The effect of unilateral and bilateral laparoscopic surgery for endometriosis on Anti-Mullerian Hormone (AMH) level after 3 and 6 months: a systematic review and meta-analysis

Background: Endometriosis is one of the most common causes of infertility. The causes of the disease and its definitive treatments are still unclear. Moreover, Anti-Mullerian Hormone (AMH) is a glycoprotein dimer that is a member of the transient growth factors family. This research work aimed to identify the effect of unilateral and bilateral laparoscopic surgery for endometriosis on AMH levels after 3 months, and 6 months, using meta-analysis.

In this study, the articles published in national and international databases of SID, MagIran, IranMedex, IranDoc, Cochrane, Embase, Science Direct, Scopus, PubMed, and Web of Science (ISI) were searched to find electronically published studies between 2010 and 2019. The heterogeneous index between studies was determined using the I 2 index.

In this meta-analysis and systematic review, 19 articles were eligible for inclusion in the study. The standardized mean difference was obtained in examining of unilateral laparoscopic surgery for endometriosis (before intervention 2.8 ± 0.11, and after 3 months 2.05 ± 0.13; and before intervention 3.1 ± 0.46 and after 6 months 2.08 ± 0.31), and in examining bilateral laparoscopic surgery for endometriosis examination (before intervention 2.0 ± 08.08, and after 3 months 1.1 ± 0.1; and before intervention 2.9 ± 0.23 and after 6 months 1.4 ± 0.19).

The results of this study demonstrate that unilateral and bilateral laparoscopic surgery for endometriosis is effective on AMH levels, and the level decreases in both comparisons.

Laparoscopy, Unilateral, Bilateral, Endometriosis, AMH, Meta-analysis © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. * Correspondence: [email protected]; [email protected] 4Department of Biostatistics, School of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran 2Department of Nursing, School of Nursing and Midwifery, Kermanshah University of Medical Sciences, Kermanshah, Iran Full list of author information is available at the end of the article Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 https://doi.org/10.1186/s12955-020-01561-3

Endometriosis refers to the implantation of endomet- rium tissue, which includes stroma and epithelial tissues outside the uterus. Endometriosis is one of the most common causes of infertility and implantation failure [1]. The study of Kresch et al. showed that among 850 patients who referred to a clinic due to chronic pain (for more than 6 months) and were under laparoscopy, 92% had endometriosis or adhesion [ 2]. Anti-Mullerian Hormone (AMH) is a glycoprotein dimer that is a member of the transient growth factors family. AMH hormone belongs to the transforming growth factor-b family and is produced by the granulosa cells of primary to small antral follicles [ 3]. Serum AMH concentration correlates with the number of small folli- cles, and is impacted by the ovarian reserve rate [ 4]. During follicle growth, AMH expression is decreased once the follicle reaches a certain size (8 mm), resulting in an increased sensitivity of the follicle to circulating FSH. This reduces AMH level, which in turn provides an environment for follicle growth until ovulation [ 5]. Various surgical treatments have also been sug- gested for endometriosis, a nd significant differences have been reported among the therapeutic results of these methods. However, t he preference of most sur- geons and patients have r ecently shifted from open surgeries toward the laparo scopic treatments since laparoscopy is considered as a faster and a less ag- gressive method. Laparos copic treatments include endometrioma aspiration, laparoscopic cystectomy, cyst drainage, catheterization with catheter or laser, and even more radical treatments such as removal of a part or the whole ovary, and sometimes with uter- ine appendages [ 6]. Moreover, by comparing the possible complications of therapeutic methods with each other, the available evidence indicates that lap- aroscopic methods are superior. Possible complica- tions in laparoscopic treatments include damage to other organs caused by the laparoscopic devices, a reduced level of AMH, wound infection, bleeding, postoperative morbidity or long-term hospitalization, ileus, deep vein thrombosis, and/or other medical complications [ 7]. There have been several preliminary pieces of re- search studying the effect of unilateral and bilateral laparoscopic surgery for endometriosis on AMH level after 3 and 6 months. However, there are contradic- tions between the results of these studies. One of the applications of meta-analysis studies is to respond to these assumptions and resolve contradictions. There- fore, the aim of this study was to identify the effect of unilateral and bilateral laparoscopic surgery for endometriosis on AMH level after 3 and 6 months using meta-analysis.

