Deep Endometriosis of The Uterosacral Ligaments

Endometriosis is a highly prevalent and debilitating whole-body disease characterized by the abnormal growth of endometrial-like cells outside the uterus, leading to hallmark symptoms of chronic pain, inflammation, and infertility ¹. Of the three primary phenotypes of endometriosis, deep endometriosis (DE) is considered the most severe form of the disease, characterized by the infiltration of abnormal growth into the fibromuscular tissue ². DE has been shown to distort the anatomical environment through both infiltration and adhesions within the surrounding milieu ³. Though all forms of endometriosis are widely associated with hallmark symptomology, DE is strongly associated with chronic pelvic pain, dysmenorrhea (painful menstrual periods), deep dyspareunia (pain during sexual intercourse), and gastrointestinal disturbances. ^4–6

Historically, DE was classified based solely on the level of infiltration greater than >5mm into peritoneum and any involvement of muscularis layers of bowel or bladder ^7,8. This definition is now challenged by a 2021 international terminology consensus, whereby DE is a deposit of endometriosis with any penetration depth, and conversely, superficial endometriosis lines the peritoneum or other structures without any infiltration depth ⁸. Limitations remain despite some improvement in characterizing DE through developing novel classification and staging systems. The revised American Society for Reproductive Medicine (rASRM) score is a widely adopted staging system for endometriosis, whereby disease is characterized as minimal, mild, moderate, and severe, using a cumulative point-grading system. Though rASRM describes features of DE in peritoneum, such as depth of infiltration, the staging guideline poorly described the location and extent of DE involved in various pelvic organs ⁸. In contrast, the revised #Enzian staging guidelines stage disease relative to anatomical compartments and invasion grading, precisely defining the location and extent of involved retroperitoneal structures, allowing for surgical planning. Furthermore, the #Enzian staging system includes highly prevalent uterosacral ligaments (USL) DE, which would be included the ASRM system as part of the peritoneum ⁹. Additionally, the American Association of Gynecologic Laparoscopists (AAGL) classification has been developed to stage endometriosis laparoscopically using a scoring system based on disease locale, level of infiltration, and adhesion states ¹⁰. Beyond surgical staging, the Ultrasound-Based Endometriosis Staging System (UBESS) has been developed to stage endometriosis pre-operatively relative to the presence of DE and OE, and ovarian and posterior adhesion states ¹¹. Although several classifications of endometriosis remain, there is currently no gold standard. Recently, a working group involving the European Society for Gynaecological Endoscopy (ESHRE) and World Endometriosis Society (WES) illuminated the need for a novel and standardized classification guidelines given the current strength and limitations for each ¹².

The USLs are bilateral connective tissue band-like structures between the uterus and sacrum, connected by the torus uterinus (TU), providing support, structure, and maintaining normal anatomy. Furthermore, the USLs carry the vital inferior hypogastric plexus (IHP), a complex network of nerves innervating nearly all pelvic organs, including the bladder, bowel, uterus, vagina and the visceral portion of the levator ani muscle ^13,14. The USLs and the respective neuronal network orchestrate nearly all physiological processes and mediate pain sensation through sympathetic pathways. Additionally, the IHP has been widely associated with chronic pelvic pain and secondary pain associated with endometriosis ^15–18.

N80.322 - Deep endometriosis of the posterior cul-de-sac

N80.3B - Deep endometriosis of the uterosacral ligament(s)

N80.512 - Deep endometriosis of the rectum

The current prevalence of endometriosis is 10% of all people assigned female at birth and 80% of people experiencing CPP ^1,19. The distribution of endometriosis varies greatly depending on the phenotype and location of the disease. Superficial endometriosis maintains the most considerable prevalence in 80% of all endometriosis diagnoses, whereas endometriomas are present in 15 to 20% of diagnoses ²⁰. Historically, DE maintained the lowest prevalence of diagnoses, with reported presentations in 1-2% of cases. However, the expected prevalence has grown substantially, estimated between 10-20% of cases, likely reflecting growth in awareness, referral, and improved first-line diagnostics. With the change in the definitions of SE and DE from the latest terminology consensus, we will see a resultant increase in the prevalence of DE even though there is no reason to believe there is a change in how endometriosis presents itself pathophysiologically on other side of the consensus statement.

The reported anatomical distribution of DE has remained relatively consistent, though some variation remains depending on the diagnostic modality and cohort assessed. However, the substantial presentation of DE in the posterior compartment has been widely appreciated, with studies reporting a prevalence of up to 98% of all DE cases in the posterior compartment ^4,21–23. Typical locales of DE within the posterior compartment include the TU, USLs, bowel, pouch of Douglas (POD), parametrium, and posterior vaginal fornix ^21,24. Although DE is most commonly found in the posterior compartment, it should be noted that DE may also form throughout the anterior compartment, including the bladder and ureters, though far less common. Among both laparoscopically and noninvasively diagnosed DE nodules, most studies agree that the most common locale for DE remains the USLs, with a prevalence ranging between 21% and 61% of DE diagnoses ^4,20,22.

