The expanding role of sonography for the diagnosis of deep infiltrating endometriosis: Results of a large case series

To investigate the value of the sonographic identification of deep infiltrating endometriosis (DIE) in women presenting with complaints suggestive of DIE. Sonography findings were correlated with subsequent surgical exploration, and histologic verification.


| INTRODUC TI ON
Endometriosis affects about 10% of women of reproductive age in the USA every year, and all too often it evades diagnosis and effective treatment. 1A subtype of it, deep infiltrating endometriosis (DIE), may represent a substantial proportion of all cases of endometriosis, though its exact incidence is currently indeterminable. 2E is difficult to verify with its laparoscopic diagnosis, given that it exists deeper to the peritoneal surface (≥5 mm), where color changes would ordinarily be seen laparoscopically.However, such deep lesions can be seen with three-dimensional transvaginal sonography (3DTVS) in the anterior pelvic compartment, in the cul-de-sac, the rectosigmoid, uterosacral ligaments, and other places in the region.][4][5][6][7][8][9][10][11][12] Given a report suggesting the inaccuracy of this imaging modality, 13 the pathologic verification represented in these studies of sonographic identification of DIE, can be considered as contrasting evidence.A comparison of ultrasound and magnetic resonance imaging for the detection of DIE states that ultrasound is superior. 14th the clinical experience of the authors observing symptomatic patients over a number of years, this series of cases is now described, attempting to correlate the pelvic examination of symptomatic patients with 2D/3DTVS imaging, laparoscopic visualization, and histologic verification.A series of clinical encounters with patients ultimately diagnosed with DIE is described in the present report.The extent of this clinical problem that is posed by some women, and the need to practically diagnose and treat it, may therefore be recognized.

| MATERIAL S AND ME THODS
A series of patient encounters is described where sonography was performed to rule out the presence of DIE in symptomatic patients in whom it was suspected.A total of 307 patients underwent transvaginal sonography, using a GE Standard 2D/3DTVS examination of the suspected areas of DIE (Voluson E8 system; GE Healthcare, Milwaukee, WI, USA) with transvaginal probe 5-9 mHz with volume acquisition and analysis.All 2D/3DTVS examinations were performed and interpreted by the same operator (CF) using the consensus opinion from the International Deep Endometriosis Analysis (IDEA) group for the sonographic diagnosis of DIE. 15 The findings were recorded, and the patients were then referred back to the physicians who had initially requested the ultrasound evaluations, along with the associated sonographic findings and conclusions.Those patients who were evaluated but did not have any features suggestive of DIE are not included in this list of DIE patients.One hundred of the patients who were sonographically diagnosed as having DIE and who opted for its surgical management were referred to surgeons who are skilled with such surgical treatment.It is the list of those patients, who were sonographically diagnosed with DIE, and who then underwent surgi- Statistical analysis was performed for descriptive purposes using IBM SPSS (IBM, Armonk, NY, USA), with a P value less than 0.05 being significant.

| RE SULTS
Of a total of 307 cases sonographically assessed over the years of 2016 through 2022, 100 cases were able to be thoroughly evaluated through surgery and biopsies, and 92 (92%) were conclusively found to have DIE at surgery as the 3DTVS had predicted.The demographic features of this population surveyed in this report are shown in Table 1.Of note, the average parity of 0 in this population should not be surprising, given the well-known association of endometriosis and infertility.Sonographic findings were correlated with the operative findings and the subsequently obtained pathologic confirmation for these 100 patients (Table 2).
The preoperative ultrasound findings of uterosacral ligament b Some patients had multiple complaints.
involvement, cul-de-sac obliteration, hydrosalpinx occurrence, rectovaginal septum involvement, and ovarian endometriomas were confirmed at surgical exploration.For example, there were 92 cases of uterosacral ligament involvement (shown in Figure 1), 53 cases of rectovaginal septum (an example shown in Figure 2), 20 cases of partial or complete cul-de-sac obliteration (an example is shown in Figure 3), 3 cases of hydrosalpinx, and 25 cases of endometriomas that were revealed preoperatively with 2DTVS (an example shown in Figure 4).In addition, an example of a finding in the anterior compartment is revealed in Figure 5. Figure 6a,b demonstrates a rectosigmoid lesion (transverse and longitudinal images displayed).
The spectrum of endometriosis ranges from the superficially implanted, noticeable through visualization of the color changes seen on the peritoneal surfaces (Figure 7), to the deep implantation (≥5 mm below the epithelial layer), which can only be seen sonographically.
Figure 8 shows the process of exploring the retroperitoneal space to remove the sonographically depicted nodularity.In our surgical explorations of those patients who were sonographically demonstrated to have the presence of DIE, evidence of superficial disease was also found in many patients (summarized in Endometriotic implantation was found affecting the appendix in five cases at surgery (5%), although evidence of this could not be seen preoperatively using ultrasound.An example of this is shown in Figure 9, with its histology revealed in Figure 10a,b.Histologic evidence of endometriosis depends on finding at least two of the three associated elements (i.e., endometrial glands, stroma, and hemosiderin deposits), yet in our series all elements were found on histology. 16Other sonographic preoperative findings were identified for relevant gynecologic problems in the course of this investigation.
These other findings are summarized in Table 3, and include leiomyomata, dermoid cyst, uterine septum, bicornuate uterus, and a cystadenofibroma.

