Anatomical Sites and Characteristics of EndometriosisLesions: Laparoscopic Investigation

& Objective: Endometriosis is a common and benign disease of the female genital system, which is often seen in reproductive age and leads to infertility, dysmenorrhea, and dyspareunia. The aim of this study is to investigate the anatomical location and characteristics of endometriosis lesions in laparoscopic surgery.

& Methods: In this cross-sectional study, 557 endometriosis patients who referred to the gynecology department of Shohadaye-Tajrish Hospital and underwent laparoscopic surgery during 2016-2021 were evaluated. Statistical analysis of data was done using SPSS software version 24.P-value less than 0.05 was considered statistically significant level.

The results of this study show that the highest anatomical distribution of endometriosis lesions was ovarian endometriosis, and the lowest was vagina. Also, the highest rate of surface lesions is uterus and bladder, and the lowest is superficial lesions of the cul-de-sac cyst.

Our results demonstrate that the distribution of endometriosis lesions is asymmetric.

Endometriosis, Laparoscopy, Anatomical Site, Lesion Distribution Characteristics types of Endometriosis Lesions Received: 2023/02/03; Accepted: 2023/07/02; Published Online: 09 Sep 2023; Use your device to scan and read the article online Corresponding Information: Nazli Najeddin Choukan, Department of Obstetrics and Gynecology, Shahid Beheshti University of Medical Sciences, Tehran, Iran Email: [email protected] Copyright © 2023, This is an original open-access article distributed under the terms of the Creative Commons Attribution-noncommercial 4.0 International License which permits copy and redistribution of the material just in noncommercial usages with proper citation.

Endometriosis refers to the presence and growth of uterine tissue outside the uterine cavity, which is a chronic and complex disease that affects women of reproductive age (1 -4). Endometriosis is related to infertility and chronic pelvic pain during the menstrual cycle and dyspareunia (3-8). About 176 million women suffer from endometriosis (3, 9, 10). The approximate prevalence of endometriosis in the Tehran province in 2013 was reported about 5- 20% (3). Endometriosis significantly affects the quality of life (Qol) of females and their families, and burden of disease is the same as other chronic diseases (3, 11-14). One of the causes of infertility is endometriosis that affects about 25-50% of infertile women (5, 6, 15). The cause and pathophysiology of endometriosis are unknown, however genetic and environmental factors may be involved (1, 16- 18).In order to check the location, number, measurement and severity of endometriosis involvement, a detailed laparoscopy evaluation is needed to consider the appropri ate treatment method depending on the severity and location of the disease (3, 7).The purpose of this study was to investigate the sites and characteristics of endometriosis lesions in laparoscopic surgery in patients referred to Shohadaye- Tajrish Hospital.

Patients and study design This cross -sectional study was performed on endometriosis patients that referred to the gynecology department at Shohadaye-Tajrish Hospital as a referral center in Tehran, Iran, between April2016 and April 2022. Patien ts with endometriosis that underwent laparoscopic surgery enrolled in this study. The sampling method was convenient and according to the 495 Characteristics of Endometriosis Lesions Volume 8, September – October 2023 Journal of Obstetrics, Gynecology and Cancer Research following statistical formula, the sample size calculated 557 patients. N= [P (1-P)] × (Z 1-α/2) ² d² Inclusion criteria in this study were: age at least 18 years, diagnosis of endometriosis and laparoscopic surgery. Information was collected based on a checklist. Also, for each surgery, laparoscopic videos of the patients were observed and evaluated, and the anatomical location of endometriosis was determined using the detailed examination of these videos. Demographic factors (age, weight, height), location of endometriosis lesion, type of lesion (superficial lesion, endometrioma, DIE), pelvic adhesion and laterality of endometriosis were investigated in these people. The ethics was approved by the ethical committee of Shahid Beheshti University of medical sciences (approval number IR.SBMU.RETECH.REC.1401.685). Statistical analysis Statistical analysis of the data was done using (spss software, version 24, IBM, USA). Statistical analysis of data was done using T-test for quantitative variables and square test for qualitative variables. A P-value less than 0.05 was considered statistically significant.

