{"paper_id":"c254518d-6c03-4d18-bf82-e5585e576696","body_text":"R E S E A R C H Open Access\nComparing long term impact on ovarian reserve\nbetween laparoscopic ovarian cystectomy and\nopen laprotomy for ovarian endometrioma\nMoustafa M Zaitoun, Mohamed Moustafa Zaitoun and Manal M El Behery *\nAbstract\nObjective: To compare the long term impact on ovarian reserve between laparoscopic ovarian cystectomy with\nbipolar electrocoagulation and laparotomic cystectomy with suturing for ovarian endometrotic cyst.\nPatient and method(s): 121 patients with benign ovarian endometroitic cysts were randomised to either\nlaparoscopic ovarian cystectomy using bipolar electrocoagulation (61 patients) or laparotomic ovarian cystectomy\nusing sutures (60 patients). Serum follicle-stimulating hormone, Antimullerian hormon, Basal antral follicle Count,\nmean ovarian diameter, and ovarian stromal blood flow velocity were measured at 6, 12 and 18 months after\nsurgery and compared in both groups.\nResult(s): A statistically significant increase of serum FSH was found in the laproscopic bipolar group at 6-, 12 and\n18-month postoperativly compared to open laparotomy suture group. Also, a statistically significant decrease of the\nmean AMH value occurred in laproscopic bipolar group at 6-, 12 and 18-month follow- up compared to open lapar-\notomy suture group. Basal antral follicle number, mean ovarian diameter and peak systolic velocity were significantly\ndecreased during the 6-, 12,18 -month follow-up in laproscopic bipolar group compared to open laparotomy suture\ngroup.\nConclusion(s): After laproscopic ovarian cystecomy for endometrioma all pareameter of ovarian reseve are\nsignificantly decreased on long term follow up as compared to open laprotomy.\nKeywords: Ovarian cysts, Laparoscopic ovarian cystectomy, Electrocoagulation, Ovarian reserve\nIntroduction\nThere is a general consensus amongst gynecologists that\novarian endometriomas require surgical treatment due\nto the ineffectiveness of medical therapies [1,2]. One of\nthe most widespread surgical techniques to excise endo-\nmetriotic cysts is laparoscopic stripping. The surgical\ntreatment of endometriomas, nevertheless, has dualistic\neffects on fertility: on one hand it represents a way to\nimmediately remove the disease and reduce relapse inci-\ndence, improve symptoms like dyspareunia and improve\nsexual life and finally give positive effects on the chances\nof spontaneous conception [3]; on the other hand, it af-\nfects the so-called ovarian reserve, i.e. the pool of small\nantral follicles within both ovaries, potentially already\ncompromised by the development of one or more endo-\nmetriomas within the gonad [4-6].\nIt has been shown that removing ovarian endometrio-\nmas does not increase success rates in IVF , as it worsens\nthe ovarian responsiveness to superovulation [5,7,8]. One\nkey point is the surgical approach at the moment of cyst\nstripping: indeed, a wide variability among surgeons still\nexists, as part of the healthy ovarian tissue may be inad-\nvertently excised together with the endometrioma wall [9].\nNowadays, an increasing number of young patients\nundergoing surgery for endometrioma are postponing\nfertility for many years after their treatment. It will\ntherefore be important for these patients and their clini-\ncians to know the possible long-term effect of endome-\ntrioma surgery on future fertility.\nShort- to medium-term studies have suggested that ex-\ncision of endometriomas causes significant damage to\n* Correspondence: mbhry@hotmail.com\nObstetrics & Gynecology Departments, Faculty of Medicine, Zagazig\nUniversity, Zagazig, Egypt\n© 2013 Zaitoun et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative\nCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and\nreproduction in any medium, provided the original work is properly cited.