{"paper_id":"b096c43c-348d-4bd2-9f39-d75c29258086","body_text":"R E S E A R C H Open Access\nOvarian endometriomas and IVF: a retrospective\ncase-control study\nFrancesca Bongioanni 1, Alberto Revelli 2*, Gianluca Gennarelli 2, Daniela Guidetti 1, Luisa Delle Delle Piane 2 and\nJan Holte 3\nAbstract\nWe performed this retrospective case-control study analyzing 428 first-attempt in vitro fertilization (IVF) cycles,\namong which 254 involved women with a previous or present diagnosis of ovarian endometriosis. First, the results\nof these 254 cycles were compared with 174 cycles involving patients with proven non-endometriotic tubal\ninfertility having similar age and body mass index. Women with ovarian endometriosis had a significantly higher\ncancellation rate, but similar pregnancy, implantation and delivery rates as patients with tubal infertility. Second,\namong the women with ovarian endometriosis, the women with a history of laparoscopic surgery for ovarian\nendometriomas prior to IVF and no visual endometriosis at ovum pick-up (n = 112) were compared with the non-\noperated women and visual endometriomas at ovum pick-up (n = 142). Patients who underwent ovarian surgery\nbefore IVF had significantly shorter period, lower antral follicle count and required higher gonadotropin doses than\npatients with non-operated endometriomas. The two groups of women with a previous or present ovarian\nendometriosis did, however, have similar pregnancy, implantation and live birth rates. In conclusion, ovarian\nendometriosis does not reduce IVF outcome compared with tubal factor. Furthermore, laparoscopic removal of\nendometriomas does not improve IVF results, but may cause a decrease of ovarian responsiveness to\ngonadotropins.\nBackground\nLaparoscopic stripping of endometriomas before IVF/\nICSI treatment in order to improve its outcome is wide-\nspread in everyday clinical practice. This procedure is,\nhowever, not based on clinical evidence[1-3]. Although\na previous metanalysis [4], showed reduced pregnancy\nrates after IVF in women with ovarian endometriosis\ncompared to patients undergoing IVF for other indica-\ntions [5], other later studies could not confirm this find-\ning [6-9]. When the influence of the surgical removal of\nendometriomas on IVF outcome was studied, operated\npatients obtained IVF results comparable to women\nwithout previous surgical intervention [10-15]. Further-\nmore, some results suggest that the surgical intervention\nmay have a negative effect on ovarian reserve [12,16-18]\nand hence putatively compromise treatment outcome\nand long-term fertility.\nThus, the possible impact of ovarian endometriosis on\nART results remain a controversial issue. The aim of\nthe present study was to retrospectively analyze a large\nnumber of IVF/ICSI cycles and to evaluate the treat-\nment outcome (a) in patients with a diagnosis of ovarian\ne n d o m e t r i o s i si nc o m p a r i s o nt ot h a ti np a t i e n t sw i t h\ntubal infertility and (b) in women with a history of\nlaparoscopic removal of ovarian endometriomas prior to\nIVF compared with the outcome in women without pre-\nvious surgical intervention and a visual endometrioma\nat OPU.\nMethods\nPatients\nA total number of 8623 first-attempt IVF cycles per-\nformed in three IVF units were retrospectively analyzed.\nIn total, 254 cycles were found to involve women diag-\nnosed with ovarian endometriosis. Of these, 142 women\nhad never undergone any ovarian surgery and displayed\none or more in situ ovarian endometriomas of small to\nmedium size (< = 6 cm in diameter; Group A), and 112\nwomen underwent IVF after the laparoscopic removal of\n* Correspondence: fertisave@yahoo.com\n2Reproductive Medicine and IVF Unit, Department of Obstetrical and\nGynecological Sciences, University of Torino, OIRM-S, Anna Hospital, Torino,\nItaly\nFull list of author information is available at the end of the article\nBongioanni et al . Reproductive Biology and Endocrinology 2011, 9:81\nhttp://www.rbej.com/content/9/1/81\n© 2011 Bongioanni 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.