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Utility of pelvic ultrasound imaging in diagnosing endometriosis

Findings and significance for gynecologic surgeons.

Endometriosis is a chronic inflammatory disease defined as the presence of ectopically implanted endometrial tissue outside of the uterus.1 It responds to hormonal changes that affect the normal endometrium, which lines the uterine cavity. Endometriosis is estimated to affect 5% to 10% of women of reproductive age, 20% of women with infertility, and up to 80% of women with chronic pelvic pain.2-4 Additionally, 40% of women with endometriosis are estimated to have infertility or subfertility.1,5,6 Endometriosis poses significant financial, psychological, and social burdens on patients, leading to isolation and frustration, higher health care resource utilization, and direct and indirect health care costs. Individuals with endometriosis are less often able to work in their desired profession and frequently miss days of school and work.7 Up to 86% of the individuals with endometriosis and chronic pelvic pain suffer from depression, compared with 38% without chronic pelvic pain.8 One study showed that patients with endometriosis spent about $26,000 more on health care expenses than those in a control group in the 5 years before and after diagnosis.9 7 Parameters Monitor

Utility of pelvic ultrasound imaging in diagnosing endometriosis

Endometriosis is a disease that gynecologists frequently encounter because of its high prevalence and symptomatology, the most common being chronic and often severe, even debilitating, pelvic pain. Why, then, has detection and treatment of endometriosis eluded so many of our patients? A primary reason is that until recently, diagnosis required surgery.

Despite the high prevalence of endometriosis, there have been several challenges hindering its diagnosis. The average time from onset of symptoms to diagnosis is 7 to 12 years.10-12 Diagnosis of endometriosis is typically difficult given that the symptoms overlap with many other pain syndromes, including inflammatory bowel disease, irritable bowel syndrome, bladder pain syndrome, pelvic floor disorders, primary dysmenorrhea, and others.13 Moreover, the stage of disease does not necessarily correlate with clinical symptoms.14 While some patients with endometriosis may remain asymptomatic, common symptoms include but are not limited to chronic and often severe pelvic pain, dysmenorrhea, dyspareunia, and dyschezia, as well as subfertility.15 Laparoscopy and tissue pathology have been the standard of care for diagnosis, even though ultrasound is the first-line imaging modality for evaluation of chronic or cyclic pelvic pain and infertility. The standard pelvic ultrasound has been too limited to detect most cases of endometriosis until recently.

Clinical suspicion and imaging modalities are of paramount importance in evaluation of chronic pelvic pain. Ultrasound, however, can be a double-edged sword in cases of endometriosis. Transvaginal ultrasound (TVUS) is a dynamic and powerful tool for both diagnosis and surgical planning, but it is operator dependent, and a standard pelvic ultrasound does not detect extraovarian endometriosis or pelvic adhesions.16 This results in the underestimation of the complexity of many surgical cases and leads to incomplete or suboptimal surgical treatment.

The majority of sonographers, sonologists, and radiologists are not trained to identify deep endometriosis or pelvic adhesions, because these techniques are fairly new.17,18 Studies show that TVUS detection of endometriosis is lower if performed without endometriosis-specific training.17 On the other hand, expert pelvic ultrasound imaging has high accuracy for detecting deep endometriosis with sensitivity and specificity, similar to MRI.19,20 To understand why, one first must understand the different types of endometrioses and how they typically appear on pelvic ultrasound.

Currently, endometriosis can be subdivided into 3 types: ovarian endometriosis (OE), deep endometriosis (DE), and superficial endometriosis (SE). OE is the easiest one to diagnose by ultrasound because it manifests as ovarian cysts, specifically endometriomas. DE was historically defined as endometriotic lesions invading more than 5 mm deep into the peritoneum, but in 2021 it was redefined as any endometriosis extending deep to the peritoneal surface.2 The pain associated with these implants is often severe. The most common site for deep endometriosis is the posterior cul-de-sac, including the uterosacral ligaments and rectum.21 This can now be reliably identified by TVUS but requires learning new techniques. Medicine is constantly advancing, and the same is true in pelvic ultrasound.

