
 Cervicitis
cervix. The uterine body is further divided into 3 parts
namely the fundus, the main body and the isthmus.  Abnormal cervical mucus
Uterus serves as an incubation chamber and allows for 5. Endocrine factors
 Kallman’s syndrome
implantation of a fertilized ovum and accommodates the
 Fertile eunuchism
fetus during pregnancy.25 The cervix serves as the
 Panhypopituitarism
connection between the uterine body and the vagina. The
 Hypothyroidism
opening or the os of the cervical canal is circular in
 Adrenal insufficiency
nulliparous women and slit-like in the parous.6
6. Miscellaneous causes
 Drugs
The fallopian tube is about 10 – 12cm in length and lies
 Radiation
in the upper border of the broad ligament bilaterally. It
 Coital difficulties
runs from uterine cornu to the ovary. Each fallopian tube
7. Idiopathic
is divided into 4 parts: funnel shaped infundibulum and
its fimbriae, wide ampulla, narrow isthmus, and the
intramural part that pierces the uterine wall. The fallopian Work up of female infertility
tubes, ovaries and associated connective tissue
After a detailed history, a careful interview and a
(parametria) are collectively called the adnexae. Fallopian
thorough physical examination should include both
tubes provide the path for the ovum to travel from the physiological and anatomical assessment.27 The
ovary to the uterus. physiological assessment should target the hormonal axis
from the hypothalamo-pituitary axis to the uterus and
Also it is the location of fertilization in its lateral one ovaries, and also the thyroid and adrenal glands. The
third (the ampullary portion of the tube).6,7 purpose is to establish whether the endocrine glands
function properly and whether the pelvic and
The ovaries are almond-sized organ. They are located in reproductive organs respond appropriately to the
the lateral pelvic wall adjacent to the bifurcation of the hormonal cyclical stimulation. The anatomical
common iliac vessels, posterior to the broad ligament and assessment is to define the morphology of the pelvic
anterior to the ureter. It measures 4cm x 2cm x 1cm and organs, since developmental anomalies or acquired
is attached to the broad ligament by the mesovarium.7 defects may interfere with normal reproduction.
Ovarian size and location are dependent on age,
menstrual status and parity. The ovarian parenchyma is

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Okeke TC et al. Int J Reprod Contracept Obstet Gynecol. 2015 Oct;4(5):1246-1256

Ovulatory function tests medication, follicular monitoring with serial TVS and
determination of serum and urine estradiol levels should
1. Basal body temperature recordings be performed. A follicle is considered mature when it
2. Endometrial biopsy to document secretory changes measures 15–18 mm in mean diameter. Ovulation is
in the endometrium thought to occur when fine echoes are seen in the mature
3. Measurement of a mid-luteal serum progesterone follicle and this is associated with serum estradiol value
4. An over-the-counter urinary ovulation prediction kit. of about 400 pg/ml or urine oestrogen excretion levels of
These do not involve pelvic sonography. 80 – 150 µg/day.27
5. Daily ultrasounds to follow the development and
ultimately the disappearance of a follicle (the most To evaluate the endometrium
accurate method of documenting ovulation).28
Changes in the endometrial thickness and variation in
Tubal patency tests uterine blood flow may be determined with US during the
menstrual cycle and during ovulation induction.
1. Hystero-salpingogram (HSG): First line test for Ultrasound allows the study of the 3 main implantation
evaluation of tubal patency because of its therapeutic markers: endometrial thickness, endometrial volume and
and diagnostic benefits.29 endometrial morphological patterns.31,32 For measurement
2. Tubal insufflation with C02 (Rubins Test) of blood flow, the role of color Doppler is required33.
3. Laparoscopy with chromotubation Some authors are of the opinion that when the Pulsatility
4. Fluoroscopic/hysteroscopic selective tubal Index (PI) of the endometrium is over 3.0, implantation is
cannulation unlikely. The relationship between the sonographic
5. Sono-HSG appearance of the endometrium and the success or failure
of pregnancy is still under investigation.33-35
Postcoital examination (Sims-Huhner test)
To guide oocyte retrieval (follicular aspiration) and in
This is used to evaluate the cervical factors and to vitro fertilization-embryo transfer (IVF-ET) or
establish that intercourse is normal.27 intrafallopian transfer fertilization

