{"paper_id":"326899da-eefb-4b49-99c7-15838b977949","body_text":"ORIGINAL ARTICLE\nUnilateral versus bilateral adnexal disease in stage III\nand stage IV endometriosis does not affect pregnancy\noutcome after operative laparoscopy\nMostafa Abuzeid & Abeer Ahmed & Khaled Sakhel &\nRiham Alwan & Mohammad Ashraf &\nMohammed Mitwally & Michael Diamond\nReceived: 14 April 2008 / Accepted: 27 June 2008 / Published online: 23 August 2008\n# Springer-V erlag 2008\nAbstract To study the effect of unilateral versus bilateral\nadnexal involvement on the pregnancy rate after operative\nlaparoscopy. Historic cohort study. A total of 143 patients\nwith advanced stages of endometriosis (stage III and IV)\nwho underwent operative laparoscopy for infertility treat-\nment were categorized into those with unilateral versus\nbilateral adnexal disease. Forty-three patients had primarily\nunilateral (group 1) and 100 had bilateral disease (group 2).\nFollow-up was up to 2 years. There was no significant\ndifference between group 1 and group 2 with respect to\npregnancy rates (28% vs 31%), delivery rates (21% vs\n23%), miscarriage rates (25% vs 13%), and ectopic rates\n(0% vs 13%). Cumulative conception rates after up to 24\ncycles of natural intercourse and up to three IUI cycles were\n59% and 49% for group 1 and group 2, respectively.\nOperative laparoscopy for advanced stages of endometriosis\nappears to be an effective treatment modality for establishing\na pregnancy in infertile patients. Pregnancy and delivery\nrates are not different in patients with unilateral or bilateral\nadnexal involvement.\nKeywords Advanced endometriosis . Pregnancy outcome .\nLaparoscopic surgery . Unilateral . Bilateral\nIntroduction\nAlthough stage III and IV endometriosis suggest advanced\ndisease, endometrial implants and adhesions are frequently\nnot symmetrically distributed in the pelvis [ 1] allowing for\nthe possibility that one adnexa may be relatively free of\nmechanical factors of infertility. The fact that one adnexa\nmay have less disease may positively influence the\npregnancy rate reported as a result of surgical treatment of\nadvanced endometriosis. That is to say, the pregnancy\noccurs as a result of ovulation/tubal ovum pickup from the\nside with less adnexal pathology. However, in such cases\nthe resulting pregnancy may be due to the effect of ablation\nof endometrial implant, as in patients with minimal or mild\nendometriosis [2]. If such a hypothesis is true, the pregnancy\nrate should be much less in patients with bilateral adnexal\ninvolvement. To examine this hypothesis, we therefore\nstudied the effect of unilateral versus bilateral adnexal\ninvolvement on the pregnancy rate after operative laparos-\nGynecol Surg (2009) 6:39 –44\nDOI 10.1007/s10397-008-0420-z\nSupport: None\nM. Abuzeid ( *) : M. Ashraf\nDivision of Reproductive Endocrinology and Infertility,\nDepartment of OB/GYN,\nHurley Medical Center,\nFlint, MI, USA\ne-mail: reprod1@hurleymc.com\nM. Abuzeid\n: M. Ashraf\nCollege of Human Medicine,\nMichigan State University,\nE Lansing, MI, USA\nA. Ahmed\nDepartment of OB/GYN,\nHurley Medical Center,\nFlint, MI, USA\nM. Abuzeid\n: K. Sakhel : R. Alwan : M. Ashraf\nIVF Michigan PC,\nRochester Hills, MI, USA\nM. Mitwally\n: M. Diamond\nDivision of Reproductive Endocrinology and Infertility,\nWayne State University,\nDetriot, MI, USA\n\ncopy for infertile patients with advanced endometriosis. We\nalso studied the pregnancy and delivery rates in these two\ngroups and in the total population after different infertility\ntreatment methods were used.