The origin of endometriosis has been one of the most explored topics, though it remains highly complex and controversial, with etiology remaining largely unknown ²⁵. Though there has been a historic acceptance of Sampson retrograde flow theory ²⁶, whereby endometrial cells flow in retrograde fashion during menstruation entering the pelvic cavity, retrograde flow as a sole cause has been displaced due to the heterogeneity of the disease and the acceptance of physiological retrograde flow ²⁷. Recent development has illuminated several mechanisms which may contribute to endometriosis development, which may be further divided into cellular (epigenetics, genetic predisposition, and mutations), environmental (toxicants), and combinatory origins (immune dysregulation and hormonal influences) ²⁵. Although several theories have been proposed, the etiology of endometriosis is likely multifaceted, and few explain the heterogeneity in disease presentation phenotypically and clinically. However, the distribution of DE has been primarily identified in the posterior compartment of the pelvis, including the USLs and bowel, where retrograde fluid may readily accumulate, though the driving mechanism remains to be elucidated.

Endometriosis involving the USLs presents a spectrum of clinical manifestations contributing to its pathology's complexity. The most prominent symptom of DE of the USLs is often severe dyspareunia and dysmenorrhea ^4,28. Given the proximity of the USLs to the posterior vaginal fornix, DE may lead to fibrosis, damage, and/or tightening of the ligaments, nerves, and posterior vagina, preventing vaginal stretch and inappropriate uterine contractility. During intercourse, this may lead to spasming, particularly during climax, of the surrounding pelvic floor muscles leading to deep dyspareunia. Other common symptoms include gastrointestinal and urological disturbances, reflecting the proximity of the USLs to pelvic structures, muscles, viscera, and nerves. Being the most common locale for DE, individual or bilateral USLs may be affected directly by nodules and adhesions, leading to thickening, scarring, and distortion of the ligaments or pelvic environment (Figure 1) ^29,30. Similarly, these lesions can extend beyond the ligaments, including the adjacent TU or parametrium or involve nearby structures such as the rectum, sigmoid colon, and the posterior vaginal fornix ³¹.

Prior to any advanced imaging and/or surgical evaluation, a detailed evaluation of a patient’s presentation, including symptomatology via clinical history and physical examination, is pivotal in the clinical care pathway in order to provide high quality care. Deep disease of the USLs is rarely assessed exclusively during an examination or imaging – that is, a full assessment of all forms of endometriosis and other pain-generating mechanisms is complete. However, there are soft markers associated with clinical presentation and physical examination, whereby symptom complexes may be associated with USL disease. In some instances, DE of the USLs may be palpable on examination, with positive site-specific tenderness, which may be valuable method to diagnose USL disease, guide advanced imaging, and predict treatment response at surgery.

Laparoscopy

Historically, surgical visualization through laparoscopic examination followed by histological confirmation was the most widely adopted method for diagnosing endometriosis ³². Though it is mainly dependent on the surgeon, the entire pelvic cavity is evaluated for all phenotypic presentations and locales of the disease, including the anterior compartment (bladder, ureters), middle compartment (uterus, ovaries, ovarian fossa, and tubes), and the posterior compartment (bowel, USLs, TU, posterior vaginal fornix, and the rectouterine pouch) ^33,34. In recent years, performing laparoscopy solely for diagnostic purposes has been reduced, instead reserving laparoscopy as a surgical confirmation and as simultaneous treatment when endometriosis is identified ³⁵.When laparoscopy is used as a diagnostic (and treatment) modality, limitations remain, specifically the relative risk of complications compared to other diagnostic tests, resource consumption,  and the extensive surgical wait times globally, promoting diagnostic delay among those affected ³⁶.

Parallel to most diagnostic modalities, laparoscopy highly depends on the surgeon’s ability to recognize the ectopic growth. A surgeon’s diagnostic test accuracy at surgery might be impacted by the heterogeneous nature of endometriosis, with substantial variation in disease presentation, including size, infiltration depth, shape, locale, and colour ^4,22,37.  When evaluating specific locales, the sensitivity and specificities, PPVs, and NPVs between the USLs ranged 100%, 74– 77%, 58-61%, and 100%, respectively ³⁸. Phenotypically, USL disease was primarily described as ‘puckered pigmented,’ though vesicular and scarred lesions were also described ³⁸.

It should be noted, however, that most studies evaluating the site-specific accuracy of laparoscopy diverge in classification systems and fail to report how many of the lesions were truly DE. Furthermore, most of the studies were published before the novel definition and classification of DE, characterized by any level of infiltration. Additionally, the imperfect relationship between what is seen laparoscopically and confirmed histologically should be appreciated, with variation in diagnostic performance being highly dependent on the heterogeneity of the disease. Specific to the USLs, in the case of severe disease of the posterior compartment, such as POD obliteration, anatomic distortion may impair a surgeon’s ability to visualize USL disease ³⁹. Even if the surgeon has the skill to dissect an obliterated POD, the classic appearances of USL DE are essentially non-existent upon reaching those regions due to anatomical distortion and bloody/cauterized planes. Subsequently, preoperative non-invasive imaging is imperative in surgical planning to identify and characterize the highly prevalent DE of the USLs.