\n\none or more endometrioma(s) of comparable size (< = 6\ncm in diameter) by the classical “stripping ” technique\n(Group B). These women did not have visual endome-\ntriomas at the time of OPU. The proportion of patients\nwith bilateral endometriomas was 14.1% in Group A (20\nout of 142) and 19.6% in group B (22 out of 112), a dif-\nference not statistically significant. In case of bilateral or\nmultiple endometriomas, their diameter was summed: in\nall cases, the total diameter did not exceed 6 cm. Endo-\nmetriosis patients in Group B were operated because\nthey were symptomatic, whereas those in Group A were\nnot operated before IVF because they were no or less\nsymptomatic, although they had endometriomas of simi-\nlar size.\nIn all patients submitted to laparoscopic ovarian resec-\ntion, the diagnosis of ovarian endometriosis was histolo-\ngically confirmed. In women who had not been\noperated before IVF (Group A), the diagnosis of ovarian\nendometriosis was based on transvaginal ultrasound\n(evidence of an adnexal mass with diffuse low level\nechoes without neoplastic or acute hemorrhage features;\n[19]) and the AFS stage was estimated to be II-III in all\ncases. None of the patients operated for ovarian endo-\nmetriosis received GnRH-agonists or other medical\ntreatments prior to or after operation.\nThe control group consisted of 174 women who\nunderwent IVF treatment during the same time period,\nwith laparoscopically diagnosed tubal factor and without\nany evidence of ovarian endometriosis. These women\ncovered similar ranges of age and BMI as the endome-\ntriosis patients (Group C).\nIVF procedure\nOvarian stimulations were conducted with daily subcu-\ntaneous injections of indiv idual starting doses of rFSH\n(Follitropin alfa (Merck-Serono, Geneva, Switzerland)\nor Follitropin beta (Organon, Oss, the Netherlands) or\nhMG (Meropur/Menopur, Ferring, Switzerland) at\nappropriate doses (100-450 IU), estimated according to\nthe woman ’sage, the antral follicle count and the basal\n(day 3) FSH. The long GnRH-agonist down-regulation\nprotocol was used (Nafarelin-Pfizer Inc., New York,\nUSA) 400 mg nasally twice daily, or buserelin (Sanofi-\nAventis, Paris, France) 0.3 mg nasally four times daily);\nin both cases half the dose was administered during\novarian stimulation. Ovarian response to gonadotro-\npins was monitored by transvaginal ultrasound plus\nserum E2 measurement every third day from stimula-\ntion day 7. Ovulation was tri ggered by injecting 10,000\nIU hCG s.c. when the leading follicle reached 18 mm,\nwith appropriate serum E2 levels. Transvaginal ultra-\nsound-guided oocyte aspir ation (OPU) was performed\napproximately 36 hours after hCG injection under\nlocal anaesthesia (paracervical block). Either IVF or\nICSI was performed according tothe clinical indication.\nAfter cultivation, embryos were transferred on Day 2\nor 3 after ovum pick-up (OPU). Luteal phase support\nwas given vaginally to all patients for 2 weeks from\nembryo transfer (progesterone vagitories (Apoteket AB,\nStockholm, Sweden) 1200 mg or gel (Merck-Serono,\nGeneva, Switzerland) 180 mg daily). Pregnancy was\ndefined as the visualization of a gestational sac at vagi-\nnal ultrasound investigation in gestational week 7. All\ndata were de-identified ahead of analysis. The study\ndid not in any way alter our routine IVF/ICSI proto-\ncols, nor did it involve any additional intervention at\ntreatment. All data were prospectively collected with\nthe intention to evaluate impact on treatment\noutcome.