\nMaterials and methods\nThis is a retrospective historical cohort study conducted\nafter obtaining approval by the local institutional research\nboard of Wayne State University. The study was conducted\nat a private infertility center (IVF Michigan). All patients\nwith advanced stages of endometriosis (stage III and IV)\nwho underwent operative laparoscopy for infertility treat-\nment between April 1993 and December 2003 were\nstudied. Endometriosis was staged at the time of surgery\naccording to the revised American Fertility Society classi-\nfication (rAFS) [ 3]. Patients whose husbands had severe\nmale factor (count less than 10 million/ml, and/or motility\nless than 20%, and/or very poor morphology) and patients\nwith cycle day 3 FSH level higher than 12 mIU/ml were\nexcluded. Patients with past history of pelvic inflammatory\ndisease (PID), history of sexually transmitted disease and/or\npositive Chlamydia trachomatis serology (IgG/IgM) were\nexcluded. A total of 143 consecutive patients who satisfied\nthe criteria were included in our study. Patients were\ncharacterized into those with unilateral versus bilateral\nadnexal disease. Adnexal disease was defined as mechan-\nical distortion of the adnexa due to the presence of deep-\nseated endometrioma(s) and/or adhesions of the ovary to\nthe ovarian fossa and/or extensive peritubal and/or peri-\novarian adhesions. Unilateral disease was defined as similar\nanatomical distortions mechanically affecting only one\nadnexa. Superficial implants of the opposite adnexa, in\nthe absence of adhesions or endometrioma(s), did not\ndisqualify a patient as having primarily unilateral disease.\nPatients designated as being in the bilateral group had\nsignificant ovarian and/or tubal pathology distorting both\nadnexae. Using these criteria, 43 patients had primarily\nunilateral and 100 had bilateral disease.\nSurgery was performed by the same surgeon (M. I. A.)\nunder similar operative setting in all patients. The same\nsurgical techniques and procedures were applied in all\npatients. When suspicious spots of endometriosis were\nfound anywhere in the pelvis, in the majority of cases,\nargon beam coagulator (Birtcher Medical System, Irvine,\nCA, USA) was used to ablate the spots seen. If endome-\ntriosis was found on the pelvic sidewall near the ureter, on\nthe bladder or bowels, CO\n2 laser (Sharplan Lasers, Inc.,\nAllendale, NJ, USA) vaporization was performed.\nSalpingo-ovariolysis was performed using blunt dissection\nof the ovary from the pelvic sidewall, and scissors and/or\nmonopolar diathermy needle tip to excise scar tissue from\nthe tubes and ovaries. If an endometrioma of more than\n1 cm was found, excision of the cyst wall was done and\nreconstruction of the ovarian cortex was performed with\none or two interrupted sutures using 3-0 Vicryl. If an\nendometrioma of less than 1 cm was found, it was opened,\nevacuated, and the lining was ablated with the argon beam\ncoagulator. If fimbrial phimosis or hydrosalpinges were\nfound, fimbrioplasty or salpingostomy was performed,\nrespectively. Starting in 1999, temporary ovarian suspen-\nsion was performed when laparoscopic surgery was\nperformed for advanced endometriosis in an attempt to\nreduce the risk of recurrence of adhesions between ovarian\nfossa and ovaries [ 4].\nFollowing surgery, Clomid was given to patients with\nanovulatory disorder. Intrauterine insemination (IUI) after\ncontrolled ovarian hyperstimulation (COH) was performed\nif male factor or ovulatory disorder resistant to Clomid (not\nresponding by ovulation) was present, or after 6 months of\nnatural intercourse. Some patients opted to start infertility\nintervention in the form of COH+IUI or in vitro fertiliza-\ntion and embryo transfer (IVF-ET) directly after surgery.\nDuring IUI, ovarian hyperstimulation was achieved\nusing mid-luteal gonadotropin-releasing hormone agonist\n(GnRH-a) pituitary down regulation followed by gonado-\ntropin injections starting on the second or third day of the\nmenstrual cycle. Ten thousand units of human chorionic\ngonadotropin (hCG) was given when the dominant follicle\nreached a diameter of 17 mm, and IUI was performed\n42 h later. For IVF/ET, controlled ovarian hyperstimulation\nwas applied according to a long GnRH-a pituitary down\nregulation protocol. In the first few years of this series,\ntraditional IVF was performed. However, intracytoplasmic\nsperm injection (ICSI) was performed in all patients in the\nlast 5 years of this series.