Ultrasound

Though there has been a historical dependence on surgical visualization and a detailed clinical history to diagnose most phenotypes of endometriosis, recent advances in non-invasive diagnostics have improved the diagnostic performance of transvaginal ultrasound (TVS). Novel guidelines, including the International Deep Endometriosis Analysis (IDEA) consensus, have standardized terminology, allowing for homogenous reporting when describing the same structures and anatomical locations ⁴⁰. Currently, TVS has a parallel, and in some cases an improved site-specific performance, relative to surgical laparoscopy for DE and endometriomas, with a sensitivity ranging from 55 to 100% and specificities of 67 to 100% ^24,31,40. Though specific locales, such as the bowel and ureters may be diagnosed with high accuracy, the USLs remain the most difficult to diagnose, with the lowest diagnostic performance with a sensitivity and specificity of 60-67% and 86-95% ^24,31,40.

Despite developments in the standardization of terminology, extensive variation in reported diagnostic performance remains. Though many centers have adopted the IDEA consensus in reporting DE, dichotomy remains between an anterior and posterior TVS approach, particularly in diagnosing DE of the USLs. This dichotomy applies primarily to those with anteverted uteruses (or anteverted retroflexed), whereby the natural space for the TVS probe is the anterior vaginal fornix. Conversely, retroverted uteruses have a larger posterior vaginal fornix, and as such, the probe naturally settles here. In retroverted uteruses, it is really only possible to utilize a posterior approach.

Anterior Approach

To assess the posterior compartment using the anterior approach, the TVS probe is inserted in the anterior vaginal fornix. The USLs can be evaluated in both sagittal and transversal sections and appear as hyperechoic tissue surrounding the cervix ^41,42, as follows (Video 1):

1. Introduce the probe into the anterior vaginal fornix. 
2. Set the depth to ensure that the cervix occupies 2/3 of the screen and the focal point is just behind the cervix.
3. In a sagittal section, the following structures can be visualized: cervix, vaginal wall, vaginal fornix, uterine torus and retrocervix.
4. Then, slowly move the probe to the right so the right USL can be assessed.
5. Repeat the same movements on the other side to visualize the left USL.
6. Sweep the probe 90° clockwise and then cranio-caudally to assess the USL transversally.

Posterior Approach

In comparison to an anterior approach, several studies propose evaluating the pelvis for DE using a posterior approach or insertion of the TVS probe along the posterior vaginal fornix ^29,43,44. Given the extensive prevalence of DE within posterior structures, such as the bowels, POD, vaginal fornix, and USLs, this approach allows for direct visualization of posterior disease due to the proximity of the probe, compared to the anterior approach, which visualizes this space through the cervix. Sonographically, using a posterior approach (oblique sagittal orientation), the USL is described as hyperechoic bands at the level of the internal cervical os, fanning out caudally and merging with the lateral rectal ligaments, proximal to the sacrum.

The technique reported by Leonardi and Condous (2019) for the evaluation of the USLs using a posterior approach may be found here and involves ⁴⁴:

1. Insert the TVS probe in the posterior vaginal fornix with the cervix and uterus anterior.
2. Decrease the penetration depth of the field to have a small depth of field as the region of interest is now very near to the probe. Position the focal point nearest to the TVS probe.
3. Begin with the probe in a midsagittal position, angled toward the rectum. Attempt to visualize the hypoechoic vaginal mucosa, nearest to the probe, and hyperechoic the posterior pouch of Douglas (POD) peritoneum, the next layer after the vagina. This hyperechoic line must be followed closely in the next step.
4. For the left USL, slowly sweep the TVS probe to the right leg and rotate counter‐clockwise (usually not more than 45°); the hyperechoic line (peritoneum) should begin to thicken. When you identify this region, stop when the hyperechoic line is thickest. This is the USL in the sagittal section. If the probe bypasses the USL laterally, the heterogenous contents of the pelvic sidewall will be reached. Slowly reverse in the opposite direction.
5. The same can be repeated for the right USL, with the rotation clockwise in this case.

Irrespective of a posterior or anterior approach, when there is USL involvement of DE, the nodule appears as a hypoechoic nodule, or a break in continuity, of the superficial hyperechoic bands Video 1. Herein, the characterization of the disease follows the IDEA consensus, measuring the nodule in three orthogonal planes ⁴⁰. In some cases, DE may be present closer to the point of insertion (along the TU), the proximal aspect of the USLs, or the distal aspect of the USLs along the peritoneum ²⁹. Furthermore, contiguous, or ‘horseshoe’ nodules have been appreciated, where a DE nodule of the USLs may be present on bilateral USLs and the connective TU. A recent study evaluating the diagnostic accuracy of the TVS posterior approach in diagnosing DE of the USLs and DE suggests an improved performance, with accuracies ranging from 92.6 to 100% ²⁹. At this point, as far as we are aware, there have been no publications that specifically state the use of the anterior approach. The dozens of diagnostic test accuracy studies that have aimed to assess USL DE have either not at all or minimally described technique ⁴⁵.

