Long-term effects of bipolar electrocoagulation and suture hemostasis on the ovarian reserve following endometriotic cystectomy: a meta-analysis

The findings of the literature search are summarized in Fig.  1 . A total of 2,838 Chinese and English research articles were retrieved. After the removal of duplicates, 1,274 articles remained. Out of these 1,274 articles, 1,182 were excluded after screening the title, 66 were excluded after reading the abstract, and 18 were excluded after reading the full text. Finally, eight articles [ 5 , 12 – 18 ] were included in this meta-analysis, of which six were RCTs [ 5 , 12 , 15 – 18 ] and two were non-RCTs [ 13 , 14 ]. Seven papers [ 5 , 12 – 15 , 17 , 18 ] were published in English, and one [ 16 ] was in Chinese. All of the studies were published between 2012 and 2021 and had sample sizes ranging from 43 to 207 patients. We excluded the Takashima’s study [ 19 ] because it was a retrospective cohort study. In Zaitoun’s [ 20 ] study, two different surgical techniques—laparoscopic electrocoagulation and abdominal suture surgery—were compared. Consequently, the results are not directly comparable to those from studies involving laparoscopy alone, and this study was excluded from the analysis. Fig. 1 Flow chart of the selection for the study Flow chart of the selection for the study Table 1 summarizes the clinical and demographic characteristics of the patients treated with electrocoagulation or suture hemostasis. There was no statistically significant difference in the mean age of the patients, the average ovarian cyst size, and other clinical variables between the two groups. In the included studies, the AMH level was measured with enzyme-linked immunosorbent assay (ELISA). Table 1 Characteristics of the included studies Study Country Research type Time Detection method Unilateral/bilateral Number of patients(C/S) Mean age Mean cyst size Time of postoperative follow-up Ferrero 2012 Italy RCT 2007.6–2010.9 ELISA Bilateral 50 31.9 ± 4.0 7.4 ± 2.9 3 mo, 6 mo, 12 mo 50 32.1 ± 3.7 7.5 6 ± 2.4 Zahra Asgari 2015 Iran RCT 2014.2–2015.3 ELISA Unilateral 47 29.33 ± 6.91 5.72 ± 1.76 3 mo 45 29.7 ± 6.75 6.75 ± 2.07 Wang 2019 China Prospective cohort 2014.12–2017.8 ELISA Both 78 No significant difference No significant difference 1 mo, 3 mo, 6 mo, 12 mo 93 No significant difference No significant difference Zhang 2013 China RCT 2013.3–2013.9 ELISA Both 69 30.9 ± 8.2 5.2 ± 2.6 1 mo, 3 mo, 6 mo, 12 mo 69 33.1 ± 7.2 5.3 ± 2.7 Tanprasertkul 2016 Thailand RCT 2013.1–2013.12 ELISA Both 25 33.6 ± 5.2 5.4 + 2.0 1 mo, 3 mo, 6 mo 25 33.6 ± 6.6 5.0 + 1.6 Song 2015 Korea Prospective cohort 2011.10–2014.5 ELISA Both 62 31.2 ± 4.8 6.4 ± 1.6 3 mo 63 30.8 ± 5.2 6.8 ± 2.2 Egypt RCT 2008.4–2012.8 ELISA Unilateral 61 24.2 ± 3.1 Not mentioned 6 mo, 12 mo 60 25.2 ± 3.0 Not mentioned Li 2013 China RCT 2008.9–2010.2 ELISA Both 54 No significant difference Not mentioned 1 mo, 3 mo, 6 mo, 12 mo 54 No significant difference Not mentioned Araujo 2021 Brazil RCT 2018.3–2020.2 ELISA Unilateral 27 29.4 ± 6.9 6.0 ± 2.0 1 mo, 6 mo 26 30.9 ± 5.5 6.2 ± 2.3 RCT, randomized controlled trial; C, coagulation; S, suture Characteristics of the included studies 3 mo, 6 mo, 12 mo 1 mo, 3 mo, 6 mo, 12 mo 1 mo, 3 mo, 6 mo, 12 mo 1 mo, 3 mo, 6 mo 6 mo, 12 mo 1 mo, 3 mo, 6 mo, 12 mo 1 mo, 6 mo RCT, randomized controlled trial; C, coagulation; S, suture The randomization in the RCT was performed using either number tables ( n  = 3) or specialized software ( n  = 3). The distribution concealment was achieved through sealed opaque envelopes. Since it was not possible to perform a double-blinded trial, all RCTs included in the study were single-blind. All of the studies controlled for variables that could have introduced bias into the result. Based on the quality assessment illustrated in Fig.  2 , all RCTs were considered to provide high-quality evidence. Similarly, the two non-RCT studies had a NOS score above 7, indicating that the quality of the evidence of the prospective cohort studies was high (Table  2 ). Fig. 2 Quality evaluation of RCT. + : low risk; ?: Unclear; Table 2 Quality evaluation of cohort studies Selection (4 ※) Comparability (2 ※) Outcome (3 ※) Total score Quality Study Representativeness of the exposed cohort (※) Selection of the non-exposed cohort (※) Ascertainment of exposure (※) Demonstration that outcome of interest was not present at start of study (※) Comparability of cohorts on the basis of the design or analysis (※※) Assessment of outcome (※) Was follow-up long enough for outcomes to occur (※) Adequacy of follow-up of cohorts(※) Song 2015 ※ ※ ※ ※ ※※ ※ ※ ※ 9 Good wang 2019 ※ ※ ※ ※ ※ ※ ※ 7 Good Quality evaluation of RCT. + : low risk; ?: Unclear; Quality evaluation of cohort studies

