Sonographic evaluation of immobility of normal and endometriotic ovary in detection of deep endometriosis

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1 Ultrasound Obstet Gynecol 2017; 49: Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: /uog Sonographic evaluation of immobility of normal and endometriotic ovary in detection of deep endometriosis B. GERGES 1,C.LU 2,S.REID 1,D.CHOU 3,T.CHANG 4,5 and G. CONDOUS 1,5,6 1 Acute Gynaecology, Early Pregnancy and Advanced Endosurgery Unit, Sydney Medical School Nepean, University of Sydney, Nepean Hospital, Penrith, NSW, Australia; 2 Department of Computer Sciences, University of Wales, Aberystwyth, UK; 3 Sydney Women s Endosurgery Centre (SWEC), Hurstville, NSW, Australia; 4 Nureva Women s Specialist Health, Campbelltown, NSW, Australia; 5 Laparoscopic Surgery for General Gynaecologist (LaSGeG), Sydney, NSW, Australia; 6 OMNI Gynaecological Care Centre for Women s Ultrasound and Early Pregnancy, St Leonards, NSW, Australia KEYWORDS: endometrioma; endometriosis; laparoscopy; ovarian mobility; soft markers; transvaginal ultrasound ABSTRACT Objectives To examine the association between ovarian immobility and presence of endometriomas and assess the diagnostic accuracy of transvaginal sonographic (TVS) ovarian immobility in the detection of deep infiltrating endometriosis (DIE). Methods This was a multicenter prospective observational study of women presenting with chronic pelvic pain from January 2009 to March Women with or without history of endometriosis who were scheduled to undergo laparoscopic surgery for endometriosis gave a detailed history and underwent specialized TVS in a tertiary referral unit prior to laparoscopy. During TVS, ovarian mobility and the presence of endometriomas were assessed. The relationship between TVS ovarian mobility, with or without endometriomas, and DIE was correlated with the gold standard, diagnosis of endometriosis at laparoscopy. Results Included in the analysis were 265 women with preoperative TVS and laparoscopic outcomes. Ovarian immobility on TVS was significantly associated with presence of endometriomas at surgery, with a prevalence of 12.2%, 10.8% and 52.7% for fixation of the left ovary only, the right ovary only and bilateral ovaries, respectively, compared with 4.2%, 3.7% and 7.3% for normal ovaries. The sensitivity, specificity, positive (PPV) and negative (NPV) predictive values and positive and negative likelihood ratios of TVS ovarian immobility for diagnosis at surgery of immobility of ovaries with endometriomas in the left ovary only were 44.4%, 92.3%, 44.4%, 92.3%, 5.8, 0.6, in the right ovary only were 50.0%, 98.5%, 80.0%, 94.2%, 33.0, 0.5 and bilaterally were 74.4%, 68.6%, 72.5%, 70.6%, 2.4, 0.4, while those for diagnosis of immobility of normal ovaries were 25.0%, 87.9%, 8.3%, 96.4%, 2.1, 0.9 for left ovary only, 14.3%, 92.9%, 7.1%, 96.6%, 2.0, 0.9 for right ovary only and 35.7%, 97.2%, 50.0%, 95.0%, 12.6, 0.7 bilaterally, respectively (P < 0.05 except for normal left and right ovaries with P = 0.2 and 0.4, respectively). The sensitivity, specificity, PPV and NPV for performance of ovarian immobility in the prediction of DIE for all women were 58.3%, 74.1%, 60.6%, 72.2% and in the prediction of need for bowel surgery were 78.2%, 71.1%, 41.3%, 92.6%, respectively. Conclusions There is a significant association between ovarian immobility and the presence of endometriomas. Ovarian immobility as a sonographic soft marker of DIE performs better in the presence of endometriomas compared with in normal ovaries. Copyright 2016 ISUOG. Published by John Wiley & Sons Ltd. INTRODUCTION Endometriosis is a common chronic disease that, classically, is characterized by the deposition of endometrial cells outside the uterine cavity. Lesions may vary in their appearance and location, ranging from the typical peritoneal implants, to ovarian endometrioma, to deep infiltrating endometriosis (DIE), which encompasses nodules involving organs in the pelvis, such as the vagina, uterosacral ligaments, bowel and bladder 1,2. Endometriosis can also result in distortion of pelvic anatomy. It may be asymptomatic or manifest as chronic pelvic pain, dyspareunia, urinary and/or bowel symptoms as well as infertility 3 5. Treatment options vary from medical management to laparoscopic excision or ablation of the endometriotic lesions 2,6 8. Correspondence to: Dr B. Gerges, Acute Gynaecology, Early Pregnancy and Advanced Endosurgery Unit, Nepean Hospital, Penrith, NSW 2750, Australia ( bgerges@gmail.com) Accepted: 5 June 2016 Copyright 2016 ISUOG. Published by John Wiley & Sons Ltd. ORIGINAL PAPER