\nZaitoun et al. Journal of Ovarian Research 2013, 6:76\nhttp://www.ovarianresearch.com/content/6/1/76\n\novarian reserve and that this does not recover within up\nto nine months [10-14].\nDespite an extensive literature search, to date we\ncouldn’t find any study that has compared laparoscopic\nsurgery with electro coagulation with laprotomy excision\nwith ovarian suturing for endometrioma regarding their\nlong term impact on ovarian reserve.\nThe aim of this prospective interventional study is to\ncompare the long term impact on ovarian reserve be-\ntween laparoscopic ovarian cystectomy with bipolar elec-\ntrocoagulation and laparotomy cystectomy with suturing\nfor ovarian endometrotic cyst.\nPatients and methods\nThis prospective randomized study was conducted from\nApril 1, 2008, to August 31, 2012, at Zagazig University\nHospitals, Zagazig, Egypt. Informed written consent was\ntaken from each participant before enrollment in the\nstudy and the study protocol was approved by the local\nethics and research committee.\nThe inclusion criteria were: Age 18 – 40 years; unilat-\neral ovarian cyst with clinical and sonographic finding\nsuggesting endometriotic cyst,; regular menstrual cycles\nin the previous6 months preceeding surgery.\nWomen who met the following criteria were excluded\nbecause these factors can affect ovarian stromal blood\nflow: previous ovarian surgery; surgical nessicity to per-\nform adnexectomy, polycystic ovary syndrome according\nto the 2003 Rotter dam criteria [15]; or other known\nendocrinological disorders, history of oral contraceptive\npill use or intake of other hormonal agents within\n3 months before enrollment. Patients with histopatho-\nlogic diagnosis of malignant ovarian cyst; or ther bengin\ncyst apart from endometrioma were excluded as well.\nPatients that got pregnant during follow period or lost\nfollow up were also excluded.\nWomen with a diagnosis of unilateral ovarian cyst\nwere observed for 3 menstrual cycles by transvaginal\nultrasound examination on day 3 of each cycle to deter-\nmine whether the cyst size remained the same or\nbecame bigger. Thereafter, patients were randomly\nallocated into two groups laparoscopy and open laparo-\ntomy groups using computer-designed randomization\nmethods. The randomization sequence was protected\n(concealed) in a sealed envelope until the the operation,\nso that operators and patients were not aware of the\nassignment. The sample size was calculated to give a\nstatistical power of 80% at a 95% confi dence interval\nof 1.47.\nAll ovarian follicles measuring 3 mm to 10 mm on\nboth ovaries were counted preoperatively in both groups\nusing the largest cross-sectional sagittal view of the\novary, the averaged ovarian diameters for each patient\nwere calculated by measuring two perpendicular diame-\nters. The stromal blood flow of the ovary was assessed\nby color Doppler ultrasound. Flow velocity waveforms\nwere obtained from stromal blood vessels away from the\novarian capsule and the utero ovarian ligament. The\n“gate” of the Doppler was positioned when a vessel with\ngood color signals was identified on the screen. The\npeak systolic velocity of stromal vessels was calculated\nelectronically when at least three similar, consecutive\nwaveforms of good quality were obtained.\nAll ultrasound studies were performed by a single\nexperienced sonographer to decrease interob-server\nvariability using the Voluson 370 pro V (GE Medical\nSystems Kretzte hnik, Zip f Austria) ultra sound device e\nquipped with a 7.5 MHz vaginal probe.The sample size\nwas calculated to give a statistical power of 80% at a 95%\nconfi dence interval of 1.47.