Pelvic sonography Once a mature follicle is detected, the oocyte may be


retrieved using one of the following techniques:
This is the most valuable, an efficient and inexpensive Laparoscopic aspiration, or transvesical or transvaginal
scoring tool to detect developmental or acquired uterine aspiration under ultrasound guidance. Fertilization may
and ovarian pathology. Female infertility that is due to be performed in vitro or in the uterus (intrauterine
gynecologic abnormalities and/or ovulation disorders insemination) or in the fallopian tube (intrafallopian
requires ultrasound as valuable contributor in its work transfer) under ultrasound-guided cannulation. The
up.27 embryo transfer (ET) procedure is the final important step
in IVF process. This is a critically important procedure
Role of ultrasonography in female infertility irrespective of how good the IVF laboratory culture
environment is, the clinician can ruin the whole
US offer the following contributions in the investigation procedure with a carelessly performed embryo transfer.
and treatment of female infertility. The entire IVF cycle depends on delicate placement of
the embryo at the proper location of the endometrial
To assess the anatomy of the pelvic organs cavity with minimal trauma and manipulation under
ultrasound guided ET.36,37 Ultrasound guided embryo
Developmental anomalies or abnormal mass or fluid transfer has a number of potential benefits such as: The
collection can be detected by either transabdominal catheter could be bent to easily pass through the cervical
sonography (TAS) or Transvaginal Sonography (TVS). canal and follow the uterine axis, which helps to prevent
stimulation and reduction in incidence of difficult
To monitor the development and evolution of ovarian transfers, endometrial trauma and bleeding that can cause
follicles excessive fundo-uterine contractions at the time of
embryo transfer has been associated with lower clinical
US is an efficient cost effective modality for studying the pregnancy rates.38-41 Secondly, the entire process of
female reproductive organs and monitoring the functional catheterization and release of the embryos can be
changes during spontaneous and induced cycles.30 During visualized, making it easier to place the embryo in the
ovulation induction with clomiphene citrate or human correct position within the uterus and decrease the chance
menopausal gonadotropin (hMG), TVS is used to monitor of improper embryo placement.38,42,43 The main
the development of ovarian follicles. This is carried out disadvantage of using ultrasound guidance during embryo
from day 7 of the patient’s cycle, preferably on a daily transfer is the additional time and personnel required with
basis. This allows the clinician to manipulate and adjust patient discomfort due to a full bladder and the urge to
the dosage of medication. During the administration of urinate.35

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Okeke TC et al. Int J Reprod Contracept Obstet Gynecol. 2015 Oct;4(5):1246-1256

To avoid the development of ovarian hyperstimulation thirds of the vagina are absent or atretic in both
syndrome (OHSS) conditions. Ovaries appear normal but may be more
superiorly located. MRI will also show the same findings
The syndrome usually occurs 5 to 8 days following like ultrasonography but HSG evaluation is not indicated
administration of hMG. It consists of pain, electrolyte for this condition. Mayer-Rokitansky-Kuster-Hauser
imbalance associated with ascites and pleural effusions, syndrome is the most common variant in this class of
extremely high level of serum estradiol (>3000pg/ml) and anomalies.45
massive stromal edema of the ovaries. Patients with large
follicles (>15mm) in the ovaries are unlikely to develop For Class II: Unicornuate uterus, US demonstrate a
hyperstimulation, which tends to occur in ovaries with fusiform “banana-shaped” endometrial canal, which is
multiple small follicles or in women who have just laterally deviated with a single fallopian tube. If this is
conceived following induction. Medication should be detected, it is better to do MRI to evaluate for a
stopped if urine oestrogen excretion levels reach rudimentary horn which is often resected to avoid an
150µg/day. It is important to point out that severe OHSS increased risk of endometriosis and/or ectopic
is rare, occurring in less than 1% of patients.44 The pregnancy.47 It is important to note that this condition is
grossly enlarged ovaries (>10cm) contain multiple echo- often associated with urinary tract anomalies with renal
poor lesions that represent either atretic follicles or areas agenesis contralateral to the dominant uterine horn most
of hemorrhage in the glands. The ovaries are prone to commonly seen.25,45
torsion, which may be detected by color Doppler
sonography. Other possible complications are For Class III: Didelphys uterus, US demonstrates 2
spontaneous rupture, thrombosis, or hemorrhage and symmetric, widely spaced uterine horns each with its own
cardiac failure. Patients usually respond well to cervix. Both HSG and MRI will show a similar picture.
supportive therapy. Spontaneous resolution usually Failure to identify and canulate both cervices during HSG
occurs in 2weeks for nongravid patients and in 4-8 weeks may lead to false diagnosis of unicornuate uterus. There
in pregnant women.44 is an association of urinary tract anomalies with this
condition which is present in 23% of women with
To assist in decreasing the risk of multiple gestations: didelphys uterus.48