Finally, 557 patients enrolled in this study and 66.7 % of women them were married. The average age of patients was 33.35 ±7.51 years (min:18 and max:49) and the average body mass index (BMI) was 25.48 ±4.35. Fifteen patients (3.7%) had family history o f endometriosis. Table 1 shows descriptive characteristics of lesions. Table 1. Descriptive characteristics of lesions Minimum Maximum Mean Std. Deviation Superficial and deep lesions Deep Peritoneal lesions 10 60 34.62 12.052 Superficial Peritoneal lesions 20 70 33.33 19.664 Deep right ovarian lesions 10 10 10.00 - Deep left ovarian lesions 10 10 10.00 - Superficial right ovarian lesions 10 30 20.00 8.165 Superficial left ovarian lesions 10 30 17.78 6.667 Ovarian adhesions Left (Dense) 10 30 18.33 7.528 Left (Filmy) 10 20 16.67 5.774 Right (Dense) 10 30 17.86 6.986 Right (Filmy) 20 20 20.00 0.000 Endometrioma size Left endometrioma size 10 150 60.19 33.107 Right endometrioma size 20 150 57.78 36.064 Out of 557 patients, 82 (14.7%) had pelvic adhesions. Table 2 shows the prevalence of lesions in patients. Among the patients who had pelvic adhesions, 46.3% (n = 38) they had no history of pelvic infection, while 53.6% (n = 44) had a history of pelvic infection, which according to chi -square test, there was no stat istically significant difference ( P-value=0.79). Table 3 shows surgeries history for the patients under study. Table 2. Prevalence of lesions in patients Frequency Percent Deep lesions Endometrioma 408 73.2 Left uterosacral 294 52.8 Right uterosacral 245 44.0 Behnaz Nouri et al. 496 Volume 8, September – October 2023 Journal of Obstetrics, Gynecology and Cancer Research Frequency Percent Rectum 158 28.4 Bladder 93 16.7 Left pelvic wall 43 7.7 Right pelvic wall 43 7.7 Right ureter 38 6.8 Left ureter 16 2.9 Sigmoid 38 6.8 Diaphragm 27 4.8 Parametrium 27 4.8 cul-de-sac 21 3.8 Vagina 6 1.1 Superficial lesions Uterine 49 8.8 Bladder 49 8.8 Cul-de-sac 6 1.1 8.8 Endometriosis adhesions No 491 88.2 Yes 66 11.8 Müllerian duct anomalies No 508 91.2 Yes 49 8.8 Myoma No 86 84.3 Subserous 16 15.7 Non-endometrioma cysts No 536 96.2 Yes 21 3.8 Stage of endometriosis Stage 1 26 4.7 Stage 2 38 6.8 Stage 3 67 12.0 Stage 4 426 76.5 Table 3. Surgeries history for the patients under study Surgeries Left side Right side Both side Oophorectomy 55 (9.9) 33(5.9) 71(12.7) Cystectomy 98 (17.6) 120 (21.5) 120 (21.5) Reconstructed ovary 13(2.3) 6(1.1) 22 (3.9) Fallopian tube occlusion 16 (2.9) 32 (5.7) 13(2.3) Salpingectomy 59 (10.6) 22(3.9) 55 (9.9) 497 Characteristics of Endometriosis Lesions Volume 8, September – October 2023 Journal of Obstetrics, Gynecology and Cancer Research The relationship between the average age and BMI of the patients and the location of the lesion is shown in Table 4. Independent t test shows there was a statistically significant difference in left uterosacral site and left pelvic wall with age of patients. The independent t -test showed a significant difference between BMI and pelvic wall, ureter, uterosacral and endometrioma lesions. Table 4. The relationship between the age and BMI of patients and location of lesions Location of lesions Yes No P-value Mean + SD Age Mean + SD Age Uterine wall 37.67 + 7.81 32.94 + 7.4 0.071 Ureter 35.43 + 7.23 33.2 + 7.55 0.452 Uterosacrals 34.12 + 7.9 32.34 + 6.94 0.238 Endometrioma 32.75 + 6.69 35.04 + 9.4 0.176 Left Uterosacral 34.85+7.61 31.67+7.12 0.032 Right Uterosacral 33.44+7.67 33.28+7.46 0.914 Rectum 33.48 + 7.58 3.30 + 7.54 0.913 Bladder 32.76+8.98 33.47+7.25 0.726 Left uterine wall 38.5+7.91 32.91+7.36 0.043 Right uterine wall 37.13+8.17 33.03+7.42 0.140 Left ureter 32.67+6.66 33.37+7.57 0.873 Right ureter 35.43+7.23 33.2+7.55 0.452 Sigmoid 33.14+9.28 33.37+7.43 0.939 Parametrium 28.8+4.02 33.59+7.59 0.166 Location of lesions Mean + SD BMI Mean + SD BMI P-value Uterine wall 25.31 + 2.46 25.49 + 4.49 0.910 Ureter 24.69 + 3.63 25.54 + 4.42 0.620 Uterosacrals 25.48 + 4.96 25.48 + 3.44 0.998 Endometrioma 25.71 + 4.54 24.86 + 3.82 0.390 Left Uterosacral 25.81+4.91 25.1+3.64 0.421 Right Uterosacral 25.42+5.31 25.53+3.47 0.906 Rectum 26.70 + 5.71 25.01 + 3.65 0.082 Bladder 24.5+3.95 25.68+4.43 0.309 Left uterine wall 25.27+2.66 25.5+4.47 0.896 Right uterine wall 25.07+2.56 25.51+4.47 0.798 Left ureter 26.47+3.72 25.45+4.39 0.693