This systematic review and meta-analysis were completed in strict accordance with PRISMA checklist. The review was conducted in accordance with a registered protocol (International Prospective Register of Systematic Reviews [PROSPERO]; PROSPERO number CRD42023472720). PRISMA checklist is provided in Table S1 . The databases PubMed, Cochrane Libraries, MEDLINE, EMBASE, Ovid, Web of Science, and Science Direct were searched for relevant articles published up to May 2023. The keywords and medical subject headings (MeSH) used for the search strategy were “Endometriosis”, “Cysts”, “Ovarian Cysts”, “Cystectomy”, “Hemostasis”, “Surgical”, “Ovarian Neoplasms”, “coagulation”, “Anti-Mmullerian Hhormone”, “Antimullerian”, “Hormones”, “Electrocoagulation”, “Hemostasis”, “Endoscopic”, “Ovarian Reserve”, “Suture Techniques” and “Sutures”. The references of relevant articles were also searched to retrieve additional studies. Two reviewers (J.W. and YX.W.) independently screened the potentially eligible studies. Any disagreements were resolved through discussion under the supervision of a third reviewer (HT.W.). Only full-length randomized controlled trials (RCT) and prospective studies published in English and Chinese comparing the preoperative and postoperative serum AMH levels after an endometriotic cystectomy with either bipolar electrocoagulation or suture hemostasis were included in this meta-analysis. Duplicate publications, case series, case reports, reviews, conference abstracts, editorials, and letters were excluded. In addition, the studies that did not report the patient eligibility criteria, surgical techniques, and enough data for extraction or calculation were excluded. Finally, studies that included female with clinical factors that may affect the OR were excluded, such as a history of polycystic ovarian syndrome, premature ovarian failure, low ovarian function, irregular menstrual cycle, having contraceptive pills, and hormone therapy up to 3 months before or after surgery, and those patients who have undergone prior ovarian surgery (e.g., oophorectomy or unilateral oophorectomy). The general study characteristics (first authors, publication years, study site and sample size); population characteristics (age, body mass index [BMI], and tumor size); hemostasis procedure (suture type and electrocoagulation device energy); and results (definition and time point measurements) were extracted from each study. For studies with incomplete data, we will contact the authors by email. The data extraction and quality assessment were carried out by J.W. and YX.W. using a pre-specified data collection form. Any disagreements were solved by consensus, and in case of persistent disagreement, a third reviewer was consulted (HT.W). The sample size, mean, and standard deviation (SD) were extracted for all continuous variables. If the studies reported the median rather than mean values and range or interquartile range rather than SD, the mean and SD were calculated [ 8 ]. This meta-analysis was conducted in accordance with the Meta-analysis Of Observational Studies in Epidemiology (MOOSE) guidelines [ 9 ]. The quality assessment of the RCTs was performed as indicated by the Cochrane Collaboration tool in the Cochrane Handbook [ 10 ]. On the other hand, the Newcastle–Ottawa Scale (NOS) was used to assess the quality of the non-RCTs [ 11 ]. The total NOS score for a study can range from 0 to 9 stars, with a higher score (> 7stars) indicating better methodological quality. Any disagreements were resolved through discussion under the supervision of a third reviewer (XM.L.). The meta-analysis was conducted using the Review Manager (RevMan) for Mac (version 5.4. Cochrane Collaboration, Oxford, England). The weighted mean difference (WMD) and 95% confidence interval (CI) were used to summarize the results of the continuous outcomes. The Cochrane’s Q test of heterogeneity and the I 2 statistic were used to assess the heterogeneity of the included studies. The I 2 score ranges from 0 to 100%. In cases where significant heterogeneity was present (indicated by a p -value < 0.10 and an I 2 value ≥ 50%), we employed a random-effects model for data analysis. Conversely, when heterogeneity was not significant, the fixed-effects model was utilized. At the same time, the sensitivity of confounding factors (unilateral cyst/bilateral cyst) was analyzed by subgroup analysis. Funnel plots were used to assess publication bias. In addition, Begg’s and Egger’s tests were performed to detect potential asymmetry in the funnel plots, which could indicate publication bias.

