Akiko Takashima, Naoki Takeshita, Kiwamu Otaka and Toshihiko Kinoshita

bs_bs_banner doi:10.1111/jog.12056 J. Obstet. Gynaecol. Res. Vol. 39, No. 7: 1246 1252, July 2013 Effects of bipolar electrocoagulation versus suture after laparoscopic excision of ovarian endometrioma on the ovarian reserve and outcome of in vitro fertilization Akiko Takashima, Naoki Takeshita, Kiwamu Otaka and Toshihiko Kinoshita Department of Obstetrics and Gynecology, Toho University Medical Center Sakura Hospital, Chiba, Japan Abstract Aim: The aim of this study was to assess the effect of coagulation versus suture used for hemostasis during laparoscopic excision of a unilateral endometrioma for outcome of in vitro fertilization (IVF). Material and Methods: This retrospective study was set in a university hospital. A total of 44 sterile patients underwent laparoscopic excision of a unilateral ovarian endometrioma. Bipolar electrocoagulation was performed for hemostasis in 21 patients and the remaining 23 patients underwent suturing. Samples of blood were taken on day 3 of menstruation before the operation. Serum levels of anti-müllerian hormone, folliclestimulating hormone and estradiol were measured. Number of antral follicles, follicular flushings, oocytes retrieved, and embryos were counted and the outcomes of IVF were recorded. Results: No significant differences in the serum levels of any of the hormones were found between the preand postoperative samples, in either group. The mean antral follicle count, number of follicular flushings, oocytes retrieved and embryos obtained were significantly lower in the treated ovary as compared with the corresponding values in the contralateral intact ovary in the suture group. The pregnancy rates were similar in the two groups. Conclusions: There was no difference in the outcome of IVF between the two different methods of hemostasis. Key words: assisted reproductive technology, clinical, endometriosis, endoscopy, ovarian function, reproductive endocrinology, infertility. Introduction Endometriosis is a disorder characterized by the presence and growth of endometrial tissue in ectopic sites. While the reported prevalence among asymptomatic women ranges from 2 to 20%, that in women with dysmenorrhea is as high as 40 60%. 1 Several studies have suggested that the presence of endometrioma impairs the oocyte quality, as reflected by the reduced rate of fertilization and implantation after controlled ovarian hyperstimulation (COH) and in vitro fertilization (IVF) treatment. 2,3 A previous study demonstrated that operative laparoscopy improved the IVF outcomes after ovarian cystectomy and treatment of endometriosis as compared with that in matched controls. 4 Therefore, laparoscopic excision of endometrioma has been established as the gold-standard surgical approach for the treatment of patients presenting with subfertility. Laparoscopic surgery of endometrioma in experienced hands is currently the most valid approach. While one of the surgical procedures for ovarian endometrioma is fenestration and electrocoagulation of the cyst wall, another is cystectomy. In a randomized study, Beretta Received: August 13 2012. Accepted: December 18 2012. Reprint request to: Dr Akiko Takashima, Department of Obstetrics and Gynecology, Toho University Medical Center Sakura Hospital, 564-1 Shinoshizu, Sakura, Chiba 285-0841, Japan. Email: akotakashi@aol.jp 1246 2013 The Authors

Coagulation versus suture for hemostasis et al. 5 found that the recurrence rate was higher and the pregnancy rate was lower after fenestration and electrocoagulation than after excision. Accordingly, excision of ovarian endometrioma is routinely performed worldwide; however, several studies have suggested that excision of ovarian endometrioma is followed by a reduced number of oocytes and a high percentage of unresponsive ovaries to gonadotrophin stimulation. 6,7 It appears that surgical removal of endometriomas may exert a negative effect on fertility. Conversely, there is also a general consensus that the pregnancy rate is not significantly affected. 