Abstract
Ultrasound has become an invaluable tool for the workup and management of patients with symptoms and signs of endometriosis. Until the publication on the systematic approach to ultrasound in patients with suspected endometriosis by the International Deep Endometriosis Analysis (IDEA) group, there was significant heterogeneity in the scientific literature in nomenclature, definitions and components of this particular scan. Despite the concise four steps outlined in their consensus statement, the nature of this ultrasound is advanced, complex and time consuming. Without intending to oversimplify the task, we propose a practical and comprehensive approach on how to perform an ultrasound scan to assess the pelvis of a woman with potential underlying endometriosis.
Keywords: algorithms, diagnostic imaging, education, endometriosis, ultrasonography
Introduction
Ultrasound is a reliable first‐line imaging modality for the assessment of patients with gynaecological concerns.1 In patients with suspected endometriosis, ultrasound serves three purposes. First, it is used to evaluate the aetiology of the patient's symptoms. Second, it has the potential to map the disease location. Lastly, it can ascertain the extent of disease. From a clinical perspective, these products of ultrasound may benefit patients by ensuring a thorough understanding of disease by both the patient, who needs to provide informed consent to treatment options, and the physician, who may adequately prepare for potentially advanced surgical procedures. In many cases, when deep endometriosis (DE) exists, physicians need to consider referral to an appropriate gynaecologic surgeon with advanced skill. The multidisciplinary input of other specialists such as colorectal or urologic surgeons or fertility specialist may also be necessary.
Recently, the International Deep Endometriosis Analysis (IDEA) group published a systematic approach to sonographically evaluate the pelvis in patients with suspected endometriosis.2 This consensus statement was developed to standardise anatomical landmarks, nomenclature of disease and the components of an ultrasound seeking to identify DE. A four‐step system was introduced, including routine evaluation of the uterus and adnexa, evaluation of soft markers such as site‐specific tenderness (SST), assessment of the pouch of Douglas (POD) using the ‘sliding sign’ and, finally, assessing the presence of DE nodules compartmentally throughout the pelvis (Table 1). Although these steps are classified in the publication as steps 1–4, the order of tasks may vary to facilitate a more practical approach taking into consideration time and patient's comfort. This publication aims to clearly outline a practical, efficient and comprehensive method of performing a pelvic ultrasound to assess for DE (Figure 1).
Table 1.
Four basic sonographic steps, which can be adopted in this or any order as long as all four steps are performed to confirm/exclude the different forms of endometriosis.2
| First step | Routine evaluation of uterus and adnexa (+ sonographic signs of adenomyosis/presence or absence of endometrioma) |
| Second step | Evaluation of transvaginal sonographic ‘soft markers’ (i.e. site‐specific tenderness and ovarian mobility) |
| Third step | Assessment of status of POD using real‐time ultrasound‐based ‘sliding sign’ |
| Fourth step | Assessment for DE nodules in anterior and posterior compartments |
DE, deep endometriosis; POD, pouch of Douglas.
Figure 1.
How to Perform an Ultrasound to Diagnosis Endometriosis.
Considerations before commencing ultrasound
A transvaginal ultrasound (TVS) is the recommended imaging modality in the diagnosis of endometriosis.3 Transabdominal ultrasound images may be required in specific cases, including assessment of the kidney and/or anterior abdominal wall, to complete all necessary elements of the scan.2 The need to perform an anterior abdominal wall ultrasound is rare and as such, will not be discussed further in this publication.
The operator should introduce themselves to the patient. Ideally, the patient has already been advised of the nature of the procedure prior to the visit. Regardless, the operator should reiterate the nature of the procedure and ensure the patient has agreed to proceed. Each clinic should follow an accredited sanitary protocol for transvaginal (TV) and transabdominal probe cleaning. After ensuring appropriate cleanliness, ultrasound gel should be placed on the tip of the TV probe. A probe cover can then be placed overtop, followed by lubricating gel to ease insertion of the probe into the patient's vagina. The concept of sonovaginography, a ‘stand‐off’ technique, can be considered to improve the detection rate of DE on ultrasound. This involves injecting 20–50 mL of ultrasound gel into the posterior fornix of the vagina using a syringe.4 Prior to initiating the TVS, patients should be instructed to empty their bladder and then be positioned and draped appropriately. It is important that the hips and knees are flexed, the legs separated and the perineum aligned with the end of medical couch to ensure adequate mobility with the TV probe. This can be achieved with a wedged cushion, a medical couch with stirrups or one with an adjustable bottom section. The scan can then begin.