By updating the meta-analyses, it provides a comprehensive understanding of the effects of different hemostatic methods on OR during endometriotic cystectomy. The results indicate a trend of gradual recovery in anti-Müllerian hormone (AMH) levels in both the electrocoagulation and suture groups post-surgery. Compared with bipolar electrocoagulation, suture hemostasis has less impact on OR, and the difference was still statistically significant at 1 year after surgery. The assessment of the OR involves evaluating the quantity and quality of the remaining ovarian follicles. AMH is primarily produced by the granulosa cells of the preantral and small antral ovarian follicles. Therefore, the AMH levels indirectly represent the total number of ovarian follicles [ 21 , 22 ]. Compared with the other blood biomarkers, AMH is considered a better marker for OR because it remains very stable throughout the menstrual cycle [ 23 ]. In addition, it can also detect changes in the OR following gynecological surgeries early before the other indicators [ 24 ]. Therefore, the research using AMH as an indicator was included in this study. Various studies have evaluated the impact of surgical hemostatic methods on the OR [ 13 , 18 , 19 ]. Takashima et al. [ 19 ]and Tanprasertkul et al. [ 15 ] found no significant difference in the postoperative OR between the two surgical groups. Similarly, Urman et al. evaluated the serum AMH levels after unilateral ovarian cystectomy and found that its decline was not associated with the cauterization method [ 25 , 26 ]. Ferrero et al. [ 5 ] found no significant difference in the mean percentage decline in AMH levels between the electrocoagulation and suture groups at 3, 6, and 12 months following surgery. On the other hand, Wang et al. reported lower postoperative AMH levels in the suture group [ 14 ]. Asgari et al. [ 18 ] noted a faster decline in the AMH levels in the electrocoagulation group at 3 months postoperatively. Song et al. [ 13 ] also showed a faster reduction in serum AMH levels in ovarian endometrioma patients treated with electrocoagulation. Antral follicle count (AFC) determined via ultrasound was also used to evaluate ovarian reserve (OR). Studies using AFC as an indicator have reached conclusions consistent with those of the present study, suggesting that ovarian reserve is less diminished in ovaries treated with sutures than in those treated with electrocoagulation [ 6 ]. Due to the delayed response of AFC to postoperative changes, Zhang et al. [ 17 ] noted that no difference of AFC was observed at the 1st month and 3rd month ( p  > 0.05), whereas at the 6th month and 12th month, AFC in suture groups was obviously higher than that in electrocoagulation (p < 0.05). Deckers et al. [ 27 ]and Ata et al. [ 28 ] performed two meta-analyses comparing the impact of these surgical techniques on OR 3 months postoperative. However, their meta-analyses included fewer studies, did not consider the techniques that used to measure AMH and the clinical characteristics. Deckers’s results only measured AMH levels at 3 months postoperatively. And the study of Ata’s did not show any recovery of AMH levels 3 months after surgery. In this meta-analysis, all serum AMH levels were evaluated using the ELISA technique, and only studies with the same follow-up time points were combined for analysis. We aimed to evaluate the long-term effects of electrocoagulation and suture hemostasis surgical modalities on OR after full consideration of various covariates. In many previous studies [ 29 , 30 ], patients were followed up for only 3 months after surgery. The studies included in our meta-analysis had a follow-up of up to 1 year, allowing for a more comprehensive observation of long-term AMH changes. Comparisons of AMH levels at 1, 3, 6, and 12 months post-surgery revealed a trend of recovery in both groups; however, the damage caused by electrocoagulation group was greater than that caused by suture group at each time point, and the difference was still statistically significant at 1 year after surgery. These studies [ 14 , 16 , 17 ] exhibited low levels of heterogeneity (I 2  = 0%), and the results were consistent, which indicates that the findings are reliable. The strength of this review is that it not only compares the effects of the two hemostasis methods on OR, but also compares the trends