\nOvarian surgery technique\nA four-port laparoscopy technique was used: an 11 mm\ntrocar was inserted through a short umbilical incision\nand connected to a video monitor (WideVieuw ™HD\nKarl Storz Endoscope); tw o additional lateral 5 mm\noperating ports and a central sovrapubic 5-10 mm oper-\nating port were also inserte d. The pneumo-peritoneum\nwas achieved by inflating CO2 (10 mmHg).\nTo excide endometriomas, an incision was performed\nat the antimesenteric site of the affected ovary using\nbipolar cautery; then, the endometrioma was drained\nwith aspiration and the pseudo-capsule was dissected\nby gentle traction and countertraction using two 5 mm\ngrasping forceps (\"stripping ”). The bleeding at the\nstripping site was stopped by bipolar cautery, only\nwhen necessary and very carefully in order to avoid\nunnecessary thermal damage to the healthy ovarian\ntissue.\nAssessment of ovarian sensitivity to FSH\nTo assess ovarian sensitivity to FSH, the ratio between\nthe number of retrieved oocytes and the number of FSH\nIU (x100) was calculated. This variable was defined\n“ovarian sensitivity ”,a si ts h o w st h ee f f e c t i v eo v a r i a n\nresponse to FSH stimulation, independently on the total\namount of administered FSH. Patients with more abun-\ndant ovarian follicular reserve tend to display higher\novarian sensitivity to exog enous FSH, whereas women\nwith a low ovarian reserve usually have a lower ovarian\nsensitivity.\nStatistical analysis\nData are expressed as the mean ± SEM or as percen-\ntages when required. Statistical comparisons among\ngroups were performed using the Fisher exact test,\nYeats’ corrected c\n2,W i l c o x o n’s test or Student ’stt e s t ,\nas appropriate. The JMP software was used for statistical\nelaboration. Significance was defined as a p value < 0.05.\nBongioanni et al . Reproductive Biology and Endocrinology 2011, 9:81\nhttp://www.rbej.com/content/9/1/81\nPage 2 of 6\n\nResults\nIVF outcome in patients with ovarian endometriosis vs.\npatients with tubal factor\nThe basal characteristics of patients with ovarian endo-\nmetriosis (Group A), previously operated of endome-\ntrioma excision (Group B) and tubal infertility (Group\nC, controls) are shown in Table 1.\nT h eg r o u p sw e r ec o m p a r a b l ef o ra g e ,B M I ,i n f e r t i l i t y\nduration, smoking habits, mean period, prevalence of\nassociated male factor, and basal (day 3) FSH levels. The\nbasal antral follicle count was significantly lower in\nwomen previously submitted to the excision of ovarian\nendometriosis (Group B) than in women with ovarian\nendometrioma(s) (Group A) or tubal factor infertility\n(Group C).\nThe outcome of IVF in patients affected by ovarian\nendometriosis versus woman with tubal factor is shown\nin Table 2. Women with ovarian endometriosis showed\na significantly higher canc ellation rate, but those who\ncompleted ovarian stimulation had a similar yield of\noocytes at OPU and a comparable ovarian sensitivity\ncompared to control subjects. Fertilization rates were\nsimilar, but women with endometriosis showed a lower\npercentage of cycles with complete failure of fertilisa-\ntion. Overall, the implantation, pregnancy and live-birth\nrates per started cycle, OPU, and ET were similar in the\ngroups.\nIVF outcome in patients with in situ ovarian\nendometrioma(s) vs. patients previously operated for\novarian endometrioma(s)\nThe clinical characteristics of patients having one or\nmore in situ ovarian endometriomas at the time of IVF\n(Group A) and of women who had been previously\noperated for endometrioma removal (Group B) are\nshown in Table 1. Operated women had a shorter mean\nperiod and lower antral follicle counts than women with\nin situ endometrioma(s).