This review presents ultrasound imaging techniques to optimize diagnosis and preoperative evaluation for endometriosis, in particular, deep endometriosis. Patients can then be triaged to the most appropriate treatments, and if surgery is indicated, the level of surgical complexity identified preoperatively. Yearslong-delayed diagnoses and incomplete surgical treatments because of lack of knowledge of these newer imaging techniques can be avoided.

How to diagnose endometriosis via ultrasound

There are 4 basic sonographic steps for examining patients with suspected endometriosis22:

Step 1: Routine evaluation of uterus and adnexa includes uterine orientation, sonographic signs of adenomyosis, and presence or absence of endometrioma.

In the absence of other causes (ie, cesarean delivery), a retroflexed uterusis strongly suggestive of deep endometriosis resulting in posterior compartment adhesions (Figure 1B).

Adenomyosis is defined as invasion of endometrial glands and stroma into the myometrium. Detailed description of the direct and indirect sonographic markers of adenomyosis as described by the Morphological Uterus Sonographic Assessment group in 2022 is beyond the scope of this paper, but studies suggest more than 89% of patients undergoing laparoscopic surgery for endometriosis show sonographic signs of adenomyosis on preoperative ultrasound,23 and patients with a previous or current diagnosis of endometriosis are significantly more likely to have adenomyosis, with an odds ratio of more than 424,25;about 50% to 90% of patients with endometriosis have coexisting adenomyosis.26,27

Next, evaluate the adnexa: This includes not just the appearance but also the location of the ovaries. Endometrioma is defined as a cystic mass arising from ectopic endometrial tissue within the ovary.

Endometriomas are the most recognized ultrasound manifestation of endometriosis. The sensitivity and specificity of TVUS detection for endometriomas and deep endometriosis (DE) is 93% to 96% and 79% to 94%, respectively.28 The presence of an endometrioma significantly increases the probability of having rectosigmoid disease, with a positive likelihood ratio of 7.29 Furthermore, up to 50% of patients with DE have an endometrioma.25,30 The classic appearance of endometrioma is a unilocular cyst with diffuse homogeneous ground-glass echoes due to the hemorrhagic debris. About 87% of endometriomas appear as low-level homogenous ground glass–appearing cysts (Figure 2A), though about 26% can have irregular cyst walls (Figure 2B).31

While 66% of endometriomas are unilocular, 18% of endometriomas in premenopausal patients will be multilocular in appearance(Figure 2C).31

About 17% of endometriomas contain solid-appearing components consistent with clot(s) (Figure 2D).31 These clots may jiggle upon movement of the probe, thus proving that they are not fixed papillations. In cases where the imager is unsure, it should be described as a solid component and evaluated with Doppler.

It is crucial to use color Doppler for adnexal lesions.32 Endometriomas do not show internal color except in the wall or septations, and it is crucial to put color Doppler on any adnexal lesion to rule out internal color flow (Figure 2A).

Evaluating the location of ovaries should be part of the ultrasound evaluation when endometriosis is suspected. Medially located ovaries attached to each other and to the back of the uterus (also known as kissing ovaries) are strongly associated with moderate to severe endometriosis and increased surgical complexity (Figure 3).31,33

Step 2: Evaluation of transvaginal sonographic associated markers of endometriosis.

In contrast to other imaging modalities, ultrasound is dynamic. Ovarian mobility can be assessed by applying gentle pressure to determine whether the ovary glides freely from surrounding structures. Negative mobility is highly associated with adhesions. Studies have shown that the sensitivity and specificity for prediction of fixation of at least 1 ovary via preoperative TVUS assessment of ovarian mobility is 89% and 90%, respectively.34

Step 3: Assessment of the posterior compartment or cul-de-sac using real-time ultrasound-based sliding sign. Sliding test is performed in sagittal view. To assess the sliding sign, gentle pressure is placed against the cervix using the transvaginal probe to establish whether the anterior rectum glides freely across the posterior aspect of the cervix and posterior vaginal wall. If the anterior rectal wall does so, the sliding sign is considered positive or normal for this location.35

Negative/abnormal sliding sign with the bowel attached to the uterus predicts an obliterated cul-de-sac.20

Sliding test is an important preoperative evaluation both for counseling as well as surgical planning for bowel surgery. One study showed that preoperative TVUS showing negative sliding can predict obliteration of cul-de-sac with 93% accuracy.35 Furthermore, more than half of patients with abnormal sliding test results are estimated to have bowel endometriosis.36

Step 4: Assessment for deep endometriotic nodules in anterior and posterior compartments.