The ultrasound: bowel
Step 4 of the IDEA approach includes assessment of the posterior compartment. We recommend separating the bowel from the posterior compartment elements and assessing this first. While the probe is slowly entering the vagina (and angled in the direction of the sacrum), the anterior rectum, rectosigmoid junction and sigmoid colon can be evaluated for endometriosis, as these are the most commonly affected posterior compartment areas.5 The consensus statement proposed distinguishing between the upper and lower anterior rectum on ultrasound because of surgical implications; only the upper rectum is visible at laparoscopy, while the lower is retroperitoneal (Figure 2). Operators should understand bowel wall anatomy (Figure 3a) and observe for either thickening of the hypoechoic muscularis propria or hypoechoic nodules (Figure 3b). These lesions may contain hyperechoic foci. Any lesion recognised in the bowel wall should be recorded in three orthogonal planes (length in mid‐sagittal plane, thickness in anteroposterior plane and transverse diameter in transverse plane) (Figure 4) and the distance between the lower margin of the most caudal lesion and the anal verge should be measured. If a lesion is detected, the morphological appearance should be documented based on the types of lesions described in the IDEA consensus statement (Figure 5).2 Furthermore, adjacent areas should be closely assessed for extension of bowel wall DE lesions. Although the IDEA group did not advise for or against the use of bowel preparation because of a paucity of comparative prospective studies, a recent publication suggests that bowel preparation is in fact helpful in better identifying nodules of the rectosigmoid colon.6 Our approach has not yet changed to incorporate bowel preparation as we continue to feel uncertain about its utility based on the current state of literature. We nevertheless respect the ever‐changing nature of research and we are willing to adopt methods that are strongly evidence based. Ultimately, we are of the opinion that the most important aspect for identification of bowel DE is the expertise of the operator.
Figure 2.
Schematic Drawing Identifying Distinct Segments and the Rectum and Sigmoid Colon: Lower (or Retroperitoneal) Anterior Rectum (1); Upper (Visible At Laparoscopy) Anterior Rectum (2); Rectosigmoid Junction (3) and Anterior Sigmoid (4). Reprinted with Permission from Wiley Publishers.2
Figure 3.
Schematic Image Showing the Histological Layers of the Rectum (a), Which Can be Seen on the Adjacent Ultrasound Image (b); A DE Nodule Can Be Seen as Labelled. Reprinted With Permission from Wiley Publishers.29
Figure 4.
Schematic Drawing Demonstrating Method of Obtaining Orthogonal Measurements, i.e. Mid‐Sagittal, Anteroposterior and Transverse. Reprinted with Permission from Wiley Publishers.2
Figure 5.
Schematic Drawings and Corresponding Ultrasound Images of Bowel Deep Endometriosis (DE). (a) DE Nodule with a Regular Outline (Absence of ‘Spikes). (b) DE Nodule with Progressive Narrowing, Like a Tail, Also Known As ‘Comet Sign’. (c) DE Nodule with Prominent Spikes Towards the Bowel Lumen, Also Known as ‘Moose Antler Sign’. (d) DE Nodule with Both Prominent Spikes Towards the Bowel Lumen (‘Moose Antler Sign’) and Progressive Narrowing Like a Tail (‘Comet Sign’). (e) DE Nodule with Both Prominent Spikes Towards the Bowel Lumen (‘Moose Antler Sign’) and Extrinsic Retraction (And Visible Mucosal Folds) (Known As ‘Pulling Sleeve Sign’). The ‘Sliding Sign’ is Expected to Be Negative. (f) DE Nodule and Extrinsic Retraction (‘Pulling Sleeve Sign’). The ‘Sliding Sign’ is Expected to BE Negative. Reprinted with Permission from Wiley Publishers.2
The ultrasound: uterus
As the probe approaches the top of vagina, we propose next evaluating the uterus. The orientation (anteverted, retroverted or military) and dimensions in three orthogonal planes should be recorded. Patients with endometriosis have a high likelihood of concurrent adenomyosis7 and as such, signs of this should be sought and described using the terms and definitions published in the Morphological Uterus Sonographic Assessment (MUSA) consensus statement.8 In addition, the ‘question mark sign’, signifying a fixed anteverted/retroflexed uterus with the fundus adhered posteriorly to the rectum and/or sigmoid colon can represent adenomyosis and/or endometriosis and should be documented if seen.8, 9
We propose the third step in the IDEA consensus statement, assessment of the status of the POD using the ‘sliding sign’, be completed at this time. This dynamic, real‐time technique involves both of the operator's hands; the one holding the TV probe and the other, applying pressure to the patient's lower abdomen. Depending on the orientation of the uterus, the method to test for POD obliteration is slightly different (Table 2, Figure 6). The test is considered positive when the uterus and cervix move independently (i.e. slide) along the anterior rectum and sigmoid (Video S1a and b). Clinically and surgically, this is reassuring for a non‐obliterated POD. Conversely, if the uterus and cervix move in unison with the anterior rectum and sigmoid, the test is negative and the POD is thought to be obliterated.10, 11
Table 2.