\nWomen with previous ovarian surgery required higher\ntotal FSH doses than patients without previous surgery,\nbut had comparable numbers of oocytes at OPU (Table\n2). Thus, ovarian sensitivity was lower in operated\nwomen. The implantation rate, pregnancy rate and live-\nbirth rate per started cycle, OPU, and ET were similar\nin the two groups.\nDiscussion\nThe present study retrospectively analyzed a large\ncohort of patients undergoing IVF in the years 2004-\n2009, identifying 254 patients with a previous or present\ndiagnosis of ovarian endometriosis. With the limitations\nof a retrospective study (although on a remarkably large\nnumber of observations), ou r results suggest that pre-\nvious or present ovarian endometriosis does not impair\nsuccess rates at IVF/ICSI, and that ovarian surgery for\nendometriosis does not result in improved ART out-\nc o m e ,b u t ,o nt h ec o n t r a r y ,m a yc o m p r o m i s eo v a r i a n\nreserve.\nLaparoscopic stripping of ovarian endometriomas as\nan intervention to improve fertility is a widespread clini-\ncal practice, not only to imp rove natural fertility, but\nalso to improve IVF outcome. This surgical strategy is\nused because of the following reasons: a) older studies\nsuggested that patients with ovarian endometriosis had\npoorer IVF outcome than wo men with other infertility\ncauses; b) some data suggest that spontaneous fecundity\nmay improve after laparoscopic cystectomy [1]; c) some\nargue that puncturing an endometrioma during oocyte\nretrieval could spread endometriotic cells in the abdom-\ninal cavity or cause a pelvic infection.\nThe risk of complications linked to the puncture of\novarian endometriomas is, however, minimal: infec-\ntions have been reported only sporadically [20,21], and\nindeed a study in which ovarian endometriomas were\nintentionally punctured an d aspirated at the time of\noocyte retrieval reported no complications [22].\nFurthermore, aspiration of endometriomas followed by\nlocal injection of methotrex ate [23] or alcoholic solu-\ntions [24,25] is considered a therapeutic option for\novarian endometriosis.\nAs for IVF outcome in women with a diagnosis of\novarian endometriosis, the pu blished data exhibit vary-\ning results. A meta-analysis from 2002 including 22 stu-\ndies showed a reduced pregnancy rate after IVF in\nwomen with endometriosis compared to treatments in\nwomen with other infertility causes, and also showed a\nlinear (inverse) relationship between the stage of the\nTable 1 Clinical characteristics of patients having one or\nmore in situ endometrioma(s) at the time of IVF (Group\nA) vs. those previously operated for laparoscopic\nendometrioma(s) removal (Group B) vs. women with\ntubal infertility (Group C, controls)\nGroup A Group B Group C p\nPatients 142 112 174\nAge (yrs) 33.8 ± 3.1 33.6 ±\n4.4\n34.0 ±\n3.1\nns\nBMI (kg/m 2) 22.7 ± 3.2 22.4 ±\n3.2\n23.1 ±\n3.3\nns\nSmoke (%) 11.8 16.1 15.3 ns\nMean period (days) 28.8 ± 4.0 27.2 ±\n4.1\n28.5 ±\n3.1\n< 0.005 1\n< 0.004 2\nInfertility duration (years) 4.0 ± 2.5 3.9 ± 2.9 3.6 ± 0.3 ns\nAssociated male factor\n(%)\n13.8 19.1 13.7 ns\nAntral follicle count 16.9 ±\n11.1\n11.7 ±\n9.4\n16.6 ±\n9.5\n<\n0.0011,2\nFSH day 3 level (U/l) 7.2 ± 3.9 7.9 ± 4.2 6.6 ± 3.5 ns\n1Group A vs Group B, 2Group B vs Group C, ns: not significant.