A negative sliding sign is highly associated with concurrent deep endometriosis. It is important to note that 90% of bowel endometriosis is localized to the rectosigmoid segment of the bowel,37 an area easily imaged by transvaginal ultrasound (Figure 4). Sonographic features of endometriotic disease of the bowel include the presence of a hypoechoic, elliptical, or C-shaped solid mass (Figure 4), distorting and replacing the normal appearance of the muscular and serosal layer of the rectal wall (Figure 5). The comet sign is a characteristic appearance of bowel wall endometriosis(Figure 4 A,B,C).38 It is important to measure these lesions in 3 planes and describe what segment of the bowel they occur in. Rectal endometriosis is shown to be frequently associated with uterosacral endometriosis (Figure 5D). Studies report that 69% of deep endometriosis cases have uterosacral ligaments involvement.39

Evaluation of the anterior compartment requires a small amount of urine be present in the bladder. Urinary tract endometriosis (UTE) refers to endometriotic implants of the bladder, ureters, kidneys, and urethra. About 0.3% to 12% of all people affected by endometriosis and 20% to 52% of individuals with deep endometriosis are found to have UTE, which can present with symptoms including dysuria, urinary frequency, recurrent urinary tract infections, and hematuria.37 The bladder base and dome (Figure 6) are most commonly affected and estimated to account for 85% of urinary tract endometriosis.40

Vesicouterine nodules typically appear as isoechoic or hypoechoic solid lesions (Figure 6).39 Similar to examination of other masses, color Doppler evaluation is crucial to differentiate benign from malignant lesions.

Endometriosis is a common and potentially debilitating condition resulting in decreased quality of life and function, yet there continues to be a substantial delay in diagnosis. Clinical suspicion and imaging modalities are of paramount importance.

Laparoscopy with histological confirmation of ectopic endometrial tissue has been the gold standard for diagnosis, but recent TVUS imaging advancements have proven to be a reliable and noninvasive tool for diagnosing endometriosis when performed by trained imagers. Expert and detailed ultrasound helps visualize anatomic areas that are not visible surgically (Figure 4) and predicts surgical complexity. This improves patient counseling and allows planning for interdisciplinary consults, thereby reducing the risk of incomplete surgeries.

1. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997;24(2):235-258. doi:10.1016/s0889-8545(05)70302-8

2. International working group of AAGL, ESGE, ESHRE and WES, Tomassetti C, Johnson NP, et al. An international terminology for endometriosis, 2021. J Minim Invasive Gynecol. 2021;28(11):1849-1859. doi:10.1016/j.jmig.2021.08.032

3. Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Marshall LM, Hunter DJ. Incidence of laparoscopically confirmed endometriosis by demographic, anthropometric, and lifestyle factors. Am J Epidemiol. 2004;160(8):784-796. doi:10.1093/aje/kwh275

4. Fuldeore MJ, Soliman AM. Prevalence and symptomatic burden of diagnosed endometriosis in the United States: national estimates from a cross-sectional survey of 59,411 women. Gynecol Obstet Invest. 2017;82(5):453-461. doi:10.1159/000452660

5. Bérubé S, Marcoux S, Langevin M, Maheux R. Fecundity of infertile women with minimal or mild endometriosis and women with unexplained infertility. The Canadian Collaborative Group on Endometriosis. Fertil Steril. 1998;69(6):1034-1041. doi:10.1016/s0015-0282(98)00081-8

6. Counseller VS, Crenshaw JL. A clinical and surgical review of endometriosis. Am J Obstet Gynecol. 1951;62(4):930-942. doi:10.1016/0002-9378(51)90180-9