2 794 Gerges et al. Laparoscopy remains the gold standard for the diagnosis of endometriosis 2 ; however, there are many preoperative imaging modalities that have been adopted in an attempt to diagnose accurately the presence and severity of endometriosis and, in particular, DIE. These include transvaginal sonography (TVS), rectal endoscopy-sonography, magnetic resonance imaging and computed tomography, of which TVS has been shown to be the most sensitive and specific in the diagnosis of DIE 9,10. Conventionally, ultrasound hard markers, such as endometriomas, hydrosalpinges and fibroids noted on imaging, are considered to correlate well with subsequent gold standard surgical confirmation However, despite the absence of an endometrioma, women are often positive for endometriosis on subsequent laparoscopy. To improve the detection of endometriosis, and superficial disease in particular, the concept of soft markers, including ovarian immobility and site-specific tenderness, were introduced in In that study, on the basis of traditional hard markers alone, TVS had a likelihood ratio of infinity (specificity, 100%) but also a high false-negative rate. In that series, conventionally, 80% (96/120) of the women would have had their scans classified as normal due to the absence of hard markers. However, 53% (51/96) of the women had an abnormal scan on the basis of soft-marker analysis, 73% (37/51) of whom had pelvic pathology at laparoscopy. The addition of soft markers (ovarian immobility, site-specific tenderness) improved the sensitivity of TVS in diagnosing peritoneal endometriosis from 34% to 87%, with a high negative predictive value (NPV) of 84%. Since these studies, tenderness-guided TVS has been used to detect DIE 16. Guerriero et al. 17 assessed the efficacy of TVS for the detection of pelvic adhesions and found a 12% possibility of pelvic adhesions in the absence of TVS features (namely, blurring of the ovarian margin) and clinical risk factors, which increased to 93% in the presence of TVS findings and three clinical risk factors. In a 2010 study, the pretest probability of pelvic adhesions increased from 74% to 96% when fixation to the uterus of at least one ovary was present and fell to 27% when this ultrasonographic finding was absent 18. Okaro et al. 15 showed that analysis of soft markers, including ovarian immobility, improved the detection of peritoneal disease in the absence of an endometrioma. This is useful but not entirely surprising as, clinically, the likelihood of disease and the need to excise endometriosis at the time of laparoscopy increases in the presence of ovarian immobility. This preoperative ultrasound information is important in the planning and counseling process. There are limited ultrasound data on the association between ovarian immobility in the presence of endometriomas as well as the predictive ability of ovarian immobility when comparing diseased and non-diseased ovaries. The aims of this study were to assess the association between ovarian immobility and the presence of endometriomas and to evaluate the accuracy of immobility on TVS in the presence and absence of endometriomas to diagnose DIE. METHODS This was a multicenter prospective observational study undertaken from January 2009 to March The women included in this study presented to the tertiary referral pelvic pain clinic with symptoms of chronic pelvic pain with or without a history of endometriosis, and all underwent TVS, followed by laparoscopy within the next 6 months. TVS was carried out at one of two centers, Nepean Hospital and OMNI Gynaecological Care, and laparoscopic surgery was performed at one of nine different hospitals: Nepean, Norwest Private, Royal Hospital for Women, Royal Prince Alfred, Hurstville Private, St. Luke s Private, Prince of Wales