\nThe serum, FSH, AMH levels were measured pre-\noperatively on day 3 of the menstrual cycle. The DSL-\n10-14400 Active Müllerian-inhibiting Substance/AMH\nenzyme-linked immuno-sorbent assay (Diagnostic Sys-\ntems Laboratories, Webster, TX, USA) was used for\nthese measurements. The intra-assay and interassay\ncoefficients of variation for AMH were 4.6% and 8.0%,\nrespectively,with a detection limit of 0.017 ng/mL. All\nsamples (preoperative andpostoperative) for a given\npatient were analyzed in a single assay.\nIn total, 79 patients underwent laparoscopic ovarian\ncystectomy by use of a stripping technique. After an\ninitial laparoscopic pelvic evaluation, abdominal and\nperitoneal washings were performed for cytology. Lap-\naroscopic ovarian cystectomy was performed by incision\nof the ovarian cyst with monopolar diathermy, identifica-\ntion of the cystic wall, and removal of the cyst wall from\nthe ovarian cortex by traction with grasping forceps in\nopposite directions. After excision of the cyst wall, bipo-\nlar energy at a power of 40 W for 4 seconds was used to\ncontrol focal bleeding. The residual ovarian tissue was\nnot sutured, and the ovarian edges were left to heal by\nsecondary intention.\nOvarian cystectomy by laparotomy through Pfannenstiel\nincision was performed on another 79 patients. After peri-\ntoneal cytology and inspection of the peritoneal cavity, the\ncleavage plane was developed by using microsurgical tech-\nniques and instruments. After excision of the cyst wall,\nmeticulous reconstruction and hemostasis of the ovarian\ntissue were achieved by use of 2 –0 polyglactin sutures\n(Vicryl; Ethicon Endo-Surgery, Cincinnati, OH, USA). The\novary was sutured edge-to-edge.\nFrozen sections were obtained and every cyst was\npathologically examined. Both techniques were per-\nformed by the same team of surgeons, with all surgeons\nhaving comparable surgical skills and experience.\nAll surgeries were performed within an adequate\nperiod of time. All patients were asked to return on day\nZaitoun et al. Journal of Ovarian Research 2013, 6:76 Page 2 of 6\nhttp://www.ovarianresearch.com/content/6/1/76\n\n3 of menstrual cycles 6, 12, 18 months after their sur-\ngery, at which point an FSH and AMH assays were per-\nformed. Basal antral follicle count, mean ovareian\ndiameter, and peak systolic velocity of stromal vessels\nwere also measured at 6, 12, 18 months in both groups.\nStatistical analyses were performed with Statistics\nPackage for Social Sciences software (SPSS, Inc.,\nChicago, IL) version 11.5 for windows. Qualitative data\nwere expressed as number and compared using chi-\nsquared test. Quantitative Keuls follow-up test was used\nfor multiple comparisons between means. P < .05 was\nconsidered statistically significant.\nResults\nAccording to the inclusion criteria, a total of 158 pa-\ntients were found elligable and initially, included in the\nstudy, with 79 women being allocated to undergo lap-\naroscopic ovarian cystectomy and 79 women being allo-\ncated to undergo open laparotomy.\nThirty seven women were excluded (4 with histo-\npasthologic diagnosis of ovarian malignancy, 6 benign\ncyst other than endometrioma, 18 got pregnant during\nfollowup, 9 lost follow up). Thus, 121 women with a\nconfirmed diagnosis of endometrioma by histopathology\nformed the final study group (61 patients in laproscopic\ngroup, 60 patients in laparotomy group). The general pa-\ntient characteristics are presented in Table 1. Both\ngroups were comparable in age and BMI, preoperative\nserun FSH, AMH were normal and comparable in both\ngroups. Pregnancies occurred in eleven patients in open\nlaparotomy group, and in seven patients in laparoscopic\ngroup during the 18 months follow up period which was\nnot statically significant.