\nIn all patients studied, we calculated endometriosis\nscores in five categories: cul-de-sac, peritoneum, ovaries,\ntubal, and grand total. After excluding patients who\nconceived with IVF-ET (in whom pregnancy is not\nsecondary to surgery), we compared these scores in patients\nwho conceived and those who failed to conceive in each\ngroup and in the total population studied. In addition, after\nexcluding 31 patients who conceived after IVF/ET, the data\nwere then analyzed with respect to the effect of the\nunderlying etiology.\nPregnancy was confirmed by vaginal ultrasonography\nand delivery verified by phone follow-up. Patients were\nfollowed until delivery if pregnant, or for a period of\n24 months following surgery if not pregnant. Data were\nexpressed as means±SD. Student ’s t-test, chi square\nanalysis, and Kruskal –Wallis one way anova analysis were\nused for statistical analysis where appropriate. Cumulative\nconception rate (CCR) was calculated using life table\nanalysis. To determine if there was any statistical signifi-\n40 Gynecol Surg (2009) 6:39 –44\n\ncance in CCR between the two groups, further survival\nanalysis was performed; the Kaplan –Meier survival analy-\nsis log rank test was used.\nResults\nThe mean age at laparoscopy was 31.8±4.5 years. The\nmean duration of infertility was 3.4±2.7 years. Table 1\nshows the demographic data of both groups. The two\ngroups did not differ significantly in age and duration of\ninfertility, although the latter approached significance with\na tendency for longer duration of infertility in the unilateral\ngroup. A significantly higher number of patients had\nprimary infertility in the unilateral group. In addition, there\nwere no significant differences in the underlying etiologies\nof infertility between the two groups. Of the patients\nstudied, 78 patients (55%) had primary infertility. Forty-\nthree patients (30.1%) had endometriosis as their sole cause\nof infertility and 100 patients (69.9%) had other infertility\nfactors (e.g., mild male factor or ovulatory disorder) in\naddition to endometriosis.\nTables 2, 3 and 4 illustrate pregnancy outcome after\nspontaneous conception, conception after IUI+COH, and\ncombination of the two methods, respectively. There was\nno significant difference in the pregnancy rates between the\nunilateral versus bilateral groups after spontaneous (19% vs\n21%), IUI+COH (40% vs 53%), and combined methods\n(28% vs 31%), respectively. In addition, there was no\nsignificant difference in delivery rates between the two\ngroups after spontaneous (14% vs 15%), IUI+COH (30%\nvs 42%), or combined (21% and 23%) conceptions,\nrespectively. Furthermore, there was no significant differ-\nence in miscarriage rates and ectopic pregnancy rates\nbetween the two groups, according to the method used to\nachieve conception. The overall conception rate, delivery\nrate, miscarriage rate, and ectopic pregnancy rate were\n20%, 15%, 17%, and 10% with spontaneous conception;\n42%, 38%, 14%, and 7% after COH+IUI; and 30%, 22%,\n16% and 9% after combined methods, respectively. There\nwere no significant differences in the CCR between\nunilateral versus bilateral groups after spontaneous concep-\ntion (53% vs 43%), IUI+COH (47% vs 81%), or combined\n(59% vs 49%), respectively.\nSome of the patients elected to proceed with IVF/ET\nshortly after surgery when they were told of the extent of\ntheir endometriosis. Others tried spontaneously and/or IUI+\nCOH for a few cycles before they decided to proceed with\nIVF/ET. Fifty-one patients underwent 75 cycles of IVF/ET\nduring the study period. There was no significant difference\nbetween the two groups in the pregnancy rate per patient\n(67% vs 58%), the delivery rate per patient (56% vs 49%),\nmiscarriage rate (8% vs 11%), and ectopic pregnancy rate\n(8% vs 5%), respectively.\nOf the 51 patients who underwent IVF/ET, 31 patients\nconceived. The pregnancy and delivery rates per patient\nwere 61% and 51%, respectively, while the miscarriage and\nectopic pregnancy rates were 10% and 7%, respectively.