Private, Liverpool and St. George Private Hospitals. Ethics approval for this study was obtained from the Human Research Ethics Committee, Sydney West Area Health Service, Nepean campus, Penrith, Australia (HREC ). Data from the first 189 women included in the current study were also analyzed and published in a separate study, which described the use of sonovaginography for the prediction of posterior compartment DIE 19,20. A standardized history was obtained and clinical examination and preoperative TVS (7.5-MHz transvaginal probe and LOGIQ-e-I (GE Medical Systems, Zipf, Austria) or Medison X8, V20 or XG (Samsung Medison, Seoul, South Korea) ultrasound machines) was performed in all women prior to laparoscopy. During TVS, the uterus was first assessed for position, size and pathology, followed by assessment of the ovaries for size, mobility and pathology. Ovarian lesions, particularly endometriomas, were described using the terms outlined previously by the International Ovarian Tumour Analysis (IOTA) group 21. All TVS examinations were supervised by a single examiner, G.C., experienced in gynecological TVS, having performed in excess of scans. Ovarian mobility was assessed by applying the same technique as that for the sliding sign 22, by identifying the ovary in both midsagittal and transverse views and applying gentle abdominal palpation in the ipsilateral fossa. If the ovary was seen to glide smoothly against the uterus and/or pelvic side wall, this equated with a positive sliding sign and the ovary was classified as mobile. Conversely, if the ovary did not glide smoothly against the uterus and/or pelvic side wall then this equated with a negative sliding sign and the ovary was classified as immobile. Surgery was performed by one of 13 advanced laparoscopic surgeons or generalist gynecologists. The relationship between TVS ovarian mobility in the presence or absence of endometriomas was correlated with the gold standard, diagnosis of endometriosis at surgery. This diagnosis was made if any of the following criteria was satisfied: (1) histological confirmation of endometriosis in at least one resected subperitoneal nodule; (2) histological confirmation of an endometrioma following ovarian cystectomy; (3) visualization and palpation of a subperitoneal nodule without biopsy and another histologically proven location of endometriosis;

3 Ovarian mobility and endometriomas 795 (4) visualization of complete obliteration of the cul-de-sac. The surgical findings were reported by each surgeon in the form of detailed text and diagrams. The surgeons were not blinded to the TVS findings prior to surgery. The ultrasound and surgical data were entered into a Microsoft Excel 2010 spreadsheet after review of the TVS and operation reports. Data were analyzed to determine the association of ovarian endometrioma and ovarian immobility in five different sub-groups: right-only ovarian immobility and left-only ovarian immobility, in which the respective ovary was immobile while the contralateral ovary was mobile; both right and left ovarian immobility, in which both ovaries were immobile; right ovarian immobility and left ovarian immobility, in which the respective ovary was immobile in the presence of immobility in both ovaries, i.e. left-only ovarian immobility + both right and left ovarian immobility. Furthermore, ovarian immobility in the presence or absence of endometriomas was correlated with DIE identified at surgery. The locations of DIE included rectosigmoid, rectocervix, rectovagina, vagina and left and right uterosacral ligaments. The five groups were assessed in terms of accuracy, sensitivity, specificity, positive predictive value (PPV), NPV and positive (LR+) and negative (LR ) likelihood ratios. Diagnostic performance of TVS in the prediction of ovarian immobility at surgery for cases with and without ovarian endometriomas was analyzed using Fisher s exact test for associations between two variables and the kappa value for agreement between two variables. Comparison of TVS prediction of ovarian immobility in women with vs those without endometriomas was performed using chi-square test. RESULTS In total, 274 women were enrolled consecutively during the study period; the