7. Sperschneider ML, Hengartner MP, Kohl-Schwartz A, et al. Does endometriosis affect professional life? A matched case-control study in Switzerland, Germany and Austria. BMJ Open. 2019;9(1):e019570. doi:10.1136/bmjopen-2017-019570

8. Koller D, Pathak GA, Wendt FR, et al. Epidemiologic and genetic associations of endometriosis with depression, anxiety, and eating disorders. JAMA Netw Open. 2023;6(1):e2251214. doi:10.1001/jamanetworkopen.2022.51214

9. Fuldeore M, Yang H, Du EX, Soliman AM, Wu EQ, Winkel C. Healthcare utilization and costs in women diagnosed with endometriosis before and after diagnosis: a longitudinal analysis of claims databases. Fertil Steril. 2015;103(1):163-171. doi:10.1016/j.fertnstert.2014.10.011

10. Fauconnier A, Staraci S, Huchon C, Roman H, Panel P, Descamps P. Comparison of patient- and physician-based descriptions of symptoms of endometriosis: a qualitative study. Hum Reprod. 2013;28(10):2686-2694. doi:10.1093/humrep/det310

11. Hadfield R, Mardon H, Barlow D, Kennedy S. Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK. Hum Reprod. 1996;11(4):878-880. doi:10.1093/oxfordjournals.humrep.a019270

12. Arruda MS, Petta CA, Abrão MS, Benetti-Pinto CL. Time elapsed from onset of symptoms to diagnosis of endometriosis in a cohort study of Brazilian women. Hum Reprod. 2003;18(4):756-759. doi:10.1093/humrep/deg136

13. Stratton P, Berkley KJ. Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications. Hum Reprod Update. 2011;17(3):327-346. doi:10.1093/humupd/dmq050

14. Johnson NP, Hummelshoj L, Adamson GD, et al. World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod. 2017;32(2):315-324. doi:10.1093/humrep/dew293

15. Zondervan KT, Becker CM, Missmer SA. Endometriosis. New Engl J Med. 2020;382(13):1244-1256. doi:10.1056/NEJMra1810764

16. American Institute of Ultrasound in Medicine (AIUM), American College of Radiology (ACR), American College of Obstetricians and Gynecologists (ACOG), Society for Pediatric Radiology (SPR), Society of Radiologists in Ultrasound (SRU). AIUM practice guideline for the performance of ultrasound of the female pelvis. J Ultrasound Med. 2014;33(6):1122-1130. doi:10.7863/ultra.33.6.1122

17. Rosefort A, Huchon C, Estrade S, Paternostre A, Bernard JP, Fauconnier A. Is training sufficient for ultrasound operators to diagnose deep infiltrating endometriosis and bowel involvement by transvaginal ultrasound? J Gynecol Obstet Hum Reprod. 2019;48(2):109-114. doi:10.1016/j.jogoh.2018.04.004

18. Fraser MA, Agarwal S, Chen I, Singh SS. Routine vs. expert-guided transvaginal ultrasound in the diagnosis of endometriosis: a retrospective review. Abdom Imaging. 2015;40(3):587-594. doi:10.1007/s00261-014-0243-5

19. Gerges B, Li W, Leonardi M, Mol BW, Condous G. Meta-analysis and systematic review to determine the optimal imaging modality for the detection of uterosacral ligaments/torus uterinus, rectovaginal septum and vaginal deep endometriosis. Hum Reprod Open. 2021;2021(4):hoab041. doi:10.1093/hropen/hoab041

20. Reid S, Lu C, Casikar I, et al. Prediction of pouch of Douglas obliteration in women with suspected endometriosis using a new real-time dynamic transvaginal ultrasound technique: the sliding sign. Ultrasound Obstet Gynecol. 2013;41(6):685-691. doi:10.1002/uog.12305

21. Foti PV, Farina R, Palmucci S, et al. Endometriosis: clinical features, MR imaging findings and pathologic correlation. Insights Imaging. 2018;9(2):149-172. doi:10.1007/s13244-017-0591-0