Pouch of Douglas assessment for obliteration using ‘sliding sign’
| Anteverted | Retroverted | |
|---|---|---|
| Step 1 | Place gentle pressure against the retro‐cervix using the transvaginal probe. Observe whether the anterior rectum glides freely across the posterior aspect of the cervix and posterior vaginal wall | Place gentle pressure against the posterior upper uterine fundus with the transvaginal probe. Observe whether the anterior rectum glides freely across the posterior upper uterine fundus |
| Step 2 | Place one hand over lower anterior abdominal wall and ballot the uterus between the palpating hand and the transvaginal probe. Assess whether the anterior bowel glides freely over the posterior aspect of the upper uterine fundus | Place one hand over lower anterior abdominal wall and ballot the uterus between the palpating hand and transvaginal probe. Assess whether the anterior sigmoid glides freely over the anterior lower uterine segment |
Figure 6.
Schematic Drawing Demonstrating How to Elicit the ‘Sliding Sign’ in an Anteverted Uterus (a) and Retroverted Uterus (b). Reprinted with Permission from Wiley Publishers.2
The ultrasound: adnexa
Once assessment of the uterus is completed, the operator can proceed with imaging the adnexa. This should include evaluation of the ovaries and Fallopian tubes. Clear annotation should be included with the obtained images differentiating between right and left. The entire ovarian size should be measured in three orthogonal planes. Any abnormalities should be quantified, measured and documented. The sonographic characteristics of any ovarian abnormality should be described according to terminology published by the International Ovarian Tumor Analysis (IOTA) group.12 When an endometrioma is visualised, there is significantly higher likelihood of multiple lesions of DE.13 As such, operators performing the ultrasound should be vigilant for DE when an endometrioma is diagnosed.
Ovarian mobility can be judged by applying pressure to the ovaries using the TV probe. Non‐mobile ovaries are considered a ‘soft marker’ potentially signifying superficial pelvic endometriosis and/or DE. The operator should observe the mobility of the ovaries against the pelvic side wall laterally, uterus medially, uterosacral ligaments (USLs) inferiorly and each other (Video S2a and b). ‘Kissing’ ovaries, an ultrasound diagnosis of ovaries fixed to each other (Figure 7), indirectly indicates intra‐abdominal adhesions and possibly underlying DE of the Fallopian tubes and/or bowel.14 In the presence of endometriosis, the Fallopian tubes may be impaired resulting in a hydrosalpinx or hematosalpinx. When these abnormalities are identified, endometriosis should be entertained in the differential diagnosis.
Figure 7.
