{"paper_id":"fab33c54-f1d5-4aa0-a01c-d63676d78d63","body_text":"Atwa et al. Middle East Fertility Society Journal           (2023) 28:21  \nhttps://doi.org/10.1186/s43043-023-00146-6\nRESEARCH Open Access\n© The Author(s) 2023. Open Access  This article is licensed under a Creative Commons Attribution 4.0 International License, which \npermits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the \noriginal author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or \nother third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line \nto the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory \nregulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this \nlicence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.\nMiddle East Fertility\nSociety Journal\nFactors associated with recurrent \nendometriomas after surgical excision\nKhaled A. Atwa1, Zakia M. Ibrahim1, Eman M. El Bassuony1 and Omima T. Taha1*   \nAbstract \nBackground Endometriosis affects women in reproductive age and causes a great impact on their lives. When \naffecting the ovary, excision represents the main management option. However, recurrence represents a challenging \nsituation for patients and physicians. This study aimed to determine factors contributing to endometriomas recur-\nrence after surgical excision.\nResults This was a quasi-experimental study recruiting 60 patients with ovarian endometrioma. The mean age \nwas 30.33 ± 7.95 years. The mean parity was 1.27 ± 0.69. The recurrence rate after excision was 11/60 (18.3%) \nafter a mean follow-up period of 22.62 ± 4.96 months. None of the patients’ characteristics or endometriosis-related \ncharacteristics were significant factors contributing to cyst recurrence (age, parity, history of infertility, preopera-\ntive endometrioma diameter, preoperative AFC, preoperative AMH, degree of pelvic pain, degree of dysmenorrhea, \ndegree of dyspareunia, pelvic tenderness, and induration) (p value > 0.05).\nConclusion The patient’s related factors and endometrioma characteristics did not predict its recurrence.\nKeywords Endometrioma, Recurrence, Prediction\nBackground\nEndometriosis is a gynecological condition which affects \nwomen of reproductive age, causing infertility, dysmen -\norrhea, and dyspareunia [1]. Surgical excision is the prin -\ncipal treatment, as medical options are of limited efficacy. \nAlthough effective, surgery is associated with multiple \ncomplications, with recurrence representing a challeng -\ning one reaching 40–45% after 5  years [2] and reopera -\ntion rates of 27% [3]. Additionally, fertility decline was \nnoted to be more prominent after further interventions \nrather than after primary surgery [4]. This makes endo -\nmetriosis a dreadful disease, and concerns about avoiding \nrecurrence are paramount [5]. Several studies evaluated \nthe role of adjuvant therapies in preventing recurrence as \nhormonal treatments [6]. Variable results were reported \nwith a predilection toward the insignificant impact of \nhormonal treatment in preventing recurrence [7, 8]. \nDetermining possible factors associated with recurrent \nendometriomas would influence treatment decisions and \noptimize treatment planes [9]. Accordingly, this study \nevaluated factors affecting endometrioma recurrence \nafter laparoscopic excision.\nMethods\nThis quasi-experimental study was conducted in the \nObstetrics and Gynecology Department at Suez Canal \nUniversity Hospital from November 1, 2020, to July 31, \n2022. We recruited eligible patients during the study \nduration according to prespecified inclusion and exclu -\nsion criteria. Inclusion criteria: (a) unilateral endome -\ntrioma, (b) unilocular endometrioma 3–8 cm, (c) age \n18–45 years, (d) regular cycles, (e) no previous history \nof ovarian operations, and (f) patients undergoing surgi -\ncal excision of the endometrioma by laparoscopy. Exclu -\nsion criteria: (a) suspected or confirmed malignancy, \n(b) women within 2 years of menarche, (c) women on \n*Correspondence:\nOmima T. Taha\nomimatharwat@yahoo.com\n1 Department of Obstetrics and Gynecology, Faculty of Medicine, Suez \nCanal University, Ismailia, Egypt\n\nPage 2 of 5Atwa et al. Middle East Fertility Society Journal           (2023) 28:21 \nprogesterone only or combined hormonal contracep -\ntion, (d) women refusing to participate in the study, and \n(f) women preferring medication for the management of \nendometriomas.\nInformed consent was obtained from all eligible study \nparticipants after adequately explaining the study pro -\ncedures and aim. Eligible patients were subjected to the \nfollowing:\n1- Complete personal and medical history. Data about \npelvic pain, dysmenorrhea, and dyspareunia were \nobtained and graded as mild, moderate, or severe.