When 4 or more mature follicles are detected, the For Class IV: Bicornuate uterus, US demonstrates a
probability of having multiple gestations is high.27 fundal uterine cleft larger than 1cm separating divergent
uterine horns. It will also show fusiform symmetric size
To identify congenital uterine anomaly and fallopian and appearance of the endometrial canals, with possible
tube anomalies: visualization of a communication between the inferior
segments of the uterine horns.25
Mullerian duct anomalies occur secondary to failure of
organogenesis, failure of fusion or failure of reabsorption, For Class V: Septate uterus, US demonstrates normal, flat
causing incomplete development of one or both of the or contour depression of the uterine fundus of less than
uterine horns.25 About 25% of women with mullerian 1cm.49 MRI will also show a similar presentation but
duct anomalies have reproductive problems such as HSG is limited in its ability to differentiate this from
increased risk of spontaneous abortion, prematurity, bicornuate uterus, a narrow angle of less than 75°
intrauterine growth restriction (IUGR), abnormal fetal lie between the uterine horns and/or an intercornual distance
and dystocia at delivery.45 These anomalies are classified of less than 4cm is suggestive of septate uterus.49 TVS
by the American Fertility Society (AFS) classification and MRI have improved the diagnostic accuracy for
scheme.46 The scheme is based on the embryologic septate uterus with hysteroscopy and laparoscopy serving
development of the mullerian ducts and is divided into 7 as gold standards for diagnosis.48 Of the mullerian duct
classes. anomalies, septate uterus is associated with the highest
rate of reproductive failures.45 It is associated with
Class I: Uterine hypoplasia and/or agenesis infertility and miscarriages which is due to poor blood
Class II: Unicornuate uterus supply to the septum providing unsuitable support for the
Class III: Uterus Didelphys implanted embryo.50
Class IV: Bicornuate uterus
Class V: Septate uterus For Class VI: Arcuate uterus, US demonstrates a single
Class VI: Arcuate uterus and endometrial canal, with a smooth, broad indentation of
Class VII: Diethylstilbesterol (DES) – related anomalies the myometrium (<1cm at the uterine fundus). The
external uterine contour is normal on both
For Class I: Uterine hypoplasia and/or agenesis, US ultrasonography and MRI. HSG may be limited in
demonstrates a fibrous remnant/connective tissue and distinguishing arcuate from septate uterus.25 An arcuate
vessels in the expected region of the uterus in the setting uterus may not have effect on fertility or obstetric
of agenesis and small hypoplastic uterine soft-tissue outcomes.51
remnant in the setting of hypoplasia. The upper two-