Method of searching articles In this study, the Persian databases of SID, MagIran, IranMedex and IranDoc, and the international databases of Cochrane, Embase, Science Direct, Scopus, PubMed and Web of Science (ISI) were searched without a lower time-limit and until December 2019, with a view to find related articles and reports. The list of references within the identified above sources were manually evaluated to find other possible studies. The keywords used to search

were selected from the Medical Subject Head- ings (MeSH) thesaurus. Laparoscopic, Unilateral, Bilat- eral, Anti-Mullerian hormone, AMH, and endometriosis were the selected search keywords. The studies were assessed according to the four-step PRISMA 2009 process, which entails the phases of: identification, screening, eligibility assessment, and finally, including the articles in the meta-analysis. Inclusion criteria Articles with the following characteristics were selected for the meta-analysis: 1) Original research articles, 2) Clinical Trial Studies, 3) Articles with their full-text be- ing available, and 4) Studies that examined the relation- ship between unilateral and bilateral laparoscopy for endometriosis and AMH. Exclusion criteria The selected studies were examined in more details. Re- view papers, and studies where their sample were not se- lected from patients with endometriosis, as well as studies reusing previous data, were excluded from the meta-analysis. Finally, 27 studies were entered into the third stage, i.e. quality evaluation. Quality evaluation In order to evaluate the quality of articles, the CON- SORT checklist was used. The checklist has a number of scales that include: study plot, background, literature re- view, place and time of study, outcome, inclusion cri- teria, sample size, and statistical analysis. The maximum score that could be obtained during the quality evalu- ation and using this checklist is 40. Studies with a score of less than 19 were considered as low-quality articles, and therefore were excluded from the study [ 8]. In this research, 19 articles that were assessed as medium or high-quality articles were entered in the final systematic review and meta-analysis phase, and 8 articles which were scored as low-quality studies were excluded. Data extraction The data from the final selection of sources were ex- tracted using a different pre-prepared checklist. The checklist includes a number of fields such as the article Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 Page 2 of 9 title, first author ’s name, year of publication, place of study, sample size of unilateral and bilateral laparoscopic surgery for endometriosis intervention groups, mean sample before intervention, mean sample after 3 and 6 months, the standard deviation of the sample before intervention, and the standard deviation of the sample after 3 and 6 months. Statistical analysis Since the focus of the research was in relation to the ef- fect of unilateral and bilateral laparoscopic surgery for endometriosis on AMH level after 3 and 6 months, fre- quency and percentage, as well as standardized mean difference in examining unilateral and bilateral laparo- scopic surgery for endometriosis before and after inter- vention in each study, were used to combine the reported results of the collected studies. The I 2 index was initially used to investigate the homogeneity among the studies; and since the reported results were found to be heterogeneous, the random effects model was used to combine the findings and perform the meta-analysis. When the I 2 index was less than 25%, it was considered as low heterogeneity, between 25 and 75% as moderate heterogeneity and more than 75% as high heterogeneity. P-value less than 0.05 was considered statistically signifi- cant. The Egger ’s test was also used to investigate the publication bias. The data were analyzed using the Com- prehensive Meta-Analysis software (Biostat, Englewood, NJ, USA Version 3). The standardized mean difference index and 95% con- fidence interval in every study, as well as the final esti- mation of the index obtained from the combination of Fig. 1 Flow diagram of study selection Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 Page 3 of 9 studies, have been illustrated in the Forrest plot. In this plot, the weight of every study has been shown in the final combined value, and the size of every square is pro- portional to the weight of that study in the meta- analysis.