\nAll patients had normal FSH values preoperatively.\nThe mean values of FSH before surgery and during the\n6,12,18-month follow-up period are shown in Table 2.\nComparing the bipolar group with the suture group, a\nstatistically significant increase of the mean FSH value\nwas seen in the laproscopic bipolar group during all the\n6,12,18 -month follow-up period.\nAll patients had normal AMH values preoperatively.\nThe mean values of AMH before surgery and during the\n6-,12,18 month follow-up period are shown in Table 3.\nComparing the bipolar group with the suture group, a\nstatistically significant decrease of the mean AMH value\nwas seen in laproscopic bipolar group the during all the\nfollow-up period.\nThe basal antral follicle number, and mean ovarian\ndiameter, and peak systolic velocity were comparable\npreoperatively in both group with no stastically signifi-\ncant difference (Table 4). At the 6,12,18 -month follow-\nup visits, the basal antral follicle number, peak systolic\nvelocity, and mean ovarian diameter of the operated\novary in the bipolar group were statistically significantly\ndecreased when compared with the suture group at the\nsame time (Table 5).\nDiscussion\nOur study has demonstrated that bipolar coagulation of\nthe ovarian parenchyma during laproscopic cystectomy\nfor endometroitic cyst adversely affects ovarian reserve\non long term follow up. Most studies on the topic of\novarian reserve after surgery are provided by infertility\ncenters and are consequently limited by the selection of\npatients. We did not consider the woman ’s postsurgical\nfertility a proper criterion for evaluating the ovarian re-\nserve. Fertility is not the result of ovarian function alone\nand depends on multiple factors. Moreover, not all of\nour patients desired to get pregnant during the study\nperiod.\nComparing the laproscopic bipolar group with the\nsuture group, a statistically significant increase of mean\nFSH value was seen in bipolar group at all of the\nfollow-up visits. All patients had normal AMH values\nTable 1 Comparison between the demographic characteristics of the two studied groups\nCharacteristics Bipolar (N = 61) Suture (N = 60) T-test P-value\nAge (Years)\n‾X±SD 24.2 ± 3.1 25.2 ± 3.0 −1.6 0.1\nBMI(kg/m2) 14\n27(5.8) 27(5.8) 0.2\nFSH preoperative level 6.5 ± 0.4 6.5 ± 0.4 −0.2 0.86\nAMH preoperative level 4.5 ± 0.8 4.6 ± 0.9 −0.1 0.8\nPregnancy occurred 7 4.0 11 8.0 0.7\nPreoperative AFC 6.6 ± 2.3 6.4 ± 2.5 0.1 0.75\nPreoperative PSV 12.7 ± 2.2 13.3 ± 1.8 1.2 0.27 1.2 0.27\nPreoperative MOD 2.3 ± 0.6 2.4 ± 0.9 0.48 0.49\nN: Number of patients.\n(P > 0.05): means non-significant.\nSD: Standard Deviation ‾X: Mean.\nZaitoun et al. Journal of Ovarian Research 2013, 6:76 Page 3 of 6\nhttp://www.ovarianresearch.com/content/6/1/76\n\npreoperatively.this runs in agreement with study of\nStreuli and co-workers which has established baseline\nsimilarities in circulating AMH in women with and\nwithout endometriomas [16,17]. Comparing the bipolar\ngroup with the suture group, a statistically significant de-\ncrease of the mean AMH value was seen in the lapro-\nscopic bipolar group during all the 18 month follow-up\nperiod.