\nAfter excluding 31 patients who conceived after IVF-ET,\nthe data were then analyzed and the pregnancy outcome\nafter combined methods (spontaneous conception and IUI+\nCOH) were calculated. The pregnancy rate and delivery\nrate were 39% and 29% in the unilateral group, 38% and\n28% in the bilateral group and 38% and 29% in the total\npopulation, respectively. We also compared the pregnancy\nrates between the two groups according to the underlying\netiology. There was no significant difference in the\npregnancy rate in relation to the underlying etiology\nbetween the two groups. Above 50% of patients achieved\npregnancy and approximately 40% delivered in both groups\nwhen all possible infertility interventions were used. When\nall possible infertility tr eatment methods were used,\ncumulative conception rate and cumulative delivery rate\nafter 24 months were 66% and 62% for group 1, 69% and\n68% for group 2, and 76% and 67% for the total population\nstudied, respectively.\nWe compared endometriosis scores in patients who\nconceived and those who failed to conceive in the two\ngroups and in the total population after excluding patients\nwho conceived with IVF-ET. There was no significant\ndifference in the endometriosis score in the unilateral\ngroup, while in both the bilateral group and in the total\nTable 1 Demographic data\nUnilateral Bilateral P value Total\nNumber of patients 43 100 143\nAge 32.0±4.7 31.8±4.5 NS 31.8±4.5\nDuration of infertility 4.0±3.0 3.1±2.5 0.052 3.4±2.7\nType of infertility\nPrimary infertility 31 (72%) 47 (47%) <0.01 78 (54.5%)\nEtiology of infertility\nEndometriosis alone 8 (18.6%) 35 (35%) NS 43 (30.1%)\nEndometriosis plus other infertility factors 35 (81.4%) 65 (65%) NS 100 (69.9%)\nGynecol Surg (2009) 6:39 –44 41\n\npopulation there was significantly lower ovarian scores ( P=\n0.007 and P=0.001, respectively) and grand total scores ( P=\n0.001 and P=0.001, respectively) in the conceived versus\nnon-conceived. No difference was detected in the tubal\nscores among the unilateral group, bilateral group, and the\ntotal population.\nDiscussion\nAlthough endometriosis is present in 25 –50% of infertile\nwomen, [ 5, 6] the majority of these patients have early\nstages of endometriosis. Since mechanical factors interfer-\ning with ovum pick up play an important role in the\nmechanisms of infertility in patients with advanced stages\nof endometriosis, the majority of these patients require\neither surgical correction or IVF/ET to achieve pregnancy.\nMany studies reported very low cumulative conception rate\n(CCR) in patients with advanced stages of endometriosis\nwithout surgical treatment [ 7–10] compared to CCR in\npatients with early stages of endometriosis [ 11–13]. Olive\nand colleagues reported no pregnancies among women with\nsevere endometriosis with expectant management, as\ncompared to 52% with mild endometriosis and expectant\nmanagement during a 25-month follow-up [ 9]. In addition,\nseveral reports suggested good CCR after surgical treatment\nof advanced endometriosis both by laparotomy and lapa-\nroscopy [ 14–16]. Other reports suggested no difference in\nthe pregnancy outcome whether laparotomy or laparoscopy\nwas utilized. [ 14, 17]\nNow, for more than a decade, laparoscopy has become\nthe gold standard of conservative surgical treatment of\ninfertility patients with endometriosis [ 14–16]. It allows the\nsurgeon to reach a diagnosis and allows him/her to proceed\nwith treatment of endometriosis and/or adhesions at the\ntime of surgery. Improvement in fecundity rate and CCR\nhave been reported after laparoscopic surgical treatment for\ninfertile patients with both early [ 2] and advanced stages of\nendometriosis [ 14, –18]. However, none of these studies\nevaluated the effect of unilateral versus bilateral adnexal\ninvolvement on the chances of achieving pregnancy\npostoperatively.