In this research work, all studies focusing on the com- parison of unilateral and bilateral laparoscopic surgery for endometriosis on AMH level after 3 and 6 months were systematically examined without time limitations and according to the PRISMA guidelines. In the initial search, 879 articles were identified. This number was re- duced to 19 for the final analysis, and includes articles that were published between 2010 and December 2019 (Fig. 1). The characteristics of studies entered into the system- atic review (Tables 1 and 2). The standardized mean difference indices in the arti- cles were used to examine the effects of the reported re- sults in the studies. In the articles where standard deviation ± mean was reported, the standardized mean difference index was used in the meta-analysis. The re- sults of the meta-analysis showed heterogeneity in stud- ies examining unilateral laparoscopic surgery for endometriosis after 3 and 6 months (I 2 = 99.9) and in re- search works examining bilateral laparoscopic surgery for endometriosis after 3 and 6 months (I 2 = 99.8). Con- sidering this, the random effects model was adopted to enable the amalgamation of the reported results. The Egger ’s test was used to investigate the presence of publication bias in the studies. According to the Egger’s test results, there was no publication bias in studies a) examining unilateral laparoscopic surgery for endometriosis after 3 and 6 months ( P = 0.244), b) exam- ining bilateral laparoscopic surgery for endometriosis after 3 and 6 months ( P = 0.891). The standardized mean difference was obtained in examining unilateral laparoscopic surgery for endometri- osis (before intervention 2.8 ± 0.11 and after 3 months 2.05 ± 0.13; and before intervention 3.1 ± 0.46 and after 6 months 2.08 ± 0.31), and in examining bilateral laparo- scopic surgery for endometriosis (before intervention 2.08 ± 0.08 and after 3 months 1.1 ± 0.1; before interven- tion 2.9 ± 0.23 and after 6 months 1.4 ± 0.19), which indi- cates unilateral and bilateral laparoscopic surgery for endometriosis is effective on AMH level. The AMH level is reduced in both comparisons, and the effect of bilat- eral laparoscopic surgery for endometriosis on AMH level was more than for unilateral laparoscopic surgery for endometriosis. Moreover, this reduction increases after 6 months. (Figs. 2, 3, 4, 5, 6).