7 The precise effect on the ovarian reserve of different types of surgery for endometrioma is yet to be clarified. The appropriate choice of laparoscopic technique in the surgical management of endometrioma for obtaining better responses to COH remains controversial. Therefore, it is still necessary to assess which might be more beneficial, coagulation or suture for hemostasis in women undergoing laparoscopic excision of endometrioma. Relevant evidence is, however, still scarce. Accordingly, the aim of the present study was to evaluate and compare the short-term outcomes, including the ovarian reserve and outcomes of IVF, in women undergoing endometrioma excision by different laparoscopic techniques. Methods Subjects The study was conducted from April 2008 to December 2010 at Toho Medical Center Sakura Hospital, Japan. The study was conducted with the approval of the Research and Ethics Board of the hospital. We examined the medical records of patients who had undergone laparoscopic excision of ovarian endometrioma followed by IVF treatment. Participants of the study were 44 women who had laparoscopic excision for unilateral endometrioma from among infertile women aged 32 40 years who consulted the hospital. Hemostasis during the surgery was achieved by coagulation in 21 patients, and by suture in the remaining 23 patients. Patients were randomized in two types of hemostatic technique. Patients undergoing hyperstimulation for their first IVF session were recruited for the study 3 months after the operation. Besides endometriosis, other infertility investigations were within normal limits. In this analysis, the indications for IVF were defined before surgery. A large number of patients, especially when age is a factor, opt to proceed with IVF, without undergoing spontaneous conception. None of the patients had taken any hormonal treatment preparations within at least 1 year prior to the laparoscopy. All met the following inclusion criteria: (i) no previous history of adnexal surgery; (ii) both ovaries present; (iii) menstrual cycle length range between 25 and 35 days; (iv) no clinical signs of hyperandrogenism; and (v) body mass index (BMI) in the range of 18 25 kg/m 2. Written informed consent from all patients was obtained. Laparoscopic procedure All laparoscopic operations were performed by the first author. Laparoscopy was performed under general anesthesia. We use diluted vasopressin (10 IU/100 ml of normal saline) to dissect the cyst wall off the ovarian stroma to minimize destruction of healthy ovarian tissue. Adhesions between the cyst and the lateral pelvic wall were lysed and the cyst was mobilized. Excision of ovarian endometrioma was performed by stripping the cyst wall from the surrounding normal ovarian tissue using two atraumatic grasping forceps by traction and countertraction, after identification of cleavage plane. After removal of the cyst wall, the bleeding ovarian wound base was rinsed with saline. Hemostasis after stripping was performed using bipolar energy in the coagulation mode set at 40 W and exposure time limited to 1 s for each site in the coagulation group. The fascia was sutured with intermittent 2-0 monofilament in the suture group. In the group in which hemostasis was achieved by suturing, all bleeding was resolved by suturing only. Sutures were made for the closure of ovarian parenchyma and bleeding control. Hemostatic procedures were minimized to the extent possible. Staging of endometriosis was performed according to the revised classification of the American Society for Reproductive Medicine (ASRM). 8 Measurement of the serum hormone concentrations Samples of blood (5 ml) were taken on menstruation day 3 before operation and before IVF cycle 3 months after the surgery, and centrifuged, and the resultant sera were frozen at -80 C until subsequent assay for anti-müllerian hormone (AMH), FSH and estradiol (E2). The serum hormone levels were determined using appropriate enzyme-linked immunosorbent assay kits. 2013 The Authors 1247

A. Takashima et al. Cycle monitoring The numbers of early antral follicles were assessed by ultrasound examination on day 3 for IVF. Ultrasonographic measurements were performed using a 5.0 9.0-MHz multi-frequency transvaginal probe (Aloka SSD-1000 with multifrequency convex endovaginal transducer UST-9112-5) according to a previously described methodology. 9 In brief, on day 3, all antral follicles measuring 2 10 mm in mean diameter were carefully counted in the treated ovary and the contralateral intact ovary. All subjects were treated by a standard treatment protocol-fsh ovarian hyperstimulation using GnRH short antagonist with human chorionic gonadotrophin (hcg) induction of follicular maturation 36 h before the collection of the eggs. The appropriate FSH dose was chosen individually according to the antral follicle count and monitoring of the growing follicles. The number and size of follicles responding to FSH stimulation were regularly monitored by transvaginal sonographic measurements. The growing follicle count used in this study was that measured on the day of oocyte pickup