In a study by Audebert et al. it was shown that the highest prevalence of endometriosis was in the ovary, uterosacral ligament, ovarian cavity, posterior cul -de- sac, and bladder, respectively). Also, the most common site of endometriosis was on the left side of the pelvis. The results of this study showed that the most adhesion is in the adnexa of patients. In this survey, average age of the patients was 33.6 years and average BMI of the Behnaz Nouri et al. 498 Volume 8, September – October 2023 Journal of Obstetrics, Gynecology and Cancer Research patients was 21.5 kg/m 2. Also, the most common site of involvement of deep endometriosis was reported in the ureter in 159 patients (14.4%) (19). In another study shown by Ajani et al. (2019), the average age of the patients was 35 years, and the most common site of endometriosi s lesions was the ovary (bilateral in 28.8% of cases) and fallopian tubes (20) . Also, in a study conducted by Yasui and et al., (2015), they examined 210 patients who underwent surgery. It was shown that the prevalence site of endometriosis was ovary, peri toneum, rectum and bladder, respectively (21). Also, in a study by Jenkins et al. (2008), it was shown that ovarian and posterior broad ligament lesions were more common and anterior cul -de-sac lesions were significantly more than posterior cul-de-sac lesions (22). In the study of Kadivar et al. in 2013, it was shown that the frequency of extrapelvic endometriosis was 48 cases (14.8%) and 40 cases of abdominal wall endometriosis. Also, abdominal wall endometriosis was observed in 12.3% of endometriosis cases (23). In this study, the frequency of endometriosis was 11.7%cases in the cesarean scar. Also, the results showed that the history of cesarean delivery in patients with abdominal wall endometriosis was more than in other patients with endometriosis (23) . In a study conducted by Lee.), it was shown that the prevalence of endometriosis in the ovary was (96.4%) (24).