final analysis included 267 (97%) women with complete ultrasound and surgical data, two of whom had an oophorectomy. Their mean age was 31.5 ± 7.8 years and 146 (55%) women had a history of endometriosis. Endometriomas were found in 74 (27.7%) women. The advanced laparoscopic surgeons performed 91% (n = 243) of the 267 laparoscopic procedures in our study. Ovarian immobility on TVS was significantly associated with presence of endometriomas at surgery, with a prevalence of 12.2%, 10.8% and 52.7% for fixation of the left ovary only, the right ovary only and bilateral ovaries, respectively, in women with endometriomas, compared with 4.2%, 3.7% and 7.3%, respectively, in women with normal ovaries at surgery (Table 1). The number of cases, sensitivity, specificity, PPV, NPV, LR+ and LR for TVS diagnosis of ovarian immobility in women with endometriomas and in those with normal ovaries are outlined in Table 1. The comparison of TVS prediction of immobility of ovaries with endometriomas compared with that of normal ovaries is given in Table S1. There was a statistically significant association between immobility of ovaries and presence of endometriomas compared with normal ovaries at surgery (Table 2). The performance of ovarian immobility at TVS in the prediction of presence of DIE at surgery and need for bowel surgery in women with and those without endometriomas is summarized in Table 3. For all women, the performance of ovarian immobility to predict DIE had a sensitivity and specificity of 58.3% and 74.1%, respectively, and that to predict the need for bowel surgery was 78.2% and 71.1%, respectively (P < 0.05). DISCUSSION This study has shown that there is a significant association between ovarian immobility at TVS and the presence of endometriomas, particularly if both ovaries are immobile. Of the women in this study with bilateral ovarian immobility at TVS, 53% were found at surgery to have coexisting endometrioma(s). In addition, the PPV for ovarian immobility at TVS and ovarian fixation at surgery increased in the presence of unilateral/bilateral endometriomas, while, conversely, the NPV for ovarian immobility at TVS was higher for women with normal ovaries vs those with endometriomas. Furthermore, we assessed the ability of ovarian immobility alone on TVS to predict the presence of DIE, and in particular the need for bowel surgery, in women with and those without endometriomas. For prediction of the need for bowel surgery, the sensitivity was higher in women with endometriomas than it was in those without (90.6% vs 57.1%) but specificity was lower (40.5% vs 78.7%). However, the PPVs for the detection of DIE and need for bowel surgery were low. Also, given the population seen at our unit, and the fact that the pretest probability of women with DIE/bowel disease would be relatively high, this further emphasizes the fact that using ovarian immobility to detect DIE/need for bowel surgery is unreliable as a preoperative tool. There have been no previous studies assessing the soft marker sign of ovarian immobility with or without endometriomas to predict DIE or need for bowel surgery. The association between ovarian immobility and ovarian endometrioma is potentially due to the formation of adhesions between the diseased ovary and uterus, associated with endometriosis, which is consistent with the findings of Guerriero et al. 18. The preoperative TVS diagnosis of ovarian immobility is important, particularly in the presence of endometrioma, as it can alert the surgeon to the potential of advanced stage disease. This in turn would allow the surgeon to plan the operation appropriately, or refer the patient to an advanced laparoscopic unit. One of the limitations of our study is that we did not evaluate the association between ovarian immobility/ endometrioma and the site of fixation (i.e. fixation lateral to the pelvic sidewall vs medial to the uterus). Anecdotally, ovarian mobility with respect to the pelvic sidewall during TVS can be more difficult to interpret, whereas ovarian mobility/immobility with respect to the uterus can be demonstrated with confidence. There are no