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For Class VII: (T-shaped DES-related uterine anomalies). follow the menstrual cycle.55 TVS and/or
DES was previously used for treatment of hyperemesis sonohysterography are the imaging modalities of choice
gravidarum and prevention of spontaneous abortions demonstrating a focal echogenic mass protruding into the
between 1945 and 1970. Female fetus exposed to DES in endometrial lumen from the endometrium, with an intact
utero are at risk of developing a hypoplastic, irregular T- endometrial stripe. MRI is used for indeterminate lesions
shaped uterus and hypoplastic and strictured fallopian with variable, appearance based on subtype.
tubes, and they have an increased incidence of vaginal
clear cell carcinoma later in life.52 In pregnant women Adenomyosis
who underwent in utero exposure to DES, the hypoplastic
uterus incurs a higher risk of spontaneous abortion, Adenomyosis is a benign condition of the uterus which
preterm delivery and ectopic pregnancy. The features of results from the invasion of myometrium by endometrial
DES-related uterine anomalies unlike other classes of glands and stroma causing hyperplastic and hypertrophic
mullerian duct anormalies, are best depicted by HSG.53 changes of the myometrium.58 The process may be
US is limited in this demonstration.25 diffuse (with enlarged globular shape) or focal area which
is referred to as an adenomyoma, which presents in 1 of 3
To identify congenital ovarian anomalies forms: as a localized version of the diffuse form; as a
well-circumscribed nodule of smooth-muscle cells,
Gonadal dysgenesis is a congenital anomaly in which endometrial glands and stroma or as a cyst secondary to
gonadal tissue is replaced by fibrous stroma with no germ repetitive bleeding, leading to cavitation.59,60
cells54. This condition is referred to as streak gonads. The Adenomyosis is associated with infertility probably due
most common form of this condition is secondary to to impaired uterine contractility required for directed
Turner syndrome (45X0 karyotype). US is not performed sperm transport through the uterus.60
to identify this condition. The diagnosis of this condition
is based on clinical, biochemical, and karyotype US is the initial imaging modality of choice
identification. US demonstrates small oval to linear demonstrating an enlarged globular uterus with loss of
fibrous tissue within the broad ligament with absence of the junctional zone. Ultrasound features of adenomyosis
normal-appearing ovaries. This condition is best seen include globular uterine enlargement, heterogeneous
with MRI, although with limited detection, with gonads myometrial echotexture, myometrial cysts, indistinct
found in only 40% to 65% of cases.25 US has limited endometrial-myometrial interface, subendometrial
utility in detecting streak gonads, but may be useful for echogenic nodules or linear striations, asymmetric
assessment of associated mullerian duct anomalies.25 myometrial thickening and indistinct lesion borders.26

To identify acquired abnormalities Uterine Synechiae

(fibroids, endometrial polyps, adenomyosis, uterine This is also known as intrauterine adhesions or
synechiae and cervical stenosis).25,26 intrauterine webs. They are adhesions of the endometrial
canal leading to partial or complete loss of the uterine
Submucous fibroid cavity and/or intrauterine cervical os. This condition may
be as a result of trauma or destruction of the endometrial
Fibroids, also known as leiomyomas or myomas are lining from previous pregnancy, infection, missed
benign estrogen-dependent smooth-muscle tumors that abortion and previous curettage.54,61 When this condition
originate from the uterine myometrium, occurring in 20% is associated with clinical symptoms of infertility,
to 40% of women in their reproductive years.1,55 They are menstrual abnormalities, and/or recurrent pregnancy loss,
solitary or multifocal lesions that arise from any part of the term Asherman syndrome is applied61. Ultrasound is
the uterus. The masses that protrude into the endometrial limited in the detection of adhesions but may show
canal, are described as submucous in location and cause irregular thickness of the endometrium with regions of
infertility by interfering with embryo implantation.48,55,56 hypoechogenicity consistent with areas of fibrosis.
TVS demonstrates a focal heterogeneous mass that is
hypoechoic to the myometrium and may have acoustic HSG is the imaging technique of choice for the diagnosis
shadowing.57 of this condition, demonstrating irregular well-defined,
angular and/or longitudinal filling defects within the
Endometrial Polyps endometrial canal.62 Sonohysterography is as effective as
HSG in the detection of synechiae, with the added benefit
Endometrial polyps are focal overgrowth of the of approximating the size of the endometrial cavity
endometrial glands and stroma surrounded by normal (Table 1).
endometrium. These lesions are divided into 3 subtypes
namely hyperplastic polyps which have glands similar to Cervical Stenosis
those seen in endometrial hyperplasia, atrophic polyps,
which occur in postmenopausal women and have atrophic It is the inability to insert a 2.5mm or thinner dilator into
cystically dilated glands; and functional polyps which the cervical canal.63 It could be congenital or secondary

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to infection. DES exposure in utero or iatrogenic trauma irregularity and subcentimetric diverticula of the isthmus.
such as previous cone biopsy, cryotherapy, or laser This condition is often bilateral.
vaporization of the cervix, causing scarring and fibrosis
are risk factors.26,63 Cervical stenosis is best visualized on Peritubal abnormalities
HSG. When there is complete obstruction, insertion of
HSG catheter is blocked, prevailing imaging of the canal Peritubal pooling of contrast materials is suggestive of
or interus.26,63 It may be necessary to have additional peritubal adhesions. The abnormal accumulation of
imaging with MRI or US to look for secondary signs of contrast material is usually seen adjacent to the ampullary
obstruction, including haematometra and hydrometra.63 ends of the tube at HSG. Both endometriosis and PID
may lead to peritubal adhesions with resultant
To identify acquired abnormalities of fallopian tube infertility.66 When there is evidence of peritubal
(Tubal occlusion, hydrosalpinx, salpingitis isthmica adhesions at HSG, MRI is particularly helpful for further
nodosa) noninvasive evaluation.26 (Table 1)