The aim of this study was to investigate the effect of uni- lateral and bilateral laparoscopic surgery for endometriosis treatment on the reduction of AMH level after 3 and 6 months, using meta-analysis, in which the standardized mean difference was obtained in examining unilateral lap- aroscopic surgery for endometriosis, and in examining bi- lateral laparoscopic surgery for endometriosis. Table 1 Characteristics of studies performed on meta-analysis in unilateral endometrial laparoscopic group Author, year, Reference Place of study sample size Mean ± SD of Before Mean ± SD of 3 months Mean ± SD of 6 months Quality Suksompong, 2012, [ 9] Thailand 28 2.14 1.45 – High Ergun, 2011, [ 10] Turkey 50 2.03 ± 0.41 1.95 ± 0.62 – High Ergun, 2015, [ 11] Turkey 38 3.15 ± 2.86 2.10 ± 1.82 – High Hwu, 2011, [ 12] Taiwan 147 2.48 1.33 – High Chang, 2010, [ 13] Korea 20 2.78 1.8 – Medium Mostaejeran, 2015, [ 14] Iran 33 3.08 1.75 – Medium Adnyana, 2018, [ 15] Indonesia 25 2.17 ± 1.24 1.79 ± 0.97 – High Chun, 2015, [ 16] Korea 26 4.97 ± 2.66 3.59 ± 1.83 – High Salihoğ lu, 2016, [ 17] Canada 34 3.50 ± 2.70 2.70 ± 1.40 – High Alborzi, 2014, [ 6] Iran 193 4.31 ± 3.82 2.53 ± 2.92 – High El-Dorf-1, 2015, [ 18] Egypt 120 3.10 ± 0.31 2.50 ± 0.11 2.20 ± 0.27 High El-Dorf-2, 2015, [ 18] Egypt 80 2.40 ± 0.22 2.00 ± 0.23 1.90 ± 0.21 High Nappi, 2016, [ 19] Italy 45 3.01 ± 0.78 – 2.76 ± 0.8 High Saito, 2018, [ 20] Japan 32 4.40 ± 2.55 – 1.2 ± 1.3 High Marshall, 2019, [ 21] Sudan 20 3.22 – 1.82 Medium Shao, 2016, [ 22] China 36 5.02 ± 3.05 – 4.43 ± 2.13 High Celik, 2012, [ 23] Turkey 39 1.05 – 0.6 High Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 Page 4 of 9 In a meta-analysis conducted by Amer et al. (2017) using 7 articles, the level of AMH after laparoscopy was reported as 2.13 ng/ml [ 27]. This difference between this and our findings may be due to the fact that in our study the articles related to unilateral and bilateral laparo- scopic surgery for endometriosis have been studied separately. In vitro fertilization (IVF) is a complex series of procedures used to help with fertility or prevent gen- etic problems and assist with the conception of a child, During IVF, mature eggs are collected from ovaries and fertilized by sperm in a lab. Then the fer- tilized egg (embryo) or eggs (embryos) are transferred to a uterus [ 27–29]. Table 2 Characteristics of studies performed on meta-analysis in bilateral endometrial laparoscopic group Author, year, Reference Place of study sample size Mean ± SD of Before Mean ± SD of 3 months Mean ± SD of 6 months Quality Suksompong, 2012, [ 9] Thailand 15 2.11 0.74 – High Ergun, 2015, [ 11] Turkey 12 1.18 ± 1.07 1.00 ± 1.01 – High Hwu, 2011, [ 12] Taiwan 147 1.7 1.03 – High Chang, 2010, [ 13] Korea 20 2.18 0.95 – Medium Adnyana, 2018, [ 15] Indonesia 35 2.07 ± 1.18 1.44 ± 0.87 – High Sumapraja, 2011, [ 24] Indonesia 22 1.64 0.6 – High Salihoğ lu, 2016, [ 17] Canada 34 2.60 ± 2.30 2.20 ± 1.9 – High Alborzi, 2014, [ 6] Iran 193 2.60 ± 1.98 1.07 ± 0.97 – High Tanprasertkul, 2014, [ 25] Thailand 39 2.01 1.60 1.68 High El-Dorf-2, 2015, [ 18] Egypt 50 2.90 ± 0.40 1.70 ± 0.30 1.6 ± 0.12 High El-Dorf-2, 2015, [ 18] Egypt 80 1.90 ± 0.24 1.30 ± 0.10 0.97 ± 0.11 High Saito, 2018, [ 20] Japan 37 3.1 ± 1.7 – 0.8 ± 0.7 High Marshall, 2019, [ 21] Sudan 39 3.19 – 0.88 Medium Shao, 2016, [ 22] China 36 4.68 ± 2.87 – 3.05 ± 1.99 High Zaitoun, 2013, [ 26] Egypt 61 4.50 ± 0.80 – 2.40 ± 0.50 Medium Celik, 2012, [ 23] Turkey 39 2.20 – 0.55 High Fig. 2 Accumulation plot obtained from studies entered in Meta-analysis analysis using standardized mean difference index of AMH changes with unilateral laparoscopic surgery of endometriosis after 3 months Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 Page 5 of 9 In a meta-analysis which was performed on women with endometrium under IVF between 1985 and 2007, 20 pieces of research were investigated; the meta- analysis demonstrated that the clinical pregnancy rate was not different between the treated and untreated groups [ 29]. Cystectomy is a common treatment among endometri- osis surgical treatments. In laparoscopic cystectomy method, which is still considered the preferred thera- peutic method, the inner layer of the cyst is separated, and removed from the ovarian tissue by two forceps, which may affect ovarian reserve [ 6]. Fig. 3 Accumulation plot obtained from studies entered in Meta-analysis analysis using standardized mean difference index of AMH changes with unilateral laparoscopic surgery of endometriosis after 6 months Fig. 4 Accumulation plot obtained from studies entered in Meta-analysis analysis using standardized mean difference index of AMH changes with bilateral laparoscopic surgery of endometriosis after 3 months Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 Page 6 of 9 Fig. 5 Accumulation plot obtained from studies entered in Meta-analysis analysis using standardized mean difference index of AMH changes with bilateral laparoscopic surgery of endometriosis after 6 months Fig. 6 Overall Standardized mean difference in bilateral and unilateral laparoscopic surgery of endometriosis before the intervention and after 3 and 6 months Nankali et al. Health and Quality of Life Outcomes (2020) 18:314 Page 7 of 9 According to a meta-analysis conducted by Somigliana et al. (2012), changes in AMH serum level after endo- metrial ablation, affect the damages caused to the ovar- ian reserve following the surgery [ 30]. Chang et al. (2010) [ 13] in a different study in China on 60 infertile women measured levels of AMH, inhibin B, FSH, LH, and estradiol on third day of the menstrual cycle and found that there was a significant difference between AMH levels on the third day of the menstrual cycle in fertile and infertile women, and concluded that AMH is correlated better with the number of recovered oocytes than with age, FSH and inhibin B. Women whose AMH levels were within the range of 4.4 ± 2.2 had a better re- sponse than women whose AMH serum levels were 0.7 ± 0.8 ( P < 0.01) [ 13]. The study of Visser et al. (2006) in the Netherlands showed that AMH is a quantitative marker of ovarian reserve as well as ovarian dysfunction. Unlike FSH, AMH can be measured on any day of the cycle. The level of AMH decreases with performing laparoscopy, and it can be predicted that the ovarian efficacy is re- duced by decreasing the AMH value [ 31]. Lekamge et al. (2007) in a study in Australia measured the baseline concentration of AMH, FSH, and antral fol- licle count from 126 women undergoing IVF treatment, and concluded that in patients with low AMH, lower oo- cytes number were formed than average persons ( P < 0.01). The fertility rate was also lower in the study group (P < 0.05) and fewer embryos were formed ( P <0 . 0 5 )[32]. According to this systematic review and meta-analysis study, the effect of bilateral laparoscopic surgery for endometriosis on AMH level was more than for unilat- eral laparoscopic surgery for endometriosis. This study demonstrates that the level of AMH is visibly reduced after endometriosis laparoscopy. This reduction of AMH levels does not stop after 6 months, but decreases even further. Therefore, gynaecologists should not overlook the decrease of AMH levels after unilateral and bilateral laparoscopic endometrial surgeries, since the decreased ovarian reserve may result in infertility, or premature menopause in future. Our study had a few limitations; the heterogeneity of the patient ’s population, in terms of age and extent of endometriosis, may have an effect on the scientific validity of the reported results. In some articles, a follow-up was performed shortly after the intervention (3 months), how- ever, the number of articles studying 6 months after the intervention was limited. Therefore, it is suggested to con- duct another meta-analysis for examining AMH levels after 9 months and 1 year.