\n2- The local gynecological examination, performed by \nthe same researcher, focused on evaluating pelvic \ntenderness and induration and was graded into mild, \nmoderate, or severe.\n3- Ultrasound examination to diagnose ovarian endo -\nmetrioma and measure its diameter [10]. The antral \nfollicle count (AFC) of the affected ovary was evalu -\nated on days 2–3 of the cycle by determining the \nnumber of follicles measuring 2–10 mm [11].\n4- Routine preoperative laboratory investigations such \nas complete blood count, coagulation profile, liver \nfunction test, and anti-mullerian hormone (AMH) \nwere withdrawn.\n5- Patients were prepared for laparoscopic cystectomy. \nAny adhesions were lysed to free the ovary before \nexcision. An incision in the endometrioma was done. \nSuction of the endometrioma contents was done. \nStripping of the cyst wall from the ovarian tissue was \ndone. Handling of the ovary was done using atrau -\nmatic grasping forceps. Bipolar cauterization was \nused to achieve hemostasis using pinpoint coagula -\ntions to avoid thermal damage to the ovary. Com -\nplete removal of the cyst wall was ensured [12]. No \nhormonal treatment was offered after the operation.\n6- Initial follow-up visit was after 3 months. However, \nlonger duration of follow-up was recommended to \nevaluate recurrences properly. Accordingly, further \nfollow-up was done after at least 1 year of the opera -\ntion. Recurrence was defined as cyst diameter > 10 \nmm [5].\nStatistical analysis\nData were statistically described as mean and stand -\nard deviation, frequencies (number of cases), and per -\ncentages when appropriate. P  value of less than 0.05 \nwere considered statistically significant. All statistical \ncalculations were done using the computer program \nSPSS (Statistical Package for the Social Science; SPSS \nInc., Chicago, IL, USA), release 23 for Microsoft Win -\ndows. Comparison between patients with recurrent \nendometriosis and those without was done by the stu -\ndent T test. Multivariate and univariate regression \nanalysis was performed to determine possible factors \nassociated with cyst recurrence.\nResults\nSixty patients were recruited throughout the study dura -\ntion. The mean age was 30.33 ± 7.95  years. The study \npopulation was either virgins or married/divorced/wid -\nowed equally. The mean parity of the married/divorced/\nwidowed patients was 1.27 ± 0.69. The mean follow-up \nperiod was 22.62 ± 4.96 months (Table 1).\nThe recurrence rate after excision was 11/60 (18.3%). \nThe mean endometrioma size after recurrence was \n3.27 ± 0.17. There was no significant difference in the \novarian reserve either before or after surgery as repre -\nsented by AMH and AFC levels between patients who \nhad recurrent endometriosis and those who did not \n(P value > 0.05) (Table  2). There was no significant dif -\nference in the extend of dysmenorrhea between both \ngroups (p value 0.575).\nNone of the patients’ characteristics or endometriosis-\nrelated characteristics were significant factors contribut -\ning to cyst recurrence by multivariate analysis (age, parity, \nhistory of infertility, preoperative endometrioma diameter, \npreoperative AFC, preoperative AMH, degree of pelvic \npain, degree of dysmenorrhea, degree of dyspareunia, pel-\nvic tenderness, and induration) (p value > 0.05) (Table 3).\nDiscussion\nAfter surgical excision, recurrence was noted in 18.3% \nof the participants. The recurrence rate after endome -\ntrioma excision was reported to be high. It ranged from \n29 to 56% after 2  years, while after 5  years, it was 43% \n[13] without postoperative medical treatment. Another \nstudy reported a recurrence rate of 6.4%. This study \nconducted follow-up visits every 3  months of surgery, \nand the results were reported after a mean follow-up \nperiod of 22.62 ± 4.96 months, while they reported their \nTable 1 Basic demographic data of the studied population \n(N = 60)\nAge (years) (mean ± SD) 30.33 ± 7.95\nOccupation\nN (%)\nNot working 29 (48.33%)\nWorking 31 (51.67%)\nResidence\nN (%)\nUrban 28 (46.67%)\nRural 32 (53.33%)\nMarital status\nN (%)\nVirgin 30 (50%)\nMarried/divorced/\nwidowed\n30 (50%)\nParity (mean ± SD) 1.27 ± 0.69\nMean follow-up period (months) (mean ± SD) 22.62 ± 4.96\n\nPage 3 of 5\nAtwa et al. Middle East Fertility Society Journal           (2023) 28:21 \n \nresults after 5  years. A large number of their partici -\npants received postoperative hormonal treatment in the \nform of oral contraceptives, Mirena for at least 1  year, \nGonadotropin releasing hormone analogs (GnRHa) for \n3–6  months, or GnRHa followed by Mirena. Only 3.4% \nof their studied population did not receive any hormonal \ntreatment which might impact the recurrence rates after \nsurgery [14]. Hormonal treatment leads to apoptosis of \nthe ectopic endometrial implants either in the pelvis or \nde novo implants leading to decreased recurrences [15]. \nThe current study provided no medical treatment after \nsurgery. Immune cells and extracellular matrix metallo -\nproteinase lead to the proliferation and survival of endo -\nmetriotic cells, explaining recurrent endometriosis [16].