\nOur data indicate that surgical treatment for advanced\nendometriosis is effective even when bilateral adnexal\ninvolvement is present. Our results, with a CCR of 53%\nafter spontaneous cycles, are similar to the results reported\nby other investigators, which suggested that approximately\n50% of patients conceived after laparoscopic surgery for\nadvanced endometriosis [ 19]. In addition, our results are in\nagreement with others that laparoscopic surgery can\nimprove pregnancy rates in patients with advanced disease\n[18, 20]. In a recent report by Littman et al., of the 19\npatients with advanced stage of endometriosis, eight\nconceived (seven spontaneously and one after Clomid/\nIUI) [42%] [ 21]. In our study, when both spontaneous and\nIUI+COH methods of conception were used, we were able\nto achieve a CCR of 59%, 49%, and 52% for the unilateral\ngroup, bilateral group, and the total population studied,\nrespectively. However, our data also suggest that when\novarian endometriosis scoring is high in bilateral disease,\nthe chances are less favorable. It may partly explain the\ndifference in pregnancy rate after laparoscopic surgical\ncorrections of advanced endometriosis in various reports.\nBusacca et al. reported a cumulative conception rate of 51%\nand 17% after operative laparoscopy for stage III and IV\nendometriosis, respectively [ 22]. Similar to our data, this\nreport suggests the more advanced (higher scores), the less\nlikely the chances of pregnancy. Similarly, Adamson et al.\nTable 2 Pregnancy outcome after spontaneous conception\nNumber of patients Pregnant (%) Delivered (%) Miscarried (%) Ectopic (%) CCR a\nUnilateral 43 8 (19) 6 (14) 2 (25) 0 (0) 53%\nBilateral 100 21 (21) 15 (15) 3 (14) 3 (14) 43%\nTotal 143 29 (20) 21 (15) 5 (17) 3 (10) 46%\na Cumulative conception rate up to 24 months after surgery\nTable 3 Pregnancy outcome after IUI+COH\nNumber\nof patients\nNumber\nof cycles\nNumber\npregnant\nper cycle (%)\nNumber\npregnant\nper patient (%)\nNumber\ndelivered\nper cycle (%)\nNumber\ndelivered\nper patient (%)\nNumber\nmiscarried\n(%)\nNumber\nectopic (%)\nCCR\na\nUnilateral 10 19 4 (21) 4 (40) 3 (16) 3 (30) 1 (25) 0 (0) 47%\nBilateral 19 32 10 (31) 10 (53) 8 (25) 8 (42) 1 (10) 1 (10) 81%\nTotal 29 51 14 (28) 14 (42) 11 (22) 11 (38) 2 (14) 1 (7) 73%\na Cumulative conception rate up to 24 months after surgery\n42 Gynecol Surg (2009) 6:39 –44\n\nreported that extensive endometriosis with higher ASRM\nscore (>71), was associated with reduced pregnancy rates\n[23]. Other reports suggested that older patients and those\nwith stage IV did not conceive as often [ 19].\nIn one recent study, Maruyama [ 24] found that cumula-\ntive rates of pregnancy after laparoscopic treatment of\nendometriosis are about 35%. Maruyama found a signifi-\ncantly lower cumulative pregnancy rate in a group of\npatients with bilateral tubal adhesions compared with those\npatients with unilateral or no tubal adhesions. However, he\ndid not find a difference in the pregnancy outcomes of\nthose patients with minimal/mild endometriosis versus\nmoderate/severe endometriosis if the endometriosis did\nnot include tubal disease. This suggests that endometrial\nimplants resulting in mechanical factors interfering with\ntubal function may have a stronger impact on pregnancy\noutcome than the extent of endometrial disease as reflected\nmerely in staging. This may explain the relative success of\nlaparoscopic correction of mechanical factors in even those\npatients with severe stages of endometriosis. In our study,\nwhen we evaluated the effect of tubal involvement, we\ncould not find any significant difference between patients\nwho conceived and those who failed to conceive. Such\nfindings were maintained in both unilateral and bilateral\ngroups and also in the total population studied. We attribute\nsuch findings to the fact that we excluded from this study\nall patients who had history of PID and/or those who had\npositive serology for Chlamydia trachomatis . Since endo-\nmetriosis is a disease of the peritoneum, surgical correction\nof any tubal pathology in our patients may have a better\nprognosis than in patients with PID.\nOur data also suggest that IUI+COH can enhance\npregnancy chances after laparoscopic surgery for advanced\nendometriosis. In our study, approximately one-third of\npatients with advanced endometriosis were able to conceive\nwithin 2 years after operative laparoscopy as a result of\nspontaneous trials and/or IUI+COH. Other reports sug-\ngested similar results when IUI+COH was used after\noperative laparoscopy for early and advanced endometriosis\n[25–27]. Therefore, it could be offered for two to three\ncycles either immediately following surgery or after three to\nfour failed cycles of spontaneous trials.