and included all follicles >17 mm in diameter. Embryo transfer was performed 72 h after the oocyte collection. Pregnancy was defined as a positive serum b-hcg result. Clinical pregnancy was defined as the ultrasonographic demonstration of an intrauterine gestational sac 4 weeks after the embryo transfer. The ovarian response was assessed by parameters such as the total dose of gonadotrophin (recombinant FSH [rfsh] or human menopausal gonadotrophin [hmg]) required for ovarian stimulation, the number of follicles on the day of oocyte pickup, the number of oocytes retrieved and the number of embryos obtained from the treated ovary and the contralateral intact ovary. Statistical analysis The concentration data and calculated indices in each group are expressed as arithmetic means SD. The c 2 or Fisher s exact test were used for comparison of categorical variables. The resultant data were tested for statistical significance using the Student s t-test and the Wilcoxon Mann Whitney U-test. P-values < 0.05 were considered to be statistically significant. Measurements The age, BMI, menstrual cycle duration, tumor size, and revised ASRM (rasrm) score at laparoscopic surgery were recorded as the baseline clinical characteristics of the patients. In addition, the pre- and postoperative serum AMH, FSH and E2 levels of all the patients enrolled in this study were determined. Patients undergoing hyperstimulation for their first IVF session were recruited for the study 3 months after the operation. We evaluated and compared the number of AFC, number of follicular flushings, number of oocytes retrieved, and number of embryos obtained from the treated ovary as well as the contralateral intact ovary in both groups. The total doses of rfsh/hmg, duration of stimulation, pregnancy rate and clinical pregnancy rate were recorded. Results A total of 44 patients underwent laparoscopic excision of endometrioma. The patient and endometrioma characteristics in both groups are summarized in Table 1. At the time of the surgery, the patients age, BMI and menstrual cycle duration were similar between the two groups. There were no significant differences between Table 1 Baseline clinical characteristics of patients who underwent surgery for endometrioma Variable Coagulation (n = 21) Suture (n = 23) P-value Age (years) 35.35 1.57 36.23 1.89 NS BMI (kg/m 2 ) 20.45 0.74 20.42 0.97 NS Menstrual cycle (day) 29.90 1.16 29.82 1.14 NS Size of cyst (cm) 6.20 0.67 6.70 0.90 NS rasrm score 40.10 7.57 49.30 9.37 NS Values are mean SD. BMI, body mass index; NS, not significant; rasrm, revised American Society for Reproductive Medicine. 1248 2013 The Authors

Coagulation versus suture for hemostasis the two groups in the operative findings, such as the rasrm score or size of the endometrioma. Comparisons of the preoperative and postoperative serum hormone concentrations are presented in Table 2. All patients had normal serum FSH levels preoperatively. There were no significant differences in the serum AMH, FSH and E2 concentrations measured preoperatively between the two groups. Small differences in the serum AMH levels measured preoperatively were observed between the two groups; however, no statistically significant decrease in the postoperative serum AMH level was observed in either group. No significant differences between the preoperative and postoperative FSH or E2 levels were found in either group. The IVF cycle characteristics are shown in Tables 3 and 4. The mean number of AFC, number of follicular flushings, number of oocytes retrieved and number of embryos obtained were significantly lower for the treated ovary as compared with that of the contralateral intact ovary in the suture group (1.7 0.7 vs 3.4 1.3, P = 0.0299; 1.5 0.7 vs 3.4 1.6, P = 0.0136; 0.9 0.5 vs 2.4 1.2, P = 0.0330; 0.5 1.0 vs 1.4 0.7, P = 0.0314). The number of AFC, number of follicles and number of retrieved oocytes during ovarian hyperstimulation for the treated ovary were not markedly different between the two groups. The total dosage of rfsh/hmg, duration of stimulation, pregnancy rate and clinical pregnancy rate were comparable between the groups. Discussion Laparoscopic ovarian surgery is a major topic in the field of reproductive medicine. Different surgical techniques have been reported and evaluated. Laparoscopic excision of ovarian endometrioma has been reported to be associated with detrimental effects on the ovarian reserve, at least immediately after the surgery. 