4 796 Gerges et al. Table 1 Diagnostic performance of transvaginal sonography (TVS) in prediction of ovarian immobility at surgery, for cases with and those without ovarian endometrioma TP FP TN FN Accuracy Prev Sens Spec PPV NPV TVS feature (n) (n) (n) (n) (%) (%) (%) (%) (%) (%) LR+ LR P* Kappa Without ovarian endometrioma (n = 191) Left ovarian immobility Right ovarian immobility Left-only ovarian immobility Right-only ovarian immobility Both right and left ovarian immobility With ovarian endometrioma (n = 74) Left ovarian immobility Right ovarian immobility Left-only ovarian immobility Right-only ovarian immobility Both right and left ovarian immobility Discrepancy in numbers of cases for certain TVS features is due to missing data for two women who had undergone oophorectomy. Left/right-only ovarian immobility indicates ovarian immobility in presence of a mobile contralateral ovary. Left/right ovarian immobility indicates ovarian immobility in the presence of an immobile contralateral ovary, i.e. bilateral ovarian immobility. *Fisher s exact test for association between ovarian endometrioma at ultrasound and ovarian immobility at surgery. Kappa value for agreement between ovarian endometrioma at ultrasound and ovarian immobility at surgery. FN, false negative; FP, false positive; LR+, positive likelihood ratio; LR, negative likelihood ratio; NPV, negative predictive value; PPV, positive predictive value; Prev, prevalence; Sens, sensitivity; Spec, specificity; TN, true negative; TP, true positive. Table 2 Diagnostic performance of ovarian endometrioma at surgery in predicting ovarian immobility in 74 women with ovarian endometrioma Accuracy Prev Sens Spec PPV NPV Feature at surgery (%) (%) (%) (%) (%) (%) LR+ LR P* Kappa Left ovarian endometrioma E Right ovarian endometrioma E Left-only ovarian endometrioma E Right-only ovarian endometrioma E Both right and left ovarian endometrioma E Left/right-only ovarian endometrioma indicates ovarian endometrioma in the presence of a normal contralateral ovary. Left/right ovarian endometrioma indicates ovarian endometrioma in the presence of an endometrioma in the contralateral ovary. *Fisher s exact test for association between endometriomas and immobility at surgery. Kappa value for agreement between endometriomas and immobility at surgery. LR+, positive likelihood ratio; LR, negative likelihood ratio; NPV, negative predictive value; PPV, positive predictive value; Prev, prevalence; Sens, sensitivity; Spec, specificity. published data on lateral fixation to the pelvic sidewall; in the future, this may be a useful tool to assist with surgical planning (i.e. if the ovary is fixed to the pelvic sidewall at TVS, the need for pelvic sidewall dissection and ureterolysis will more likely be required). The association of ovarian immobility and endometriomas on ultrasound were variable in their statistical significance when only one ovary was affected. These results differ from those of Guerriero et al. 18, who found an increased pretest probability for pelvic adhesions of 89% when one ovary was fixed to the uterus and 30% with the fixation of both ovaries, whereas our study found a higher sensitivity for TVS prediction of ovarian immobility when both ovaries contained endometriomas compared with only one ovary with endometrioma (sensitivity, 74% and 44 50%, respectively). These findings may be a result of performance bias, as the sonographer may be more attuned to assessing immobility in the presence of endometriomas, given the disease potential, and may be more likely to assume, or even overlook assessment of, ovarian mobility when the ovaries appear normal. This limitation is difficult to overcome methodologically as the ovaries are assessed morphologically prior to assessment of mobility. In the absence of specialized ultrasound for prediction of obliteration of the pouch of Douglas (POD), TVS markers for endometriosis, such as ovarian fixation and ovarian endometrioma, may be useful in determining the risk of POD obliteration preoperatively. Ulukus et al. 23 published a study including 340 women with benign ovarian cysts to determine whether laterality of endometriomas was related to severity of endometriosis, and found that women with right-sided endometrioma had a significantly higher rate of POD obliteration than had women with left-sided endometrioma (21% vs 6%). In a recent study by our group, TVS markers such as ovarian fixation (unilateral/bilateral), ovarian endometrioma (unilateral/bilateral) and posterior compartment DIE were found to be significantly associated with POD obliteration at laparoscopy 20. However, when ovarian fixation and endometrioma were included in a mathematical model with the uterine sliding