\nOur data suggest consistent excellent results of IVF-ET\nafter operative laparoscopy. Therefore, our result is in favor\nof the IVF-ET procedure after surgery for endometriosis.\nIVF-ET should be considered after operative laparoscopy\nwhenever there is marked bilateral ovarian involvement\nand/or failure of conception spontaneously, or after a few\ntrials of IUI+COH. In addition, it should be considered\nfrom the outset in patients with additional infertility factors;\ne.g., male factor, advanced female age, and prolonged\nduration of infertility. Recently, Littman et al. reported eight\nIVF pregnancies (five in patients with stage III or IV) in\npatients with endometriosis after operative laparoscopy\nwho had two failed IVF cycles on average. However, the\nliterature is not conclusive on this issue [ 28–30]. It is worth\nof note that ICSI is being utilized more frequently in these\npatients in view of reports of decreased fertilization rate\nafter traditional IVF/ET [ 29, 31, 32]. Some reports\nsuggested that ICSI can overcome apparent defects in\noocytes derived from endometriosis patients [ 33].\nHowever, our study has some limitations including its\nretrospective nature, the heterogenous group of patients\nstudied with the fact that only 30% of the patients had\nendometriosis as their only cause of infertility and the fact\nthat, following surgery, the patients were not carried\nforward in a similar manner. On the other hand, this study\nwas carried out by one surgeon at one unit and therefore,\nrepresents consistent management over the period of the\nstudy. In addition, it is extremely difficult to answer the\nquestion posed in this study by limiting the data to only\nthose with the single diagnosis of endometriosis. Further-\nmore, the fact that spontaneous pregnancy rate is similar in\nboth groups is very suggestive that laparoscopic surgical\ntreatment is as effective in the presence of bilateral adnexal\ninvolvement as in unilateral adnexal disease irrespective of\nthe presence of additional infertility factors.\nIn conclusion, the data in our study suggest that\nconservative laparoscopic surgery for advanced stages of\nendometriosis appears to be an effective treatment modality\nin patients with both unilateral and bilateral adnexal\ninvolvement. However, a large prospective study is needed\nto confirm our findings. In addition, IUI+COH may enhance\nchances of conception in patients with advanced endometri-\nTable 4 Pregnancy outcome after combined methods (spontaneous conception and IUI+COH)\nNumber\nof patients\nNumber\npregnant\nper patient (%)\nNumber\ndelivered\nper patient (%)\nNumber\nmiscarried (%)\nNumber\nectopic (%)\nCCR\na\nUnilateral 43 12 (28) 9 (21) 3 (25) 0 (0) 59%\nBilateral 100 31 (31) 23 (23) 4 (13) 4 (13) 49%\nTotal 143 43 (30) 32 (22) 7 (16) 4 (9) 52%\na Cumulative conception rate up to 24 months after surgery\nGynecol Surg (2009) 6:39 –44 43\n\nosis after operative laparoscopy. However, as expected, the\nmore advanced the disease, the lesser the likelihood of\npregnancy after surgical correction. Such patients should be\ncounseled to consider other opportunities including proceed-\ning with IVF-ET, which can achieve excellent results.\nAcknowledgments The abstract of this paper was presented in part\nat the Endometriosis 2000 7th Biennial World Congress, London, May\n14–17, 2000\nAbstract presented in part at the ASRM/CFAS meeting, Montreal\nCanada October 15 –19, Fertil Steril (84): Suppl 1, S198, Sept. 2005\nThe authors would like to thank Jenny LaChance for her assistance\nin statistical analysis and Cheryl Anderson for her assistance in the\npreparation of this manuscript.\nReferences\n1. Chapron C, Chopin N, Borghese B, Foulot H, Dousset B, V acher-\nLavenu MC, Vieira M, Hasan W, Bricou A (2006) Deeply\ninfiltrating endometriosis: pathogenetic implications of the ana-\ntomical distribution. Hum Reprod 21(7):1839 –1845\n2. 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