10 It was reported that reduced ovarian reserve after excision of ovarian endometrioma is observed in both natural Table 2 Serum hormonal concentrations between two groups pre- and post-surgery Coagulation Suture Pre Post P-value Pre Post P-value AMH (ng/ml) 3.25 1.16 3.16 1.27 NS 3.48 0.91 2.88 0.83 NS FSH (IU/L) 5.01 0.99 5.47 1.53 NS 4.55 0.80 5.02 0.86 NS E2 (IU/L) 36.2 1.34 42.1 18.7 NS 43.3 12.2 53.9 8.9 NS Values are mean SD. AMH, anti-müllerian hormone; E2, estradiol; FSH, follicle-stimulating hormone; NS, not significant. Table 3 Comparison of number of follicles in the treated ovary and in the non-treated contralateral ovary during ovarian hyperstimulation for IVF Coagulation Suture Treated Non-treated P-value Treated Non-treated P-value Antral follicle count 2.7 0.9 3.3 1.3 NS 1.7 0.7 3.4 1.3 <0.05 Number of follicular flushings 3.4 1.6 4.4 2.5 NS 1.5 0.7 3.4 1.6 <0.05 Number of oocytes retrieved 1.7 0.9 2.5 1.4 NS 0.9 0.5 2.4 1.2 <0.05 Number of embryos obtained 1.2 0.9 1.7 0.9 NS 0.5 1.0 1.4 0.7 <0.05 Values are mean SD. IVF, in vitro fertilization; NS, not significant. Table 4 Characteristics of in vitro fertilization cycles in patients who underwent surgery for endometrioma Coagulation Suture P-value Dosage of rfsh/hmg 1442.8 300.8 1606.3 172.9 NS Duration of stimulation (day) 13.14 1.02 13.39 0.56 NS Pregnancy rate (%) 33.33 30.43 NS Clinical pregnancy rate (%) 23.81 21.74 NS Values are mean SD. hmg, human menopausal gonadotrophin; NS, not significant; rfsh, recombinant follicle-stimulating hormone. 2013 The Authors 1249

A. Takashima et al. and stimulated cycles. 11 13 Previous studies have demonstrated that both the number of follicles and number of oocytes retrieved during ovarian hyperstimulation were markedly reduced for the treated ovary as compared with those for the contralateral intact ovary. 7,13 Despite damaging the ovarian response, a recent meta-analysis showed that excision of endometrioma had no significant effect on the pregnancy rate. 14 At present, the commonly accepted view is that ovarian endometrioma and its surgical treatment may cause quantitative, but not qualitative injury to the ovarian reserve. 7,13 Various indicators have been used in both natural and stimulated cycles, including AMH, cycle-day-3 FSH, AFC and different indexes of IVF outcome. AMH is a glycoprotein that is exclusively produced by the granulosa cells of the ovarian follicles in female adults; 15 it is a potential biomarker of ovarian reserve that may predict the number of responsive follicles. The strong relation between the serum AMH levels and the number of antral follicles supports the use of AMH measurements as a quantitative marker of the ovarian follicular status. 16,17 Serum basal AMH levels may be positively correlated with the ovarian response to IVF treatment, therefore, serum AMH appears to be strongly correlated with the number of retrieved oocytes. 18 In our study, no statistically significant differences were observed between the mean pre- and postoperative AMH levels in either group. The mean AMH level in the suture group decreased from 3.48 0.91 presurgery to 2.88 0.83 post-surgery; however, this reduction was not statistically significant (P > 0.05). Several studies have demonstrated significant decreases in the postoperative serum AMH levels at 1 month after surgery as compared with the preoperative levels in both patients with and without endometrioma. 10,19 In one study, the serum AMH levels decreased significantly until day 7 after laparoscopic cystectomy and thereafter increased gradually to recover to about 65% of the preoperative level by 3 months after the surgery. 20 Our present study is one of the few to have analyzed the serum levels of AMH until 3 months after ovarian surgery and our results suggest that the ovarian dysfunction occurring after surgery may recover by 3 months after surgery. This is consistent with results of a small study, which was concluded from 44 cases studied for just 3 months. Our sample size was also relatively small, and it will therefore be necessary to investigate with a larger number of patients. Basal FSH and E2 levels have been widely accepted and used as markers of ovarian reserve. 21 In our present series, no significant increase of the basal FSH or E2 levels was observed postoperatively. AFC can be used as a direct quantitative marker of ovarian reserve as assessed histologically by counting the number of ovarian primordial follicles. 