\nBongioanni et al . Reproductive Biology and Endocrinology 2011, 9:81\nhttp://www.rbej.com/content/9/1/81\nPage 3 of 6\n\ndisease and the pregnancy rate [4]. However, several\nsubsequent studies, including a large epidemiological\nsurvey [9], reported similar IVF outcome in patients\nwith ovarian endometrios is as in women with other\ninfertility causes [6,8,26,27] . A recent study comparing\npatients with endometriomas with women with non-\nendometriotic ovarian cysts suggested that ovarian\nendometriosis was associated with poorer embryo qual-\nity, although the pregnancy rate was unaffected [28].\nIntervention studies investi gating the effectiveness of\nlaparoscopic removal of ovarian endometriosis as a tool\nto improve subsequent IVF results also show mainly\nnegative results. Several reports showed that the out-\ncome of IVF in patients previously submitted to laparo-\nscopic stripping of endometriomas was similar to that of\nendometriosis-free controls [27,29-32]. As these studies\ndid not include a group of patients with endometriomas\nwho had not been subject to surgery, the impact of\noperating ovarian endometriosis per se could not be\nevaluated. In line with our results, a recent metanalysis\nshowed that the outcome of IVF was similar in patients\nwith in situ ovarian endometriomas as in endometriosis-\nfree women [7]. In 30 infertile patients that served as\ntheir own controls as they were treated with IVF both\nbefore and after surgical treatment of ovarian endome-\ntriosis, Shahine [15] showed that embryo quality on day\n3 was not improved after ovarian surgery, and IVF\nresults remained comparable to those obtained before\nthe operation. A recent meta -analysis including five\nstudies comparing surgery vs. no treatment of endome-\ntrioma before IVF showed that there was no significant\ndifference in the clinical pregnancy rate between the\noperated and the non-operated patients [13]. Only the\nstudy of Barri [33] reported a better IVF outcome in\npatients with ovarian endom etriosis previously sub-\nmitted to ovarian surgery vs. patients undergoing IVF as\nthe first therapeutic option. Thus, most available data\nclearly show that surgical management of endometrio-\nmas gives no advantage for a subsequent IVF.\nOur results showed that wo men operated for ovarian\nendometriosis exhibited several markers of a reduced\novarian reserve. Thus, cancellation rates, mean period\n[34], antral follicle counts and ovarian sensitivity to\nFSH/hMG were all reduced in the group of operated\nwomen. These findings are well in line with previous\ndata. Patients previously submitted to laparoscopic\ncystectomy required a higher gonadotropin dose to\nachieve a similar ovarian response [12,16-18] or showed\na lower oocyte yield [12,14,32,35-37]. In women oper-\nated for a monolateral ovarian endometrioma, it was\nreported that the operated ovary produced a lower num-\nber of follicles than the contralateral [38,39]. Indeed a\nhistologically proven loss of functional ovarian tissue\nclose to the cyst was well documented [40]. Moreover,\nTinkanen [10] reported that non-operated patients had\nsignificantly more embryos and higher pregnancy and\nlive birth rates than operated women. In a prospective,\nrandomized trial, Demirol [12] showed that operated\nTable 2 IVF outcome of patients having one or more in situ endometrioma(s) at the time of IVF (Group A) vs. those\npreviously operated for laparoscopic endometrioma(s) removal (Group B) vs. woman with tubal infertility (Group C,\ncontrols)\nGroup A Group B Group C p\nCancellation rate (%) 7.5 9.8 2.9 < 0.02 2,3\nTotal FSH dose (IU) 2339 ± 1248 3298 ± 1404 2537 ± 1090 < 0.001 1,3\nN. of retrieved oocytes 9.4 ± 4.3 8.2 ± 5.3 9.6 ± 4.0 < 0.03 3\nMII oocytes (%) 71.2 68.8 66.9 ns\nOvarian sensitivity 5.6 ± 3.2 3.5 ± 3.5 5.0 ± 3.0 < 0.001 1,3\nType of treatment (%)\nIVF 77 72 68 ns\nICSI 19 23 25 ns\nCombined 457 n s\nFertilization rate (%) 67.7 73.4 70.2 ns\nCycles with no fertilization (%) 6.6 8.2 10.0 < 0.04 2\nNumber of embryos transferred 2.0 ± 0.5 2.1 ± 0.6 2.2 ± 0.4 ns\nPregnancy rate/ started cycle (%) 41.5 36.6 35.0 ns\nPregnancy rate/OPU (%) 45.0 40.6 36.1 ns\nPregnancy rate/ ET (%) 48.4 44.1 40.1 ns\nImplantation rate (%) 24.2 24.6 22.1 ns\nLive-birth rate/ET (%) 34.6 25.8 30.8 ns\n1Group A vs Group B, 2Group B vs Group C, 3Group A vs Group C, ns: not significant.