It should be noted that in the presence of physiological fluid within the POD, the acoustic window is enhanced, allowing for a more detailed evaluation of DE at the sacral aspect and evaluation of superficial endometriosis of the USL, though this remains to be explored and validated. Uterus orientation may also influence how the USLs are visualized on TVS, where retroversion may influence, and in some cases improve, how the USLs are visualized due to the immediate positioning of the probe within the posterior vaginal fornix. In the presence of severe disease, including obliteration of the POD, it is imperative for a more detailed evaluation of the USL involvement. Characteristically, obliteration of an anteverted uterus is more associated with bowel DE and obliteration of retroverted uterus may be more associated with USL DE ⁴⁶. In some cases, anatomy from the adnexa, including the ovaries, may adhere along the USLs, further distorting anatomy, Figure 2. All features should be documented and reported, characterizing disease severity, management, and surgical planning.

Limitations of TVS

Although TVS has shown indisputable improvement in diagnosing DE, several limitations remain. Due to its elusive nature, TVS relies on extensive expertise and high-quality equipment to visualize normal and abnormal anatomy, particularly of the USLs. Specifically, in the presence of severe disease, the anatomy and respective landmarks may be distorted, aiding in the complexity of diagnosis mapping disease ³¹. A more detailed evaluation of the respective compartments is imperative in these cases. However, it is currently unknown how severe disease influences the diagnostic performance of TVS, particularly of the USLs.

Furthermore, although there has been significant improvement in TVS through standardization in reporting, some variation remains in diagnostic performance depending on the approach utilized. There is likely no one correct way of diagnosing DE of the USLs between an anterior and posterior TVS approach. Irrespective, normal and abnormal USLs may be visualized and characterized with extensive training. However, the dichotomy between both approaches limits the reproducibility and current estimated site-specific diagnostic performances. It is possible that the techniques are complementary rather than one should be preferentially used.

There is currently no cure for endometriosis; however, there are several methods of treating and managing the life-long and multisystem disease. Similarly, there are no treatment guidelines or current studies evaluating the effectiveness of current treatments specific to the phenotype and locale of endometriosis. Generalized approaches are adopted between pharmacological intervention using hormonal therapy or surgical resection of disease, with treatments largely dependent on current and future fertility ⁵.

Traditional laparoscopic resection of DE involves an initial complete evaluation of all pelvic sites for disease, whereby DE may be excised directly from the surrounding tissue. However, due to the superficial nature of the USLs, the extent of resection is highly dependent on the disease severity and level of infiltration ^47,48. If a nodule has minor infiltration within the connective bands, the USLs may be spared, with dissection and resection solely of the nodule with respective margins. Comparatively, if the DE has significant infiltration into the USLs, extensive dissection may be performed, potentially necessitating complete removal of the affected USL. In the presence of severe disease, normalization of anatomy through adhesiolysis and dissection within the retroperitoneum (i.e. complete ureterolyses are often needed) and pararectal space may need to be performed to access the USLs and the respective disease ⁴⁹.

Few current studies evaluate symptom improvement associated with laparoscopic resection and dissection of DE of the USLs. However, it has been suggested that a substantial improvement in symptoms, with up to 84.2% of patients with dysmenorrhea, 94.1% with deep dyspareunia, and 77.7% of patients with chronic pelvic pain, followed by USL DE resection ^48,50. Adhesions are a common yet clinically significant byproduct of surgery. Among those with USL resection, over half of the patients experience filmy avascular and vascular adhesions at the site of USL resection ⁵¹. Excision of DE of the USLs has also been associated with fertility outcomes, with approximately half of patients being able to conceive spontaneously and having an intrauterine pregnancy, though the findings were largely observational, requiring further robust investigation ⁵². Although it is currently unknown how laparoscopic resection of DE of the USLs influences symptoms not traditionally associated as being gynecological in origin, including gastrointestinal and urinary symptoms, it is imperative to consider nerve-sparing excision ^14,53. Due to the proximity of the hypogastric along the USLs, ureters, and pararectal space, it is essential for the surgeon to initially map the hypogastric and anatomical landmarks to decrease the risk of complication among those with DE of the USLs ¹⁴.

Beyond surgical and hormonal approaches, self-management and holistic approaches have proven to be invaluable in the management of endometriosis symptoms, including various multimodal approaches such as diet, yoga, heat, mindfulness, cannabis, and physical therapy ^54,55. Studies have suggested that over 75% of people with endometriosis use self-management strategies to manage varying symptoms or improve aspects of quality of life that have been negatively impacted, including pain, sleep, stress, intercourse, gastrointestinal function, and physical and mental health ⁵⁴. Physical strategies such as physical therapy have shown significant improvement in pelvic floor function, including muscle relaxation and a reduction of dyspareunia and chronic pelvic pain ^56,57.  Similarly, psychosocial strategies, such as mindfulness-based psychological intervention, have significantly reduced pain and improved well-being and overall quality of life, with lasting effects ^58,59. Although these strategies remain widely adopted, it is currently unknown what the effectiveness of hormonal therapy and self-management strategies are on DE of the USLs.