22 The number of oocytes retrieved after ovarian stimulation is related to the number of oocytes remaining in the ovary. The results of our study show that AFC, number of follicular flushings, and number of oocytes retrieved were all significantly lower for the treated ovary than for the contralateral intact ovary in the suture groups. This finding implies that the suturing procedure can cause quantitative injury to the ovarian reserve. We speculate the following possible causes of the decreased ovarian reserve. First, a potential deleterious mechanism is the accidental removal of a substantial amount of ovarian tissue during cystectomy. It has been reported that removal of ovarian cysts that have well-defined ovarian capsules (dermoid, serous and mucinous cysts) result in some ovarian tissue being removed in 6% of the cases. 23 On the other hand, a small rim of tissue containing primordial follicles is removed in more than 50% of cases undergoing excision of endometriomas. 24 Second, the ovary could be directly damaged by the electrosurgical coagulation or suture employed for hemostasis. After stripping of the cystic wall, the subsequent bleeding of the ovarian stromal wound base is usually controlled by bipolar electrocoagulation or suturing. Potentially, surgery-induced ovarian tissue damage can be increased by both heat and sutures. Even gentle bipolar electrocoagulation of the wound base can potentially harm the surrounding healthy ovarian tissue. 25 In contrast, sutures produce additional damage of healthy tissue, and an increase of intraovarian pressure with ischemic regions can result. Therefore, gentle and careful bipolar coagulation or careful suture is of paramount importance for achieving hemostasis after stripping of the cyst capsule during cystectomy. Third, other mechanisms that may be responsible for the reduced ovarian reserve could be damage to the ovarian vasculature and inflammation-mediated injury resulting in the loss of healthy ovarian follicles. 13 Previous studies have demonstrated that suturing for hemostasis was associated with a more favorable outcome in respect to the ovarian reserve 25 27 and postoperative ovarian adhesion formation, 28 than bipolar electrocoagulation; however, our data do not lend 1250 2013 The Authors

Coagulation versus suture for hemostasis support to this conclusion. A probable reason is the use of different laparoscopic techniques between our studies. In our procedure, we injected diluted vasopressin into the space between the cyst wall and the normal ovarian cortex; the vasopressin effect reduced oozing from the ovarian cortex. In addition to the vasoconstrictive effect of vasopressin, as a result of the hydrodissection effect, the injection administered into the appropriate layer also facilitated clearer detection of the boundary between the cyst wall and the normal ovarian tissue. 29 The relative ease of removal capsule is also associated with loss of bleeding. This procedure may avoid coagulation of the remaining ovarian stroma and the ovarian hilus to possibly reduce the extent of damage to the normal ovarian tissue. The bipolar electrosurgical coagulation might damage the ovarian vascular system, but ischemic damage induced by suturing is far more extensive and irreversible. Some authors have reported severe complications after the administration of vasopressin. As endogenous vasopressin levels sometimes rise during laparoscopy, patients may become susceptible to the drug s effects, and appropriate precautions must be taken. Although vasopressin is used to decrease blood loss during surgery in various clinical fields, in this analysis, the overall evaluation of the patients was not compatible with having a significant effect on systemic circulatory dynamics. Our data show that suturing, as compared to bipolar electrocoagulation, for hemostasis after laparoscopic stripping of endometrioma exerted greater damage on the quantitative ovarian reserve, even though the pregnancy rate was not significantly affected. This is the first report to evaluate and compare the outcomes of IVF in women following excision of endometrioma by different laparoscopic techniques. We concluded that there were no significant differences in the IVF outcomes in response to COH cycles depending on the laparoscopic technique used for hemostasis in patients undergoing excision of unilateral endometrioma. The present study results, however, did not clarify whether the damage to the ovaries resulting from the operative treatment was transitory or permanent. Despite the limited number of postoperative trials and short follow-up intervals, this study demonstrated that coagulation is more beneficial than suture for hemostasis during endometrioma excision in order to minimize damage to the normal ovarian parenchyma. 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