\nWhen comparing the suture group with the bipolar\ngroup, a statistically significant decrease in basal antral\nfollicle count and mean ovarian diameter were revealed\nin bipolar group during the 6,12,18 month follow-up\nevaluations; also a statistically significant decrease in\npeak systolic velocity was seen in bipolar group during\nall the follow- up visits. Our results disagree with those\nof Candiani et al. [18] who studied the antral follicle\ncount, ovarian volume, stromal blood flow, and side of\novulation in 31 patients after laparoscopic cystectomy,\nbut they failed to observe the reduction of stromal blood\nflow, this could be due to short term (3 months) follow\nup period. So they could not classify the possible mecha-\nnisms that caused gonad injury.\nSeveral retrospective studies detected reduced re-\nsponses to gonadotropin [19,20] with a marked reduc-\ntion in the number of both dominant follicles and\nTable 2 Comparison between the mean values of serum\nFSH (mIU/mL) between bipolar and suture groups\nMean values Laproscopy bipolar\ngroup (N = 61)\nLaprotomy\nsuture group\n(N = 60)\nT-test P-value\nFSH\npreoperative\nlevel\n‾X±SD 6.5 ± 0.4 6.5 ± 0.4 −0.2 0.86\nFSH 6th\nmonth\n‾X±SD 11.4 ± 0.3 7.3 ± 0.4 31.7 0.000***\nFSH 12 th\nmonth\n‾X±SD 10.7 ± 0.3 6.9 ± 0.4 33.5 0.000***\nFSH 18th\nmonth\n‾X±SD 10.5 ± 0.3 6.7 ± 0.4 32.7 0.000***\np-value 0.000*** 0.000***\nSD: Standard Deviation ‾X: Mean.\n***p<0.005 highly significant.\nTable 3 Comparison between the mean values of serum\nAMH (ng/mL) between bipolar and suture groups\nMean values Laproscopy bipolar\ngroup (N = 61)\nLaprotomy\nsuture group\n(N = 60)\nT-test P-value\nAMH\npreoperative\nlevel\n‾X±SD 4.5 ± 0.8 4.6 ± 0.9 −0.1 0.8\nAMH 6 th m\n‾X±SD 2.4 ± 0.5 4.5 ± 0.9 −9.5 0.000***\nAMH 12 th\n‾X±SD 2.7 ± 0.5 4.4 ± 0.9 −7.9 0.000***\nAMH 18th m\n‾X±SD 2.5 ± 0.4 4.5 ± 0.9 −8.9 0.000***\np-value 0.000*** 0.32\n(P > 0.05): Means non-significant.\n***p<0.005 highly significant.\nSD: Standard Deviation ‾X: Mean.\nTable 4 Comparison between the mean values of AFC,\nPSV (cm/s) and MOD (cm) on transvaginal ultrasound\nexaminations of the un operated intact ovaries between\nbipolar and suture groups\nMean\npreoperative\nvalues\nLaproscopy\nbipolar\ngroup (N = 61)\nLaprotomy\nsuture\ngroup (N = 60)\nT-test P-value\nAFC 6.6 ± 2.3 6.4 ± 2.5 0.1 0.75\nPSV 12.7 ± 2.2 13.3 ± 1.8 1.2 0.27\nMOD 2.3 ± 0.6 2.4 ± 0.9 0.48 0.49\n(P > 0.05): Means non-significant.\nAFC: Antral Follicle Count.\nPSV: Peak Systolic Velocity.\nMOD: Mean Ovarian Diameter.\nTable 5 Statistical comparison between post operative\nmean values of AFC, PSV (cm/s) and MOD (cm) on TVS\nexaminations between bipolar and suture groups\nMean\nvalues\nLaproscopy bipolar\ngroup (N = 61)\nLaprotomy suture\ngroup (N = 60)\nT-test P-value\n6th\nmonth\nAFC 3.0 ± 2.5 4.8 ± 2.1 0.0 0.05\nPSV 8.4 ± 2.9 10.2 ± 3.4 4.1 0.05\nMOD 2.2 ± 0.6 4.4 ± 0.2 1.5 0.03*\n12\nmonth\nAFC 3.6 ± 2.0 4.8 ± 2.3 3.5 0.05\nPSV 8.0 ± 3.7 11.0 ± 2.9 9.2 0.004***\nMOD 2.0 ± 0.5 2.6 ± 0.4 19.8 0.000***\n18\nmonth\nAFC 4.0 ± 2.6 5.9 ± 2.4 6.5 0.01*\nPSV 7.8 ± 4.0 11.2 ± 3.8 9.9 0.003**\nMOD 1.79 ± 0.3 2.4 ± 0.5 4.9 0.03*\n(P > 0.05): Means non-significant.\n*P<0.05: Significant.\n**P<0.05: Significant\n***P<0.005 highly significant.\nAFC: Antral Follicle Count.\nPSV: Peak Systolic Velocity.\nMOD: Mean Ovarian Diameter.\nZaitoun et al. Journal of Ovarian Research 2013, 6:76 Page 4 of 6\nhttp://www.ovarianresearch.com/content/6/1/76\n\nretrieved oocytes in the operated ovary after cystectomy\n[21,22]. While others have not found any adverse out-\ncomes after ovarian cystectomy compared with controls\n[23,24] and reported that laparoscopic cystectomy of\novarian endometriomas did not affect ovarian response\nto gonadotropin stimulation, although the gonadotropin\ndose was higher in the cystectomy group.