‘Kissing’ Ovaries; Indirectly Indicates Intra‐Abdominal Adhesions and Possibly Underlying Deep Endometriosis (DE) of the Fallopian Tubes and/or Bowel. Reprinted with Permission from Wiley Publishers.2
The ultrasound: anterior compartment
The anterior compartment is comprised of the urinary bladder, uterovesical region and ureters. At this point in the scan, if a small amount of urine has collected in the bladder, this is not a concern; a slightly filled bladder may reduce the frequency of false‐negative findings.2 The anatomical landmarks of the bladder relevant to the locations of DE are schematically demonstrated in Figure 8a. The muscularis of the bladder wall is the most likely layer affected by DE while the bladder base is the most likely site of DE (Figure 8b). Lesions may appear as hypoechoic linear or spherical lesions, with or without regular contours (Video S3).15, 16, 17, 18, 19, 20, 21 The uterovesical region should be examined for tethering to the uterus (i.e. obliteration of the space). The concept of the ‘sliding sign’ can be applied here as well. The clinician interpreting the results of the ultrasound should have awareness of the patient's past surgical history, including Caesarean sections, which may produce the same tethering as endometriosis. The operator should hold the TV probe in the anterior fornix with one hand and the other hand should be placed over the suprapubic region. By balloting the uterus between the probe and hand, the operator can judge whether the posterior bladder slides freely over the anterior uterine wall. Like the assessment for POD obliteration, an independently moving bladder from the uterus represents a positive ‘sliding sign’ and a non‐obliterated uterovesical space (Video S4). When the bladder and uterus move together, the operator should document a negative ‘sliding sign’, representing an obliterated space.22
Figure 8.
Schematic of Bladder Anatomic Landmarks; the Demarcation Point Between the Base and the Dome of the Bladder is the Uterovesical Pouch (a). Ultrasound Image and Schematic of Bladder Endometriotic Nodule in the Bladder Base (b) Reprinted with Permission from Wiley Publishers.2
The ureters can also be imaged and assessed for damage secondary to endometriosis. To identify the ureters, the operator should hold the probe midline in the sagittal plane, pointing towards the bladder, and first identify the urethra. Once in view, move the probe laterally toward the pelvic wall. It may assist the operator in visualising the ureters to reverse the image in both the vertical and horizontal planes. In normal cases, the ureter will appear as a hypoechoic tubular structure, which will vermiculate (i.e. contract to move urine from the kidneys to bladder) (Video S5). Ureteric dilatation should be assessed and if present, the distance between the dilatation and the distal ureteric orifice should be measured.23, 24, 25 When DE is diagnosed on TVS, a transabdominal scan of the kidney is necessary to rule out hydroureteronephrosis, which may exist in asymptomatic ureteral stenosis.2, 26, 27
The ultrasound: the posterior compartment
The posterior compartment sites include USLs, posterior vaginal fornix, rectovaginal septum (RVS), anterior rectum, anterior rectosigmoid junction and sigmoid colon.2, 5 As the bowel has already been investigated, we propose this stage of the ultrasound involves assessment of the posterior vaginal fornix, RVS and USLs. To best achieve this, we suggest gently placing the TV probe in the posterior vaginal fornix. A thorough understanding of anatomy is crucial to this step of the ultrasound as the areas visualised are novel in the setting of ultrasound. The IDEA group published a schematic to differentiate the RVS from the posterior vaginal fornix (Figure 9). To improve the detection of DE in the vagina and/or RVS, sonovaginography can be implemented.4 Using the lines drawn in Figure 9 and knowledge of the ultrasound appearance of the three layers (vagina, RVS and anterior rectal wall), an operator should be able to identify isolated RVS lesions from posterior vaginal fornix lesions from those that cross boundaries (Figure 10, Video S6). An example of one that crosses boundaries is the rectovaginal nodule, which extends from the posterior vaginal fornix to the anterior rectum. Clinically, these are usually large lesions and retroperitoneal; therefore, they are not visible on laparoscopy. This makes identification on ultrasound all the more important for diagnosis and surgical planning. These appear as hourglass‐shaped or ‘diabolo’‐like nodules (Figure 11).28
Figure 9.
Schematic Drawing Demonstrating Ultrasound Definition of the Rectovaginal Septum (RVS) (Double‐Headed Green Arrow) and The Posterior Vaginal Fornix (Space Between The Blue Line and The Red Line). Reprinted with Permission from Wiley Publishers.2
Figure 10.
Schematic and Ultrasound Images Demonstrating an Isolated RVS Nodule. Note the Hyperechoic Nature of the RVS (Red Star) and Adjacent Hypoechoic Layers of Vagina (Yellow Star) and Rectal Wall Muscularis (Green Circle). Reprinted with Permission from Wiley Publishers.2
Figure 11.