5 Ovarian mobility and endometriomas 797 Table 3 Diagnostic performance of ovarian immobility at transvaginal sonography in prediction of deep infiltrating endometriosis (DIE) at surgery or need for bowel surgery in women without and those with endometrioma Accuracy Prev Sens Spec PPV NPV DIE at surgery (%) (%) (%) (%) (%) (%) LR+ LR P* Kappa All (n = 265) Any DIE < Rectosigmoid DIE < Rectocervical DIE < Rectovaginal DIE < Vaginal DIE Left USL DIE Right USL DIE Bowel surgery < Without endometrioma (n = 191) Any DIE Rectosigmoid DIE Rectocervical DIE Rectovaginal DIE Vaginal DIE Left USL DIE Right USL DIE Bowel surgery With endometrioma (n = 74) Any DIE Rectosigmoid DIE Rectocervical DIE Rectovaginal DIE Vaginal DIE Left USL DIE Right USL DIE Bowel surgery Two women who had undergone oophorectomy have been excluded. *Fisher s exact test for association between ovarian immobility at ultrasound and findings at surgery. Kappa value for agreement between ovarian immobility at ultrasound and findings at surgery. LR+, positive likelihood ratio; LR, negative likelihood ratio; NPV, negative predictive value; PPV, positive predictive value; Prev, prevalence; Sens, sensitivity; Spec, specificity; USL, uterosacral ligament. sign to predict POD obliteration, the sliding sign with addition of these features did not outperform the uterine sliding sign alone. Our current study confirms the strong association between ovarian immobility at TVS and the presence of ovarian endometrioma. The TVS finding of ovarian immobility and ovarian endometrioma should alert the clinician to the likelihood of advanced endometriotic disease, including an increased risk of POD obliteration and/or posterior compartment DIE (especially bowel DIE). In conclusion, there is a significant association between ovarian immobility and the presence of endometriomas when compared with normal ovaries. The performance of the sonographic soft marker, ovarian immobility, is better in the presence of endometriomas compared with in normal ovaries. Ovarian immobility alone, however, is not a good predictor of DIE. Future studies need to evaluate the repeatability and reproducibility of assessment of ovarian immobility as well the site of fixation in relation to the uterus and pelvic sidewall. ACKNOWLEDGMENTS We would like to thank Dr Ishwari Casikar, Dr Fernando Infante, Dr Uche Menakaya and Dr Batool Nadim for their contribution to the data collection. We would also like to thank the following laparoscopic surgeons for their contribution to this study: Jason Abbott, Dheya Al Mashat, Greg Cario, Michael Cooper, Qemer Khoshnow, David Kowalski and Geoffrey Reid. REFERENCES 1. Giudice LC. Clinical practice. Endometriosis. NEnglJMed2010; 362: Johnson NP, Hummelshoj L, World Endometriosis Society Montpellier Consortium. Consensus on current management of endometriosis. Hum Reprod 2013; 28: Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertil Steril 2012; 98: Berube 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: Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril 2008; 90: Vercellini P, Somigliana E, Consonni D, Frattaruolo MP, De Giorgi O, Fedele L. Surgical versus medical treatment for endometriosis-associated severe deep dyspareunia: I. Effect on pain during intercourse and patient satisfaction. Hum Reprod 2012; 27: Abbott J, Hawe J, Hunter D, Holmes M, Finn P, Garry R. Laparoscopic excision of endometriosis: a randomized, placebo-controlled trial. Fertil Steril 2004; 82: Marcoux S, Maheux R, Berube S. Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. N Engl J Med 1997; 337: Noventa M, Saccardi C, Litta P, Vitagliano A, D Antona D, Abdulrahim B, Duncan A, Alexander-Sefre F, Aldrich CJ, Quaranta M, Gizzo S. Ultrasound techniques in

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