of the effects of the two hemostasis methods on OR at different time points after 1 year of follow-up. We applied strict inclusion and exclusion criteria, including only RCT and prospective cohort studies and studies with adequate follow-up to ensure the best quality of evidence. Our meta-analysis has some limitations that have to be acknowledged. Various factors contributed to heterogeneity in the included studies. Most studies provided limited details on the energy, electrocoagulation duration, and number of solidification points. These factors may impact the severity of tissue damage following ovarian surgery. In addition, it is important to acknowledge that the surgeons’ experience may impact the tissue damage following surgery and, ultimately, the OR. However, only three studies provided information about the surgeon’s experience. The gynecologists in the studies of Tanprasertkul et al. [ 15 ] and Song et al. [ 13 ] performed more than 100 laparoscopic ovarian cystectomies. Zahra et al. [ 18 ] explained that the same team performed the surgical procedure but did not provide any information about the professional background of the surgeons. Finally, fewer studies were included in current analysis, and more high-quality RCTS are expected in the future. These findings highlight the importance of careful selection of electrocoagulation patients and the damage from electrocoagulation was still evident at 1 year after surgery. Future studies should focus on the risk factors of hemostatic methods on OR damage (electrocoagulation energy, electrocoagulation frequency, electrocoagulation time, suture thread type and number), and more high-quality, well-designed randomized controlled trials with long follow-up time are needed to fully evaluate. This knowledge can help develop prevention strategies for high-risk patients who have not had children. Suturing could be a better choice after stripping ovarian endometriomas.

Endometriosis is a chronic condition affecting about 176 million women worldwide in which the endometrial tissue with growth function is present outside the uterine cavity [ 1 ]. About 17–44% of patients with endometriosis develop ovarian cysts, filled with dark altered blood known as endometriomas [ 2 ]. Although these cysts are benign, they can cause severe pain and impair fertility. Maintaining the ovarian reserve (OR) is important for women of reproductive age. Hence, there is a growing necessity to gain a better understanding of the potential long-term consequences of ovarian surgery on subsequent fertility. The treatment for endometriomas remains controversial. According to a Cochrane systematic evaluation, endometriotic cystic wall resection has demonstrated in terms of reducing the recurrence of endometriomas and preserving ovarian function [ 3 ]. Various factors could contribute to reduced OR following surgery, including the disease itself and surgical procedure [ 4 ]. Electrocoagulation and suture hemostasis are commonly used to stop bleeding following the removal of an ovarian cyst. Electrocoagulation involves using an electric current to coagulate and seal the blood vessels. Although this technique provides a fast and efficient method to control ovarian wound bleeding, it can cause thermal damage to surrounding normal tissue, disrupt the ovarian blood circulation, and affect the normal development of the follicles. On the other hand, suture hemostasis involves using stitches to secure and ligate blood vessels to stop the bleeding effectively. However, the sutures can also cause additional damage to healthy tissue. Moreover, the sutures can damage the ovarian blood vessels and cause local inflammation and edema after surgery. Currently, most studies believe that electrocoagulation has greater damage to ovarian function, However, inconsistencies in follow-up durations across these studies, along with some conflicting conclusions, leave the impact of these hemostatic techniques on ovarian reserve (OR) uncertain [ 5 – 7 ]. This meta-analysis aims to compare short- and long-term OR outcomes in patients undergoing electrocoagulation versus suture hemostasis, with the goal of clarifying which technique incurs greater damage and whether electrocoagulation warrants absolute contraindication. Determining the likelihood of OR recovery over time is critical for both surgeons and patients.