Schematic and Ultrasound Image Demonstrating a ‘Diabolo’‐Like Nodule of Deep Endometriosis (DE) from the Posterior Vaginal Fornix Extending into the Anterior Rectum. Reprinted with Permission from Wiley Publishers.2
Similar to the Fallopian tubes, the USLs are not usually seen on ultrasound (unless there is fluid in the POD). In the case of abnormality, they may be visible. To evaluate for endometriotic lesions of the USLs, place the transvaginal probe sagittal in the posterior vaginal fornix in the midline and then sweep the probe inferolaterally to the cervix.2 Operators should document hypoechoic thickening of the peritoneal fat surrounding the USLs as a sign of DE (Figure 12). These lesions should be followed to adjacent tissues to rule out larger endometriotic lesions.
Figure 12.
Schematic and Ultrasound Image Demonstrating the Location of Deep Endometriosis (DE) in the Right Uterosacral Ligament in Transverse View (Within Green Circle). Reprinted with Permission from Wiley Publishers.2
The ultrasound: site‐specific tenderness
The last element of the scan is a dynamic assessment of SST, one of the ‘soft markers’.2 We recommend completing this aspect of the ultrasound as the last step to prevent interruption or termination of the scan secondary to pain. Having completed the scan for diagnosis of endometriotic lesions, the operator may now be more familiar with the patient's anatomy to fulfil this step. As stated above, it is important to inform the patient that they may experience discomfort or pain. Moreover, their feedback to the operator performing the scan is essential. The key anatomic locations to assess in this component of the scan include the uterus, adnexa, USLs and POD. Currently, the IDEA group recommends a scoring system of 0 or 1; 0 for no pain and 1 for pain. However, this test is still limited in that no scoring system has been validated as yet.
Once SST testing is finished, the scan can be concluded. A detailed report should be prepared encompassing all findings, normal or abnormal.
Conclusions
This review has outlined a practical approach to performing an ultrasound to evaluate patients with suspected endometriosis. The approach is based on both the IDEA group's consensus statement2 and hands‐on experience. The four‐step system was adapted to the model proposed in Figure 1 to optimise efficiency and promote patient's comfort. We appreciate that there may be other reasonable approaches to complete this type of scan. We also understand that with subsequent studies, components of the scan may change with time. An example of this is bowel preparation, which remains controversial. Each institution should decide to either adopt the approach outlined here or develop their own. Regardless, to fulfil the necessities of an ultrasound to evaluate for endometriosis, we emphasise the importance of ensuring advanced operator experience and incorporating all components from the IDEA consensus statement.
Disclosure statement
Nothing to disclose.
Author declaration
(i) Authorship listing conforms with the journal's authorship policy, and (ii) All authors are in agreement with the content of the submitted manuscript.
Supporting information
Video S1a. Video demonstrating a positive ‘sliding sign’ between the posterior uterine wall and the anterior rectum and sigmoid.
Video S1b. Video demonstrating a positive ‘sliding sign’ between the posterior retro cervix and the anterior rectum.
Video S2a. Video demonstrating mobility between the left ovary and the pelvic side wall and uterus.
Video S2b. Video demonstrating immobility between the left ovary and posterior uterine cervix.
Video S3. Video demonstrating bladder endometriosis.
Video S4. Video demonstrating a positive sliding sign between the bladder and the anterior uterus, representing the normal state (that is, non‐obliterated vesicouterine space).
Video S5. Video demonstrating the normal appearance of a ureter on ultrasound, including vermiculation.
Video S6. Video demonstrating normal anatomy of aspects of the posterior compartment: rectovaginal septum and posterior vaginal fornix.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Video S1a. Video demonstrating a positive ‘sliding sign’ between the posterior uterine wall and the anterior rectum and sigmoid.
Video S1b. Video demonstrating a positive ‘sliding sign’ between the posterior retro cervix and the anterior rectum.
Video S2a. Video demonstrating mobility between the left ovary and the pelvic side wall and uterus.
Video S2b. Video demonstrating immobility between the left ovary and posterior uterine cervix.
Video S3. Video demonstrating bladder endometriosis.
Video S4. Video demonstrating a positive sliding sign between the bladder and the anterior uterus, representing the normal state (that is, non‐obliterated vesicouterine space).
Video S5. Video demonstrating the normal appearance of a ureter on ultrasound, including vermiculation.
Video S6. Video demonstrating normal anatomy of aspects of the posterior compartment: rectovaginal septum and posterior vaginal fornix.