Fallopian tube abnormalities are the most common cause To identify acquired abnormalities of the ovaries
of female infertility accounting for 30-40% of cases.64
Occlusion may occur at site along the course of the tube. Ultrasound does not play a major role in the diagnosis of
The differential diagnosis of tubal occlusion includes primary causes of ovarian factor infertility. The primary
tubal spasm, infection and prior surgery.62 Rare causes of causes are nonfunctional ovaries, premature ovarian
tubal occlusion include granulomatous salpingitis due to failure and gonadal dysgenesis. They are diagnosed based
tuberculosis, intraluminal endometriosis, parasitic on clinical and biochemical findings. However,
infection and congenital atresia of the fallopian tubes.26 ultrasound can play a major role in detecting the
secondary causes of ovarian factor infertility such as
HSG is the gold-standard imaging modality in the endometriosis and polycystic ovarian syndrome.
diagnosis of occlusion within the fallopian tube (Table 1).
The obstruction results in lack of intraperitoneal free Endometriosis
spillage of contrast.65 When the obstruction is identified
within the proximal cornual portion of the fallopian tube, It is the implantation of endometrial glands and stroma
differentiation from spasm must be considered with outside the endometrial cavity, primarily affecting the
delayed imaging or administration of a spasmolytic agent ovaries and peritoneal surfaces of the pelvis.70,71
such as scopolamine or glucagon to determine whether Endometriosis often presents as chronic pelvic pain and
the obstruction is permanent or temporary.62,65,66,67 In infertility.
addition it may be helpful to place the patient prone and
re-inject contrast material into the uterus.56 Ovarian lesions often present as cyst with hemorrhage
(endometroma), deep invasion of endometriosis on the
Hydrosalpinx peritoneum resulting in fibrosis and muscular
hyperplasia. Ultrasound of an endometroma demonstrates
It is the dilatation of the proximal tube as a result of a thick-walled complex cyst with homogeneous low level
blockage of ampullary portion of the fallopian tube taking echoes, often called chocolate cyst, and may have small
on a classic sausage-shaped appearance.25 The condition calcification along the wall of the cyst.25,70 It is difficult
is often bilateral and is caused by scarring or adhesions of to visualize peritoneal implants with ultrasound but can
the distal tube from PID, adhesions from previous pelvic be suspected if there is tethering of the bowel or if the
surgery or trauma, endometriosis and tubal neoplasm.68,69 ovaries are in close approximation to the uterus.26,70 MRI
HSG demonstrates a dilated proximal tube with absence has unproved detection of peritoneal implants, but the
of free intra-peritoneal spillage of contrast. There is need sensitivity is low (13%).25
for post procedural antibiotic prophylaxis (doxycycline)
to prevent infection from stasis of contrast material Polycystic ovary syndrome
within the obstructed tube.56 Ultrasound and MRI may
show a fluid-filled tubular structure. The imaging This is a syndrome in which 2 or 3 conditions must be
characteristics of the fluid vary depending on whether the present to make a diagnosis: (1) Oligo-ovulation and/or
fluid is simple, hemorrhagic, protein or pus filled.68,69 anovulation, (2) Hyperandrogenism without other cause,
(Table 1) and (3) polycystic ovaries without other cause.
Ultrasound plays an important role in this diagnosis by
Salpingitis Isthmica Nodosa quantification of ovarian volume and assessment of cyst
size and number. TVS is the imaging modality of choice,
It is an inflammatory process within the fallopian tube of demonstrating ovarian volume greater than 10ml, more
unknown etiology, with small out-pouching on the than 12 cysts measuring 2 to 9mm in diameter per ovary
isthmic portion of the fallopian tube.69 This condition is and increased echogenicity of the ovarian stroma. It is
often associated with PID, infertility and occasionally possible to have great overlap of these findings with
ectopic pregnancy.26,62 HSG demonstrates tubal normal ovarian ranges.26

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Table 1: Imaging techniques.6,7,25-27