\nRecurrent endometriosis differed in its rate between \nstudies. This was rendered to the variable factors con -\ntributing to its recurrence as the definition of recurrence \ndepended on subjective pain sensation or clinical and radi-\nological evaluation. Also, the type of endometriosis, disease \nseverity, method of excision, surgical skills, and time to \nrecurrence was reported [5]. The evaluation of recurrence \ndepending on symptoms was higher than the sonographic \nevaluation, with a poor correlation between pain and actual \nrecurrence [17]—the current study evaluated recurrence \nusing ultrasound after 3 months of excision.\nThere was no difference in the endometrioma size \nbefore surgery among women with recurrent endome -\ntriosis and those without. Also, there was no difference \nin age, parity, extend of dysmenorrhea, and the ovarian \nreserve before and after surgery among both groups. This \nwas evident in an earlier study where there was no differ -\nence in patients’ age, parity, and BMI among those with \nrecurrent endometriosis and those without. However, \nthe extent of dysmenorrhea was increased significantly \namong those with recurrent endometriosis (p value \n0.001) [14]. This difference would be related to the pres -\nence of concomitant conditions as adenomyosis which \nwas not evaluated in our study population. it has been \nreported that dysmenorrhea was evident in women with \nadenomyosis due to associated deeply situated dense \nendometrial glands in the myometrium [18].\nThe current study demonstrated no significant risk fac-\ntor associated with cyst recurrence. Another study done \nby Koga et al. 2006 demonstrated that previous history \nof medical treatment and endometrioma size predicted \nrecurrence significantly [19]. An earlier study reported \nthat younger age at surgery was associated with recur -\nrent endometriosis. This was rendered to the increased \nestrogen concentration in younger women leading \nto preoperative hormonal treatment which results in \natrophy and reduced size of the endometriotic lesions \nleading to missed removal in surgery [20]. It has been \nreported that risk factors contributing to endometrio -\nsis recurrence were heterogeneous among studies. The \nstage of endometriosis, adhesions, and size and num -\nber of endometrioma did not influence recurrence while \nprevious surgery was significantly associated with recur -\nrence. This was explained by the progressive and aggres -\nsive nature of the disease [21]. Another study concluded \nTable 2 Ovarian reserve and endometrioma size between patients with recurrent endometriomas and those without\nRecurrent endometrioma\n11/60 (18.3%)\nNo recurrence\n49/60 (81.7%)\nP value\nAge 33.5 ± 6.9 29.6 ± 8.04 0.139\nParity 1.5 ± 0.6 1.2 ± 0.7 0.244\nPreoperative endometrioma diameter 5.9 ± 1.6 5.3 ± 1.76 0.354\nPostoperative endometrioma diameter 3.27 ± 0.17 0.07 ± 0.53 0.0001\nPreoperative AFC 5.9 ± 1.6 5.2 ± 2.2 0.809\nPostoperative AFC 3.9 ± 1.4 3.3 ± 1.7 0.469\nPreoperative AMH 1.76 ± 0.4 1.8 ± 0.4 0.843\nPostoperative AMH 1.5 ± 0.44 1.5 ± 0.43 0.649\nTable 3 Multivariate analysis for the factors affecting recurrent \nendometriomas after laparoscopic excision\nBeta 95% confidence \ninterval\nP value\nConstant  − 0.108  − 2.328–2.113 0.920\nAge 0.008  − 0.027–0.044 0.626\nParity 0.070  − 0.297–0.436 0.694\nInfertility  − 0.221  − 0.662–0.221 0.307\nEndometrioma  \ndiameter\n0.003  − 0.137–0.143 0.961\nAFC (preoperative)  − 0.013  − 0.131–0.106 0.822\nAMH (preoperative) 0.086  − 0.462–0.633 0.745\nDegree of pain 0.122  − 0.181–0.426 0.408\nDegree of  \ndysmenorrhea\n0.105  − 0.256–0.466 0.546\nDegree of dyspareunia  − 0.029  − 0.284–0.227 0.815\nPelvic tenderness  − 0.136  − 0.431–0.160 0.347\nInduration  − 0.054  − 0.351–0.243 0.706\n\nPage 4 of 5Atwa et al. Middle East Fertility Society Journal           (2023) 28:21 \nthat dysmenorrhea and ovarian cyst separations were \nassociated with endometrioma recurrence [22]. Dys -\nmenorrhea was rendered to the disease itself as a result \nof bleeding from focal endometriotic implants, release of \ninflammatory mediators, and direct irritation of the pel -\nvic nerves and peritoneum [22]. While Selcuk et al. men -\ntioned that deeply penetrating endometrial tissue in the \novary was significantly associated with recurrent endo -\nmetrioma [23]. This was explained by decreased apop -\ntosis and increased proliferation with deeply infiltrated \nendometriosis [22].