| DISCUSS ION
From the 100 patients reviewed with 2D/3DTVS scans, and who had surgical and histologic verification of DIE, some consistent sonographic features have become apparent.The specifically demonstrated sonographic features of DIE that were found are listed in Table 2.The clinical value of combining the sonographic 3DTVS imaging with the skill of performing the bimanual examination was recognized with this case series.An example of this can be seen with the technique using the vaginal transducer to move the uterus (i.e., the "sliding test"), so viewing the degree of pelvic immobility.This is sometimes described as a frozen pelvis, a commonly seen aspect of endometriosis. 17e incidence of appendiceal endometriotic implantation was noteworthy, suggesting that when considering the diagnosis of endometriosis, the appendix should be routinely examined at surgical exploration.Appendiceal endometriosis has been previously mentioned when the diagnosis of endometriosis is discussed, and this case series confirms it as a recognized category of endometriosis. 18 should be underscored that our case series findings resulted from ultrasound interpretations that were made by a gynecologist who spoke with each patient, and gynecologically examined them, and performed the transvaginal sonographic analysis (CF).

Case experience No. of cases
b Includes fibroids, cystadenofibroma, uterine septum, bicornuate uterus, and appendix findings.

F I G U R E 1 Uterosacral ligament (USL) nodularity seen between calipers bilaterally.
Furthermore, a single experienced gynecologic surgeon (AS) performed each of the surgical procedures, performing all of the pertinent biopsies with the described histologic findings.
As is apparent from the current medical literature, DIE is simply part of the spectrum of endometriosis.Although signs of DIE itself cannot be visualized laparoscopically, the previous statements that the diagnosis of endometriosis can only be confirmed by laparoscopy should no longer be considered valid.As the form of endometriosis that can be visualized on the peritoneal surface cannot be visualized sonographically, it appears that both laparoscopy and sonography may be needed for a definitive diagnosis of endometriosis.[21] This analysis included the operative findings of the tissue identified with preoperative 3DTVS.When nodularity of a uterosacral ligament was sonographically noted, the operative dissection found tissue that was histologically consistent with endometriosis.
When obliteration of the cul-de-sac was sonographically noted, cal exploration and histologic sampling, that are included in this case series.The clinical observations were performed consistent with the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) recommendations for observational studies.This retrospective observational report was approved by the Advocate Institutional Review Board (# 22.198ET, exempt) and conducted from September 1, 2016 through April 30, 2022, at Advocate Illinois Masonic Medical Center.Patient consent was deemed as not being required for this analysis and publication.

23 F I G U R E 2 F I G U R E 3 F I G U R E 7 F I G U R E 8 F I G U R E 9
the operative findings confirmed it to be true in each case.Overall, the 3DTVS descriptions were consistent with the operative and histologic reports, underscoring the value of sonography when preoperatively describing the features of DIE.Though the intent of this observational investigation was to correlate the findings of 3DTVS with what can be found in the operating room, to demonstrate its diagnostic value, it seems that there may be potential for designing investigations in the future to compare the benefits and complications of medical and surgical treatment of DIE, based on its sonographic diagnosis, as has been demonstrated by others.22,Rectovaginalseptum (RVS) nodularity between calipers.Sonographic image of cul-de-sac (CDS) obliteration, highlighted by "kissing" ovaries.F I G U R E 4 Two-dimensional transvaginal ultraound image of a left endometrioma, between calipers.Given that there are limited investigations in which sonographic diagnosis, surgical identification, and histologic verification of DIE are compared, it is a strength of the present investigation to offer such details at this time.A limitation of this current investigation can be considered its relatively modest size.However, considering the intricate challenges associated with precisely procuring tissue to authenticate retroperitoneal lesions that are identified clinically and sonographically, establishing the diagnostic efficacy of 3DTVS for any form of endometriosis could present considerable difficulty.In light of the findings in the present study, 3DTVS should be considered as a definitive method for diagnosing DIE, a diagnosis F I G U R E 5 An endometriotic lesion of the posterior bladder wall was found in the anterior compartment.F I G U R E 6 (a) Sagittal image of a rectosigmoid lesion.(b) Transverse image of a rectosigmoid lesion.Laparoscopic appearance of superficial endometriosis of anterior peritoneum shown with arrows.View of the process of opening retroperitoneal space for removal of deep lesions (uterosacral ligament [USL] and rectovaginal septum nodularity).USLs labeled.Laparoscopic image of suspected endometriosis at the tip of the appendix (with attachment of omentum), containing endometriotic implant, confirmed by pathology.F I G U R E 1 0 (a) Histologic picture of appendiceal endometriosis, shown in Figure 9, revealing endometrial glands (arrows) and stroma (bracket).(b) Appendiceal endometriosis displaying region of golden-brown hemosiderin deposits (arrow).TA B L E 3 Other sonographic findings in data set.