The intricate landscape of DE within the USLs presents a multifaceted challenge for researchers and clinicians, remaining the most common location with historically poor diagnostic accuracy. From unravelling its etiological underpinnings and understanding its epidemiological impact to discussing advancements in diagnostics and diverse treatment modalities, our examination underscores the complexity of this condition. Addressing DE of the USLs necessitates ongoing research, innovation, and personalized care strategies to improve outcomes and enhance the quality of life for those affected by this challenging gynecological condition.

1.        Zondervan KT, Becker CM, Missmer SA. Endometriosis. N Engl J Med [Internet] 2020 [cited 2021 Oct 16];382:1244–56. Available from: https://www.nejm.org/doi/full/10.1056/NEJMra1810764

2.        Singh S, Soliman AM, Rahal Y, Robert C, Defoy I, Nisbet P, et al. Prevalence, Symptomatic Burden, and Diagnosis of Endometriosis in Canada: Cross-Sectional Survey of 30 000 Women. J Obstet Gynaecol Canada 2020;42:829–38.

3.        Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril [Internet] 2012 [cited 2021 Aug 26];98:564–71. Available from: http://www.fertstert.org/article/S0015028212017979/fulltext

4.        Dai Y, Leng JH, Lang JH, Li XY, Zhang JJ. Anatomical distribution of pelvic deep infiltrating endometriosis and its relationship with pain symptoms. Chin Med J (Engl) [Internet] 2012 [cited 2023 Jun 2];125:209–13. Available from: https://journals.lww.com/cmj/Fulltext/2012/01020/Anatomical_distribution_of_pelvic_deep.10.aspx

5.        Vercellini P, Viganò P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol 2013 105 [Internet] 2013 [cited 2021 Sep 12];10:261–75. Available from: https://www.nature.com/articles/nrendo.2013.255

6.        Fauconnier A, Chapron C, Dubuisson JB, Vieira M, Dousset B, Bréart G. Relation between pain symptoms and the anatomic location of deep infiltrating endometriosis. Fertil Steril 2002;78:719–26.

7.        Abrao MS, Andres MP, Miller CE, Gingold JA, Rius M, Neto JS, et al. AAGL 2021 Endometriosis Classification: An Anatomy-based Surgical Complexity Score. J Minim Invasive Gynecol [Internet] 2021 [cited 2021 Dec 31];28:1941-1950.e1. Available from: http://www.jmig.org/article/S1553465021011730/fulltext

8.        International Working Group of AAGL EE and W, Tomassetti C, Johnson NP, Petrozza J, Abrao MS, Einarsson JI, et al. An international terminology for endometriosis, 2021,. Hum Reprod Open [Internet] 2021 [cited 2022 Aug 24];2021:16. Available from: https://academic.oup.com/hropen/article/2021/4/hoab029/6406627

9.        Keckstein J, Saridogan E, Ulrich UA, Sillem M, Oppelt P, Schweppe KW, et al. The #Enzian classification: A comprehensive non-invasive and surgical description system for endometriosis. Acta Obstet Gynecol Scand [Internet] 2021 [cited 2021 Oct 21];100:1165–75. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/aogs.14099

10.      Abrao MS, Andres MP, Miller CE, Gingold JA, Rius M, Neto JS, et al. AAGL 2021 Endometriosis Classification: An Anatomy-based Surgical Complexity Score. J Minim Invasive Gynecol [Internet] 2021 [cited 2021 Oct 21];0:0–1. Available from: http://www.jmig.org/article/S1553465021011730/fulltext

11.      Menakaya U, Reid S, Lu C, Bassem G, Infante F, Condous G. Performance of  ultrasound-based endometriosis staging system (UBESS) for predicting level of complexity of laparoscopic surgery for endometriosis. Ultrasound Obstet Gynecol [Internet] 2016 [cited 2022 Aug 24];48:786–95. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.15858

12.      Keckstein J, Becker CM, Canis M, Feki A, Grimbizis GF, Hummelshoj L, et al. Recommendations for the surgical treatment of endometriosis. Part 2: Deep endometriosis. Hum Reprod Open [Internet] 2020 [cited 2023 Nov 30];2020. Available from: https://pubmed.ncbi.nlm.nih.gov/32064361/

13.      Azaïs H, Collinet P, Delmas V, Rubod C. Uterosacral ligament and hypogastric nerve anatomical relationship. Application to deep endometriotic nodules surgery. Gynécologie Obs Fertil 2013;41:179–83.