\nOther mechanical factors explaining recurrent endome-\ntriosis were regrowth of endometriotic lesions from resid-\nual loci [24], which was emphasized by the reappearance \nof endometriotic lesions at the same site after excision [25]. \nThe use of laser ablation results in prevention of recurrence \nfor at least 2  years, which elaborates the role of abnormal \nuterine contraction in the generation of ectopic endometrial \nimplants [26, 27]. Lymph node involvement has also been \nreported as a possible cause of recurrence [28]. Immuno -\nlogical factors contribute to endometriotic spots’ de novo \nor in  situ regeneration. It has been reported that CD-16 \nexpressing natural killer cells are abundant in the peritoneal \nfluid and blood of women with endometriosis and are not \naffected by surgical excision or hormonal therapy [29].\nVariable results were rendered to multiple factors, includ-\ning different surgical procedures adopted, different surgical \nexperiences, different outcome measures, different types \nand stages of endometriosis between studies, different target \npopulations, and the evaluation duration. Also, a possible \nbias in selection and recruitment, recall and data reporting, \nand inaccurate statistical analysis would contribute to the \ncontradictory results. Incomplete removal of endometrio-\nmas because of extensive pelvic adhesions contributed to \nendometrioma recurrence. Additionally, different method-\nologies and power between studies are paramount [5, 14]. \nThe presence of associated conditions as adenomyosis was \nassociated with increased recurrence rates; however, this \nwas not evaluated in the current study [30].\nStrengths of the study\nThe study used the same technique of the surgical excision \nperformed by the same surgical team. The recurrence rate \nwas evaluated depending on recurrence in the same ovary. \nRecurrence was evaluated depending on ultrasound visu -\nalization of the cyst rather than depending on symptoms.\nLimitations of the study\nThe follow-up duration was relatively small from 12 \nto 30  months. The sample size was small. Pregnancy \nrates after the intervention was not evaluated. It \nwas performed in a single hospital which limits data \ngeneralization. We recruited women with unilocular \nendometriomas, while the involvement of women with \nmultilocular cysts would be more informative.\nConclusion\nThe patient’s related factors and endometrioma charac -\nteristics did not predict its recurrence.\nAbbreviations\nANC  Antral follicle count\nAMH  Anti-Mullerian hormone\nrAFS  Revised American Fertility Society\nSupplementary Information\nThe online version contains supplementary material available at https:// doi. \norg/ 10. 1186/ s43043- 023- 00146-6.\nAdditional file 1. \nAcknowledgements\nNot applicable. The authors are compliant to respond to any post-publication \nqueries regarding this study. Contact would be through the corresponding \nauthor.\nAuthors’ contributions\nKH Atwa: protocol/project development and manuscript writing/editing. \nOT Taha: data collection and analysis. EM El Bassuony: data collection and \nmanagement and manuscript writing/editing. ZM Ibrahim: protocol/project \ndevelopment, manuscript writing/editing, data analysis, and manuscript \nwriting/editing.\nFunding\nSelf-funded.\nAvailability of data and materials\nNot applicable.\nDeclarations\nEthics approval and consent to participate\nAll procedures performed in in the study were in accordance with the ethical \nstandards of the institutional and/or national research committee and with \nthe 1964 Helsinki Declaration and its later amendments or comparable ethical \nstandards. The study was conducted after the approval of our research ethics \ncommittee. Informed consent was obtained from all participants before \nrecruitment.\nConsent for publication\nNot applicable.\nCompeting interests\nThe authors declare that they have no competing interests.\nReceived: 4 October 2022   Accepted: 6 August 2023\nReferences\n 1. Farquhar CM (2000) Endometriosis Extracts from the clinical evidence. \nBMJ 320:1449–1452\n\nPage 5 of 5\nAtwa et al. 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