\nBongioanni et al . Reproductive Biology and Endocrinology 2011, 9:81\nhttp://www.rbej.com/content/9/1/81\nPage 4 of 6\n\nwomen required a higher FSH dose and a longer stimu-\nlation, obtained less oocytes and finally had similar IVF\noutcome as women with in situ endometriomas.\nSomigliana [14] reported that women operated for bilat-\neral endometriotic ovarian cysts and subsequently sub-\nmitted to IVF had a higher withdrawal rate for poor\nresponse, retrieved less oocytes despite the use of higher\ndoses of gonadotropins, and had significantly lower\npregnancy and delivery rate s than non-endometriotic,\nnever operated on the ovary, controls.\nIn conclusion, with the limitations of a retrospective\nstudy we show herein that the presence of ovarian endo-\nmetriosis is not a cause of poorer IVF outcome and that\nlaparoscopic stripping before IVF does not improve out-\ncome. On the contrary, the operation may reduce ovar-\nian reserve and increase the need for exogenous\nhormones to retrieve an adequate number of oocytes,\nthus increasing the overall cost of the treatment. Our\nobservations, in line with most recent data, add evidence\nagainst laparoscopic ovarian surgery for endometriomas\nin asymptomatic patients who are candidates for IVF.\nAuthor details\n1LIVET Infertility and IVF Clinic, Torino, Italy. 2Reproductive Medicine and IVF\nUnit, Department of Obstetrical and Gynecological Sciences, University of\nTorino, OIRM-S, Anna Hospital, Torino, Italy.\n3Carl von Linne ’ Clinic, Uppsala,\nSweden.\nAuthors’ contributions\nFB, DG and LDP collected the data and provided the first draft of the\nmanuscript. GG participated in the design of the study and performed the\nstatistical analysis. AR and JH conceived of the study, participated in its\ndesign and coordination, and helped to draft the manuscript. All authors\nread and approved the final manuscript.\nCompeting interests\nThe authors declare that they have no competing interests.\nReceived: 16 February 2011 Accepted: 17 June 2011\nPublished: 17 June 2011\nReferences\n1. Somigliana E, Vercellini P, Viganó P, Ragni G, Crosignani PG: Should\nendometriomas be treated before IVF-ICSI cycles? Hum Reprod Update\n2006, 12:57-64.\n2. Vercellini P, Somigliana E, Viganò P, Abbiati A, Barbara G, Crosignani PG:\nSurgery for endometriosis-associated infertility: a pragmatic approach.\nHum Reprod 2009, 24:254-269.\n3. Garcia-Velasco JA, Somigliana E: Management of endometriomas in\nwomen requiring IVF: to touch or not to touch. Hum Reprod 2009,\n24:496-501.\n4. Barnhart K, Dunsmoor-Su R, Coutifaris C: Effect of endometriosis on in\nvitro fertilization. Fertil Steril 2002, 77:1148-1155.\n5. 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Muzii L, Bellati F, Bianchi A, Palaia I, Manci N, Zullo MA, Angioli R, Panici PB:\nLaparoscopic stripping of endometriomas: a randomized trial on\ndifferent surgical techniques. Part II: pathological results. Hum Reprod\n2005, 20:1987-1992.\ndoi:10.1186/1477-7827-9-81\nCite this article as: Bongioanni et al .: Ovarian endometriomas and IVF: a\nretrospective case-control study. Reproductive Biology and Endocrinology\n2011 9:81.\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\nBongioanni et al . Reproductive Biology and Endocrinology 2011, 9:81\nhttp://www.rbej.com/content/9/1/81\nPage 6 of 6","source_license":"CC0","license_restricted":false}