22. Guerriero S, Condous G, van den Bosch T, et al. Systematic approach to sonographic evaluation of the pelvis in women with suspected endometriosis, including terms, definitions and measurements: a consensus opinion from the International Deep Endometriosis Analysis (IDEA) group. Ultrasound Obstet Gynecol. 2016;48(3):318-332. doi:10.1002/uog.15955

23. Eisenberg VH, Arbib N, Schiff E, Goldenberg M, Seidman DS, Soriano D. Sonographic signs of adenomyosis are prevalent in women undergoing surgery for endometriosis and may suggest a higher risk of infertility. Biomed Res Int. 2017;2017:8967803. doi:10.1155/2017/8967803

24. Naftalin J, Hoo W, Pateman K, Mavrelos D, Holland T, Jurkovic D. How common is adenomyosis? A prospective study of prevalence using transvaginal ultrasound in a gynaecology clinic. Hum Reprod. 2012;27(12):3432-3439. doi:10.1093/humrep/des332

25. Kunz G, Beil D, Huppert P, Noe M, Kissler S, Leyendecker G. Adenomyosis in endometriosis—prevalence and impact on fertility. Evidence from magnetic resonance imaging. Hum Reprod. 2005;20(8):2309-2316. doi:10.1093/humrep/dei021

26. Leyendecker G, Bilgicyildirim A, Inacker M, et al. Adenomyosis and endometriosis. Re-visiting their association and further insights into the mechanisms of auto-traumatisation. An MRI study. Arch Gynecol Obstet. 2015;291(4):917-932. doi:10.1007/s00404-014-3437-8

27. Lazzeri L, Di Giovanni A, Exacoustos C, et al. Preoperative and postoperative clinical and transvaginal ultrasound findings of adenomyosis in patients with deep infiltrating endometriosis. Reprod Sci. 2014;21(8):1027-1033. doi:10.1177/1933719114522520

28. Nisenblat V, Bossuyt PMM, Farquhar C, Johnson N, Hull ML. Imaging modalities for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev. 2016;2(2):CD009591. doi:10.1002/14651858.CD009591.pub2

29. Banerjee SK, Ballard KD, Wright JT. Endometriomas as a marker of disease severity. J Minim Invasive Gynecol. 2008;15(5):538-540. doi:10.1016/j.jmig.2008.05.004

30. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril. 1999;72(2):310-315. doi:10.1016/s0015-0282(99)00211-3

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32. Timmerman D, Testa AC, Bourne T, et al. Simple ultrasound-based rules for the diagnosis of ovarian cancer. Ultrasound Obstet Gynecol. 2008;31(6):681-690. doi:10.1002/uog.5365

33. Ghezzi F, Raio L, Cromi A, et al. “Kissing ovaries”: a sonographic sign of moderate to severe endometriosis. Fertil Steril. 2005;83(1):143-147. doi:10.1016/j.fertnstert.2004.05.094

34. Rao T, Condous G, Reid S. Ovarian immobility at transvaginal ultrasound: an important sonographic marker for prediction of need for pelvic sidewall surgery in women with suspected endometriosis. J Ultrasound Med. 2022;41(5):1109-1113. doi:10.1002/jum.15800

35. Hudelist G, Fritzer N, Staettner S, et al. Uterine sliding sign: a simple sonographic predictor for presence of deep infiltrating endometriosis of the rectum. Ultrasound Obstet Gynecol. 2013;41(6):692-695. doi:10.1002/uog.12431

36. Khong SY, Bignardi T, Luscombe G, Lam A. Is pouch of Douglas obliteration a marker of bowel endometriosis? J Minim Invasive Gynecol. 2011;18(3):333-337. doi:10.1016/j.jmig.2011.01.011

37. Bailey HR, Ott MT, Hartendorp P. Aggressive surgical management for advanced colorectal endometriosis. Dis Colon Rectum. 1994;37(8):747-753. doi:10.1007/BF02050136

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Ultra Sound Machine A recent study reveals that adolescents with autism and other developmental disabilities have fewer visits to obstetrician-gynecologists and lower hormonal contraceptive use compared to their typically developing peers, highlighting a need for improved reproductive health services.