14.      Lemos N, Souza C, Marques RM, Kamergorodsky G, Schor E, Girão MJBC. Laparoscopic anatomy of the autonomic nerves of the pelvis and the concept of nerve-sparing surgery by direct visualization of autonomic nerve bundles. Fertil Steril [Internet] 2015 [cited 2023 Jun 12];104:e11–2. Available from: http://www.fertstert.org/article/S0015028215016490/fulltext

15.      Nascu PC, Vilos GA, Ettler HC, Abu-Rafea B, Hollet-Caines J, Ahmad R. Histopathologic findings on uterosacral ligaments in women with chronic pelvic pain and visually normal pelvis at laparoscopy. J Minim Invasive Gynecol [Internet] 2006 [cited 2023 Jun 13];13:201–4. Available from: http://www.jmig.org/article/S1553465006000720/fulltext

16.      Khodaverdi S, Alebouyeh MR, Sadegi K, Mehdizadehkashi A, Kaveh M, Entezari SR, et al. Superior hypogastric plexus block as an effective treatment method for endometriosis-related chronic pelvic pain: an open-label pilot clinical trial. J Obstet Gynaecol [Internet] 2021 [cited 2023 Jun 13];41:966–71. Available from: https://pubmed.ncbi.nlm.nih.gov/33243036/

17.      Urits I, Schwartz R, Siddaiah HB, Kikkeri S, Chernobylsky D, Charipova K, et al. Inferior Hypogastric Block for the Treatment of Chronic Pelvic Pain. Anesthesiol Pain Med 2021 111 [Internet] 2021 [cited 2023 Jun 13];11:1–9. Available from: https://brieflands.com/articles/aapm-112225.html

18.      Dubernard G, Rouzier R, David-Montefiore E, Bazot M, Daraï E. Urinary Complications After Surgery for Posterior Deep Infiltrating Endometriosis are Related to the Extent of Dissection and to Uterosacral Ligaments Resection. J Minim Invasive Gynecol [Internet] 2008 [cited 2023 Jun 13];15:235–40. Available from: http://www.jmig.org/article/S1553465007011995/fulltext

19.      Sarria-Santamera A, Orazumbekova B, Terzic M, Issanov A, Chaowen C, Asúnsolo-Del-barco A. Systematic Review and Meta-Analysis of Incidence and Prevalence of Endometriosis. Healthc 2021, Vol 9, Page 29 [Internet] 2020 [cited 2023 Jun 13];9:29. Available from: https://www.mdpi.com/2227-9032/9/1/29/htm

20.      Chaggar P, Tellum T, Thanatsis N, De Braud L V., Setty T, Jurkovic D. Prevalence of deep and ovarian endometriosis in women attending a general gynecology clinic: prospective cohort study. Ultrasound Obstet Gynecol [Internet] 2023 [cited 2023 Oct 2];61:632–41. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.26175

21.      Manieri Rocha R, Leonardi M, Eathorne A, Armour M, Condous G. Anatomical distribution of endometriosis: A cross-sectional analysis of transvaginal ultrasound in symptomatic patients. Australas J Ultrasound Med [Internet] 2023 [cited 2023 Apr 23];https://doi.org/10.1002/ajum.12327. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/ajum.12327

22.      Audebert A, Petousis S, Margioula-Siarkou C, Ravanos K, Prapas N, Prapas Y. Anatomic distribution of endometriosis: A reappraisal based on series of 1101 patients. Eur J Obstet Gynecol Reprod Biol 2018;230:36–40.

23.      Chapron C, Fauconnier A, Vieira M, Barakat H, Dousset B, Pansini V, et al. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod [Internet] 2003 [cited 2023 Jan 30];18:157–61. Available from: https://academic.oup.com/humrep/article/18/1/157/880320

24.      Indrielle-Kelly T, Frühauf F, Fanta M, Burgetova A, Lavu D, Dundr P, et al. Diagnostic Accuracy of Ultrasound and MRI in the Mapping of Deep Pelvic Endometriosis Using the International Deep Endometriosis Analysis (IDEA) Consensus. Biomed Res Int 2020;2020.

25.      Saunders PTK, Horne AW. Endometriosis: Etiology, pathobiology, and therapeutic prospects. Cell [Internet] 2021 [cited 2023 Nov 20];184:2807–24. Available from: http://www.cell.com/article/S0092867421005766/fulltext

26.      Sampson J. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obs Gynecol [Internet] 1927 [cited 2021 Oct 20];14:422–69. Available from: https://ci.nii.ac.jp/naid/10018118388

27.      Vercellini ( P, Somigliana E, Fedele L, Vercellini P, Vercellini P, Viganò P, et al. Endometriosis: pathogenesis and treatment. Nat Rev | Endocrinol [Internet] 2014 [cited 2021 Sep 12];10:261–75. Available from: www.nature.com/nrendo

28.      Chopin N, Vieira M, Borghese B, Foulot H, Dousset B, Coste J, et al. Operative management of deeply infiltrating endometriosis: Results on pelvic pain symptoms according to a surgical classification. J Minim Invasive Gynecol [Internet] 2005 [cited 2023 Nov 20];12:106–12. Available from: http://www.jmig.org/article/S1553465005000464/fulltext

29.      Freger SM, Mathew L, Freger SM, Turnbull V, Mcgowan K, Leonardi M, et al. Prospective diagnostic test accuracy of uterosacral ligament and torus uterinus endometriosis using transvaginal ultrasound posterior approach. Ultrasound Obstet Gynecol [Internet] 2023 [cited 2023 Oct 2];Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.27492

30.      Zhang Y, Xiao X, Xu F, Lin Q, Xu J, Du B. Evaluation of uterosacral ligament involvement in deep endometriosis by transvaginal ultrasonography. Front Pharmacol 2019;10:430427.