Five studies [ 12 , 14 – 17 ] compared the AMH levels between the two surgical methods 1 month after surgery. The random-effects model was used for the meta-analysis since there was statistical heterogeneity among all studies (I 2  = 84%). Compared with the suture group, the bipolar coagulation group had statistically significantly lower serum AMH levels 1 month after surgery (WMD: −0.52, 95%CI (−1.02, −0.01), P  = 0.04) (Fig.  3 ). Fig. 3 One month postoperatively between electrocoagulation group and suture group. CI, confidence interval; I 2 , sample heterogeneity; SD = standard deviation One month postoperatively between electrocoagulation group and suture group. CI, confidence interval; I 2 , sample heterogeneity; SD = standard deviation Seven studies [ 5 , 13 – 18 ] compared the AMH levels between the two surgical methods 3 months after surgery. The random-effects model was used for the meta-analysis since all studies had statistical heterogeneity (I 2  = 61%). The AMH serum levels in the bipolar electrocoagulation group were significantly lower than those of the suture group 3 months after surgery (WMD: −0.72, 95%CI (−1.13, −0.31), P  = 0.0005) (Fig.  4 ). Fig. 4 Three months postoperatively between electrocoagulation group and suture group Three months postoperatively between electrocoagulation group and suture group Six studies [ 5 , 12 , 14 – 17 ] compared the AMH levels between the two surgical methods 6 months after surgery. Since all studies had statistically significant heterogeneity (I 2  = 61%), the random-effects model was used for meta-analysis. The bipolar electrocoagulation groups had significantly lower serum AMH levels than the suture group 6 months after surgery (WMD: −0.80, 95%CI (−1.22, −0.38), P  = 0.0002) (Fig.  5 ). Fig. 5 Six months postoperatively between electrocoagulation group and suture group Six months postoperatively between electrocoagulation group and suture group Four studies [ 5 , 14 , 16 , 17 ] compared the AMH levels between the two surgical methods 12 months after surgery. Since there was statistical heterogeneity among all studies (I 2  = 61%), the random-effects model was used for the meta-analysis. Compared to the suture group, the patients in the bipolar electrocoagulation group had statistically significantly lower serum AMH levels 12 months after surgery (WMD: −0.81, 95%CI (−1.24, −0.37), P  = 0.0003) (Fig.  6 ). Fig. 6 Twelve months postoperatively between electrocoagulation group and suture group Twelve months postoperatively between electrocoagulation group and suture group Three studies [ 14 , 16 , 17 ] reported the AMH levels for the two surgical methods before and 1, 3, 6, and 12 months after surgery comprehensively. The mean difference of AMH in electrocoagulation group at 1, 3, 6, and 12 months after surgery was −1.75, −1.37, −1.10, and −0.92, respectively; meanwhile, in the suture group were −2.50, −2.46, −2.33, and −2.24, respectively (Fig.  7 ). Fig. 7 Mean difference of AMH after surgery Mean difference of AMH after surgery These findings indicate that AMH gradually recovered at 1, 3, 6, 12 months after surgery, and the damage caused by electrocoagulation group was greater than that caused by suture group at each time point, and the difference was still statistically significant at 1 year after surgery. After visually examining the Berg funnel plot, no significant asymmetry indicative of publication bias was noted between the groups (Fig. S1 ).

Below is the link to the electronic supplementary material. Supplementary file1 (JPG 203 kb) Supplementary file2 (JPG 195 kb) Supplementary file3 (JPG 203 kb) Supplementary file4 (JPG 204 kb) Supplementary file5 (JPG 218 kb) Supplementary file6 (JPG 197 kb) Supplementary file7 (JPG 199 kb) Supplementary file8 (JPG 209 kb) Supplementary file9 (JPG 80 kb) Supplementary file1 (JPG 203 kb) Supplementary file2 (JPG 195 kb) Supplementary file3 (JPG 203 kb) Supplementary file4 (JPG 204 kb) Supplementary file5 (JPG 218 kb) Supplementary file6 (JPG 197 kb) Supplementary file7 (JPG 199 kb) Supplementary file8 (JPG 209 kb) Supplementary file9 (JPG 80 kb)