Type of Routinely used Information about Need for


Average
Imaging in evaluation of endometrial cavity Draw back Risks Anesthesi
cost
Technique infertile couple and fallopian tube a
Routinely used.
Uses sound Well tolerated,
Limited accuracy in
waves to obtain radiation free, $ 150 – $
Transvaginal diagnosing Very low No need
medical images readily available, 450
Ultrasound abnormalities of the risk of for
of various cheap and easy to (less
(TVS) endometrial cavity heating anesthesia
organs and use and can be expensive).
and tubal pathology
tissues in the repeated
body.
Not routinely Gives extensive
used. Less information with Very low risk of 1 – 3% risk
preferred high sensitivity. radiation exposure. of
Hysterosalpi
procedure: Gold standard in Inability to infection, $600 – Yes
ngography
traditional the diagnosis of distinguish a polyp abdominal $800
(HSG)
method used to tubal occlusion from a fibroid pain and
evaluate female within the fallopian tumor injury
infertility. tube.
Not routinely
used. Provides
Lack of
information on
comprehensive
pathological
Sono-HSG evaluation of Low No Need
lesions in $750 -
(Fluid fallopian tubes and Easy tolerability. infection for
endometrial $1000
Ultrasound) need for a second risk. anesthesia
cavity but
procedure e.g.
limited
hysteroscopy.
information on
tubal patency.
Detects Contraindi
Not routinely
pathological lesions cated in
used. Uses Noninvasive and
including tubal patients
magnetic field, radiation free but it
lesions and pituitary with No need
radio waves and has limited Expensive
MRI adenoma. Best for cardiac for
computers to availability and (high cost)
delineating pacemaker anesthesia
generate images high cost. Can’t
morphology, and and
of tissues within easily be repeated.
orientation of pelvic cochlear
the body.
structures. implants.

Limitations of ultrasonography anomalies. The diagnosis of streak gonads is based on


clinical, biochemical and karyotype identification.
Ultrasonographic limitations broadly include suboptimal
visualization of fallopian tubes and broad ligament, failure US is limited in the demonstration of features of DES-
to delineate small ovaries and inability to obtain images in related anomalies such as hypoplastic, irregular T-shaped
the surgical plane, limited field of view, interference by uterus and hypoplastic and strictured fallopian tubes unlike
obesity or by gaseous bowel loops and subjective errors.5,6 other classes of mullerian duct anomalies that are best
depicted by HSG.25,53
US do not play major role in the diagnosis of primary
causes of ovarian factor infertility such as nonfunctional US is limited in detection of uterine synechiae
ovaries, premature ovarian failure, and gonadal (intrauterine adhesions) but may show irregular thickness
dysgenesis. However, US can play a major role in of the endometrium with regions of hypoechogenicity
detecting the secondary causes of ovarian factor infertility consistent with areas of fibrosis.
such as endometriosis and polycystic ovarian syndrome.
US also have limited utility in detecting streak gonads but US is limited in detection of cervical stenosis but can be
may be useful for assessment of associated mullerian duct used to look for secondary signs of obstruction including
haematometra and hydrometra.63 US is also limited in the

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detection of tubal occlusion. In this condition, HSG is the 12. Hackeloer B, Nitschke S, Daume E, Sturm G, Buch
gold-standard imaging modality in the diagnosis of tubal holz R. Ultrasonics of ovarian changes under
occlusion within the fallopian tube. gonadotrophin stimulation. Geburtshilfe Frauenheilkd.
1977;38:185
CONCLUSION 13. Hacheloer BJ, Fleming R, Robinson HP, Adam AH,
Coutts JRT. Correlation of ultrasonic and
Female Infertility is an immense stress to couples, families endocrinologic assessment of human follicular
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origin with both congenital and acquired problems of the 29.
uterus, fallopian tubes and ovaries. Ultrasound plays an 14. Kerin JF, Warnes GM, Crocker J, et al. 3-hour urinary
important role in female infertility work-up with HSG, radio immunoassay for luteinizing hormone to detect
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complimentary role in the screening, diagnosis, and/or 15. O’Herlithy C, de Crespigny L, Robinson HP.
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time ultrasound. BJOG 1980;87:613.
Funding: No funding sources 16. Montzavinos T, Garcia JE, Jones HW Jr. Ultrasound
Conflict of interest: None declared measurement of ovarian follicles stimulated by human
Ethical approval: Not required gonadotropins for oocyte recovery and in intro
fertilization. Fertile Steril. 1983;40:461.
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comprehensive review. Int J Reprod Contracept
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