31.      Leonardi M, Uzuner C, Mestdagh W, Lu C, Guerriero S, Zajicek M, et al. Diagnostic accuracy of transvaginal ultrasound for detection of endometriosis using International Deep Endometriosis Analysis (IDEA) approach: prospective international pilot study. Ultrasound Obs Gynecol [Internet] 2022 [cited 2023 Jan 30];60:404–13. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.24936

32.      Gratton SM, Choudhry AJ, Vilos GA, Vilos A, Baier K, Holubeshen S, et al. Diagnosis of Endometriosis at Laparoscopy: A Validation Study Comparing Surgeon Visualization with Histologic Findings. J Obstet Gynaecol Canada [Internet] 2022 [cited 2023 Nov 20];44:135–41. Available from: http://www.jogc.com/article/S1701216321006976/fulltext

33.      Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS, Abrao MS, et al. World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod [Internet] 2017 [cited 2022 Apr 7];32:315–24. Available from: https://academic.oup.com/humrep/article/32/2/315/2631390

34.      Becker CM, Bokor A, Heikinheimo O, Horne A, Jansen F, Kiesel L, et al. ESHRE guideline: endometriosis. Hum Reprod Open [Internet] 2022 [cited 2022 Apr 7];2022:1–26. Available from: https://academic.oup.com/hropen/article/2022/2/hoac009/6537540

35.      Leonardi M, Gibbons T, Armour M, Wang R, Glanville E, Hodgson R, et al. When to Do Surgery and When Not to Do Surgery for Endometriosis: A Systematic Review and Meta-analysis. J Minim Invasive Gynecol 2020;27:390-407.e3.

36.      Pascoal E, Wessels JM, Aas-Eng MK, Abrao MS, Condous G, Jurkovic D, et al. Strengths and limitations of diagnostic tools for endometriosis and relevance in diagnostic test accuracy research. Ultrasound Obs Gynecol [Internet] 2022 [cited 2023 Jan 30];60:309–27. Available from: https://pubmed.ncbi.nlm.nih.gov/35229963/

37.      Albee RB, Sinervo K, Fisher DT. Laparoscopic excision of lesions suggestive of endometriosis or otherwise atypical in appearance: relationship between visual findings and final histologic diagnosis. J Minim Invasive Gynecol [Internet] 2008 [cited 2023 Feb 25];15:32–7. Available from: https://pubmed.ncbi.nlm.nih.gov/18262141/

38.      Walter AJ, Hentz JG, Magtibay PM, Cornella JL, Magrina JF. Endometriosis: Correlation between histologic and visual findings at laparoscopy. Am J Obstet Gynecol 2001;184:1407–13.

39.      Goncalves M, Neto S, Andres M, Siufi D, de Mattos L, Abrao M. Systematic evaluation of endometriosis by transvaginal ultrasound can accurately replace diagnostic laparoscopy, mainly for deep and ovarian endometriosis. Hum Reprod [Internet] 2021 [cited 2021 Oct 21];36:1492–500. Available from: https://pubmed.ncbi.nlm.nih.gov/33864088/

40.      Guerriero S, Condous G, Bosch T van den, Valentin L, Leone FPG, Schoubroeck D Van, 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 Obs Gynecol [Internet] 2016 [cited 2021 Oct 21];48:318–32. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.15955

41.      Savelli L, Ambrosio M, Salucci P, Raimondo D, Arena A, Seracchioli R. Transvaginal ultrasound features of normal uterosacral ligaments. Fertil Steril [Internet] 2021 [cited 2023 Nov 20];116:275–7. Available from: http://www.fertstert.org/article/S001502822032687X/fulltext

42.      Moro F, Zermano S, Ianieri MM, Nardone ADC, Carfagna P, Ciccarone F, et al. Dynamic transvaginal ultrasound examination for assessing anatomy of parametria. Ultrasound Obstet Gynecol [Internet] 2023 [cited 2023 Nov 20];Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.26313

43.      Leonardi M, Martins WP, Espada M, Arianayagam M, Condous G. Proposed technique to visualize and classify uterosacral ligament deep endometriosis with and without infiltration into parametrium or torus uterinus. Ultrasound Obs Gynecol [Internet] 2020 [cited 2022 Sep 27];55:137–9. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.20300

44.      Leonardi M, Condous G. A pictorial guide to the ultrasound identification and assessment of uterosacral ligaments in women with potential endometriosis. Australas J Ultrasound Med [Internet] 2019 [cited 2023 May 15];22:157–64. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/ajum.12178

45.      Nisenblat V, Bossuyt PMM, Farquhar C, Johnson N, Hull ML. Imaging modalities for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev 2016;Art. No.: CD009591. DOI: 10.1002/14651858.CD009591.

46.      Mick I, Marien M, Tigdi J, Zeni G, Scattolon S, Leonardi M. The “Triangle Sign”: A Novel Dynamic Ultrasound Technique for Identifying an Obliterated Cul-De-Sac in Patients with a Retroverted Uterus. J Minim Invasive Gynecol 2023;30:S68.