\nFedele et al. [1] reported that bipolar electrocoagula-\ntion of the ovarian parenchyma during laparoscopic re-\nmoval of endometriotic ovarian cysts adversely affected\novarian function, this goes in line with our results, how-\never in their study only FSH levels of endometrioma pa-\ntients was checked which does not rule out the possible\novarian damage by endometriosis itself.\nIn cases where laparoscopic excision must be abso-\nlutely done (e.g. for relevant symptoms), alternative sur-\ngical techniques such as the combined cystectomy plus\nablation [25] or the ultrasound-guided puncture with\nmethotrexate [26] or alcohol injection [27,28] could be\nconsidered, especially in patients who are aged over 38\nyears or who have an already small ovarian reserve.\nRecent study [29] showed that, even when performed\nby experienced laparoscopists with the highest level of\ncautiousness, the laparoscopic stripping of endometriotic\ncysts reduces the ovarian follicular reserve. The signifi-\ncant reduction of AMH after surgery confirms previous\nhistological observations, suggesting that part of the\nhealthy ovarian pericapsular tissue, containing primor-\ndial and preantral follicles, is removed or damaged des-\npite every surgical effort to be atraumatic. This must be\ncarefully considered when ovarian surgery is proposed to\npatients with one or more ovarian endometriomas, but\nno relevant symptoms besides infertility.\nShortcoming of this study is that it would have been\nmore scientific to compare bipolar electro coagulation\nwith hemostatic suturing using the laparoscopic route for\nboth approaches. However, laparoscopic ovarian stripping\nusing bipolar electro coagulation and open laparotomy\nusing hemostatic suture are the 2 most commonly used\ntechniques for managing benign ovarian cysts at the study\nhospital, and the surgeons participating in the study did\nnot have adequate experience with laparoscopic suturing\ntechniques as we mentioned previously [18].\nThe results of our study support the following obser-\nvations. First, the laparoscopic excision of ovarian cysts\nis associated with a statistically significant reduction long\nterm impact on ovarian reserve. Second, the damage\ncannot be ascribed merely to the amount of ovarian tis-\nsue removed during surgery; the damage to the ovarian\nvascular system by electrocoagulation is another factor.\nHowever, further studies in a larger number of patients\nare required to make certain judgments whether the in-\njury is related to other factors and to ascertain which is\nthe less harmful alternative therapeutic approach.\nCompeting interests\nThe authors declare that they have no competing interests.\nAuthors’ contributions\nFirst author: study design, perform experiment. Second author: analyse data,\ncollect material for writing, Third author: supply material for writing, shared\nin data analysis, wrote the manuscript. All authors read and approved the\nfinal manuscript.\nReceived: 22 August 2013 Accepted: 9 October 2013\nPublished: 2 November 2013\nReferences\n1. Farquhar C, Sutton C: The evidence for the management of\nendometriosis. Curr Opin Obstet Gynecol [Review] 1998, 10(4):321–332.\n2. 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Journal of Ovarian Research\n2013 6:76.\nSubmit your next manuscript to BioMed Central\nand take full advantage of: \n• Convenient online submission\n• Thorough peer review\n• No space constraints or color figure charges\n• Immediate publication on acceptance\n• Inclusion in PubMed, CAS, Scopus and Google Scholar\n• Research which is freely available for redistribution\nSubmit your manuscript at \nwww.biomedcentral.com/submit\nZaitoun et al. Journal of Ovarian Research 2013, 6:76 Page 6 of 6\nhttp://www.ovarianresearch.com/content/6/1/76","source_license":"CC0","license_restricted":false}