Based on our finding and some other studies, demonstrate that the distribution of endometriosis lesions is asymmetric. The results of this study show that the anatomical distribution of endometrioma lesions in this study has the highest percentage related to ovarian endometrioma and the lowest percentage related to vagina. Most of the anatomical distribution after ovarian endometrioma is related to the left uterosacral, right uterosacral, rectum, bladder, uterus and appendix. Also, the highest rate of surface lesions is related to the uterus and bladder, and the lowest is related to the superficial lesions of the cul-de-sac. Acknowledgments We sincerely thank the women who participated in the present study. We are also grateful to Deputy for Research of Shahid Beheshti University of Medical Sciences who supported us in this project. Authors' Contribution All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Concept and design: BN, MA and NNC. Drafting of the manuscript: NNC, MA and BN. Critical revision of the manuscript for important inte llectual content: All authors. Statistical analysis: NNC. Supervision: BN. Funding/Support The author(s) received no financial support for the research, authorship, and/or publication of this article. Conflict of Interest The authors certify that they have no affiliations with or involvement in any organization or entity with any financial or non-financial interest in the subject matter or materials discussed in the manuscript. 1. Zondervan KT, Becker CM, Koga K, Missmer SA, Taylor RN, Viganò P. Endometriosis. Nat Rev Dis Primers. 2018;4(1):9. [DOI:10.1038/s41572-018-0008-5] [PMID] 2. Dahaghin S, Hosseini Doust R, Mirnejad R. Molecular Detection of Ureaplasma urealyticum and Chlamydia trachomatis in Women with Endometriosis. Iran J Med Microbiol. 2019;13 (2):125-31. [DOI:10.30699/ijmm.13.2.125] 3. Naji Omidi F, Abolghasemi J, Chaichian S, Rimaz S, Najmi Z, Mehdizadehkashi A. Evaluation of the factors influencing endometriosis in reproductive age women. Med Sci J Islamic Azad Univ. 2016;26(3):188-94. 4. Hoorsan H, Mirmiran P, Chaichian S, Moradi Y, Akhlaghdoust M, Hoorsan R, et al. Diet and Risk of Endometriosis: A Systematic Review and Meta-Analysis Study. Iran Red Crescent Med J. 2017;19(9): e41248. [DOI:10.5812/ircmj.41248] 5. Moazzami B, Chaichian S, Samie S, Zolbin MM, Jesmi F, Akhlaghdoust M, et al. Does endometriosis increase susceptibility to COVID - 19 infections? A case-control study in women of reproductive age. BMC Women's Health. 2021; 21(1):1-7. [PMID] [PMCID] [DOI:10.1186/s12905-021-01270-z] 6. Sarbazi F, Akbari E, Karimi A, Nouri B, Noori Ardebili SH. The Clinical Outcome of Laparoscopic Surgery for Endometriosis on Pain, Ovarian Reserve, and Cancer Antigen 125 (CA - 125): A Cohort Study. Int J Fertil Steril. 2021; 15(4):275-9.