47.      Chapron C, Dubuisson JB. Laparoscopic treatment of deep endometriosis located on the uterosacral ligaments. Hum Reprod [Internet] 1996 [cited 2023 Jun 12];11:868–73. Available from: https://dx.doi.org/10.1093/oxfordjournals.humrep.a019268

48.      Chapron C, Dubuisson JB, Fritel X, Fernandez B, Poncelet C, Béguin S, et al. Operative management of deep endometriosis infiltrating the uterosacral ligaments. J Am Assoc Gynecol Laparosc 1999;6:31–7.

49.      Deura I, Kaponis A, Itou M, Taniguchi F, Iwabe T, Harada T. Advanced Techniques of Adhesiolysis for Severe Endometriosis. J Minim Invasive Gynecol [Internet] 2010 [cited 2023 Nov 15];17:S190. Available from: http://www.jmig.org/article/S1553465010004449/fulltext

50.      Chapron C, Dubuisson JB. Laparoscopic treatment of deep endometriosis located on the uterosacral ligaments. Hum Reprod [Internet] 1996 [cited 2023 Nov 20];11:868–73. Available from: https://dx.doi.org/10.1093/oxfordjournals.humrep.a019268

51.      Chapron C, Guibert J, Fauconnier A, Vieira M, Dubuisson JB. Adhesion Formation after Laparoscopic Resection of Uterosacral Ligaments in Women with Endometriosis. J Am Assoc Gynecol Laparosc 2001;8:368–73.

52.      Chapron C, Fritel X, Dubuisson JB. Fertility after laparoscopic management of deep endometriosis infiltrating the uterosacral ligaments. Hum Reprod [Internet] 1999 [cited 2023 Nov 21];14:329–32. Available from: https://dx.doi.org/10.1093/humrep/14.2.329

53.      Fujii M, Sagae S, Sato T, Tsugane M, Murakami G, Kudo R. Investigation of the Localization of Nerves in the Uterosacral Ligament: Determination of the Optimal Site for Uterosacral Nerve Ablation. Gynecol Obstet Invest [Internet] 2002 [cited 2023 Oct 2];54:11–7. Available from: https://dx.doi.org/10.1159/000066289

54.      Armour M, Sinclair J, Chalmers KJ, Smith CA. Self-management strategies amongst Australian women with endometriosis: a national online survey. BMC Complement Altern Med [Internet] 2019 [cited 2021 Dec 31];19. Available from: https://pubmed.ncbi.nlm.nih.gov/30646891/

55.      Leonardi M, Horne AW, Vincent K, Sinclair J, Sherman KA, Ciccia D, et al. Self-management strategies to consider to combat endometriosis symptoms during the COVID-19 pandemic. Hum Reprod Open [Internet] 2020 [cited 2021 Oct 23];2020. Available from: https://academic.oup.com/hropen/article/2020/2/hoaa028/5849477

56.      Del Forno S, Arena A, Alessandrini M, Pellizzone V, Lenzi J, Raimondo D, et al. Transperineal Ultrasound Visual Feedback Assisted Pelvic Floor Muscle Physiotherapy in Women With Deep Infiltrating Endometriosis and Dyspareunia: A Pilot Study. J Sex Marital Ther [Internet] 2020 [cited 2023 Nov 3];46:603–11. Available from: https://www.tandfonline.com/doi/abs/10.1080/0092623X.2020.1765057

57.      Raimondo D, Youssef A, Mabrouk M, Del Forno S, Martelli V, Pilu G, et al. Pelvic floor muscle dysfunction on 3D/4D transperineal ultrasound in patients with deep infiltrating endometriosis: a pilot study. Ultrasound Obstet Gynecol [Internet] 2017 [cited 2023 Nov 15];50:527–32. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/uog.17323

58.      Hansen KE, Kesmodel US, Kold M, Forman A. Long-term effects of mindfulness-based psychological intervention for coping with pain in endometriosis: A six-year follow-up on a pilot study. Nord Psychol [Internet] 2017 [cited 2023 Nov 10];69:100–9. Available from: https://www.tandfonline.com/doi/abs/10.1080/19012276.2016.1181562

59.      Kold M, Hansen T, Vedsted-Hansen H, Forman A. Mindfulness-based psychological intervention for coping with pain in endometriosis. Nord Psychol [Internet] 2012 [cited 2023 Nov 20];64:2–16. Available from: https://www.tandfonline.com/doi/abs/10.1080/19012276.2012.693727

Figure 1: Laparoscopic view of pigmented DE affecting bilateral USLs, without torus involvement.

Legend: DE = Deep Endometriosis, USL = Uterosacral Ligament      

Figure 2: Sonographic visualization of DE of the Left USL impacted by severe adhesions and an endometrioma fixed to the USL, using a transvaginal posterior approach.

Legend: DE = Deep Endometriosis, USL = Uterosacral Ligament      

Video 1: Sonographic visualization of DE of the Left USL using a transvaginal posterior approach, depicted as an anechoic disruption in the hyperechoic USL band.

Legend: DE = Deep Endometriosis, USL = Uterosacral Ligament

Please note that the maximum upload size is 5MB, and larger images and video clips can be sent to [email protected].