499 Characteristics of Endometriosis Lesions Volume 8, September – October 2023 Journal of Obstetrics, Gynecology and Cancer Research 7. Hoorsan H, Alavi Majd H, Chaichian S, Mehdizadehkashi A, Hoorsan R, Akhlaqghdoust M, et al. Maternal Anthropometric Characteristics and Adverse Pregnancy Outcomes in Iranian Women: A Confirmation Analysis. Arch Iran Med. 2018;21(2):61-6. 8. Sarbazi F, Akbari E, Nouri B. Pain Management in Endometriosis. Interv Pain Med Neuromod. 2022;2(1):e128043. [ DOI:10.5812/ipmn- 128043] 9. Nouri B, Roshandel S. Is Artificial Intelligence a New Diagnos tic Approach for Patients with Endometriosis? Interv Pain Med Neuromod. 2022;2(1):e128720. [ DOI:10.5812/ipmn- 128720] 10. Nouri B, Arab M, nasiri m. Endometriosis: Clinical, Magnetic Resonance Imag ing and Pathologic Findings. J Obstet Gynecol Cancer Res. 2022(14):61. 11. Davoodi P, J. Ghadimi D, Rezaei M, Khazei Tabari MA, Shirani A, Nouri B, et al. Endometriosis and COVID -19: Clinical Presentation and Quality of Life, a Systematic Review. J Obstet Gyne col Cancer Res. 2023; 8(4):314-25. 12. Morgan-Ortiz F, López -de la Torre MA, López- Zepeda MA, Morgan -Ruiz FV, Ortiz -Bojórquez JC, Bolívar -Rodríguez MA. Clinical characteristics and location of lesions in patients with deep infiltrating endometriosis using the revised Enzian classification. J Turk Ger Gynecol Assoc. 2019;20(3):133-7. [PMID] [PMCID] [DOI:10.4274/jtgga.galenos.2018.2018.0120] 13. Angioni S, Nappi L, Sorrentino F, Peiretti M, Daniilidis A, Pontis A, et al. Laparoscopic treatment of deep endometriosis with a diode laser: our experience. Arch Gynecol Obstet. 2021;304(5):1221-31. [PMID] [PMCID] [DOI:10.1007/s00404-021-06154-z] 14. Agarwal SK, Chapron C, Giudice LC, Laufer MR, Leyland N, Missmer SA, et al. Clinical diagnosis of endometriosis: a call to action. Am J Obstet Gynecol. 2019;220(4):354-e1-12. [DOI:10.1016/j.ajog.2018.12.039] [PMID] 15. Gui B, Valentini AL, Ninivaggi V, Marino M, Iacobucci M, Bonomo L. Deep pelvic endometriosis: don't forget round ligaments. Review of anatomy, clinical characteristics, and MR imaging fea tures. Abdom Imaging. 2014; 39(3):622-32. [PMID] [DOI:10.1007/s00261- 014-0091-3] 16. 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. 2008;15(1):32-7. [DOI:10.1016/j.jmig.2007.08.619] [PMID] 17. Foti PV, Farina R, Palmucci S, Vizzini IAA, Libertini N, Coronella M, et al. Endometriosis: clinical features, MR ima ging findings and pathologic correlation. Insights into Imaging. 2018;9(2):149-72. [PMID] [PMCID] [DOI:10.1007/s13244-017-0591-0] 18. Di Giovanni A, Casarella L, Coppola M, Falcone F, Iuzzolino D, Rasile M, et al. Ultrasound Evaluation of Retrocervical and Parametrial Deep Endometriosis on the Basis of Surgical Anatomic Landmarks. J Minim Invasive Gynecol. 2022;29(10):1140-8. [DOI:10.1016/j.jmig.2022.06.014] [PMID] 19. 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. [DOI:10.1016/j.ejogrb.2018.09.001] [PMID] 20. Ajani MA, Salami A, Nwanji ID, Olusanya AA, Fatunla OE. Distribution and Characteristics of Endometriotic Lesions in South -Western Nigeria: A Single Institutional Experience. Med J Zamb. 2019;46(1):28-32. [DOI:10.55320/mjz.46.1.227] 21. Yasui T, Hayashi K, Nagai K, Mizunuma H, Kubota T, Lee J -S, et al. Risk Profiles for Endometriosis in Japanese Women: Results From a Repeated Survey of Self -Reports. J Epidemiol. 2015;25(3):194-203. [PMID] [PMCID] [DOI:10.2188/jea.JE20140124] 22. Jenkins TR, Liu CY, White J. Does Response to Hormonal Therapy Predict Pr esence or Absence of Endometriosis? J Minim Invasive Gynecol. 2008;15(1):82-6. [DOI:10.1016/j.jmig.2007.09.002] [PMID] 23. Kadivar M, Vafa A, Farahzadi A, Khani S. 6 years evaluation of prevalence of abdominal wall endometriosis in patients with definite histopathological diagnosis of endometriosis admitted in Rasool -Akram, Shariati and Atieh Hospitals in Tehran. Razi J Med Sci. 2012; 18(93):20-6. 24. Lee SY, Koo YJ, Lee DH. Classification of endometriosis. Yeungnam Univ J Med. 2021; 38(1):10-8. [ DOI:10.12701/yujm.2020.00444] [PMID] Behnaz Nouri et al. 500 Volume 8, September – October 2023 Journal of Obstetrics, Gynecology and Cancer Research How to Cite This Article: Nouri, B., Arab, M., Najeddin Choukan, N. Anatomical Sites and Characteristics of EndometriosisLesions: Laparoscopic Investigation. J Obstet Gynecol Cancer Res. 2023; 8(5):494-500. Download citation: RIS | EndNote | Mendeley |BibTeX |