The results of this study indicate that unilateral and bi- lateral laparoscopic surgery for endometriosis is effective on AMH level and the level decreases for both compari- sons. The effect of bilateral laparoscopic surgery for endometriosis on AMH level reduction is more than unilateral laparoscopic surgery for endometriosis; more- over this reduction intensifies after 6 months. Therefore, the findings in this research work can be beneficial for health policy makers and professionals in this field. Abbreviations AMH: Anti-Müllerian Hormone; FSH: Follicle-Stimulating Hormone; CONSORT: Consolidated Standards of Reporting Trials; PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analysis

By Student Research Committee of Kermanshah University of Medical Sciences. Authors’ contributions PKJ and AVN contributed to the design, MM and NS statistical analysis, participated in most of the study steps. SS and MK and AHF prepared the manuscript. All authors have read and approved the content of the manuscript. Funding By Student Research Committee of Kermanshah University of Medical Sciences, Deputy for Research and Technology, Kermanshah University of Medical Sciences (IR) (3009261). Availability of data and materials Datasets are available through the corresponding author upon reasonable request. Ethics approval and consent to participate None declared. Consent for publication Not applicable. Competing interests The authors declare that they have no conflict of interest. Author details 1School of Medicine, Department of Obstetrics and Gynecology, Kermanshah University of Medical Sciences, Kermanshah, Iran. 2Department of Nursing, School of Nursing and Midwifery, Kermanshah University of Medical Sciences, Kermanshah, Iran. 3Department of Biology, Faculty of Science, University Putra Malaysia, Serdang, Selangor, Malaysia. 4Department of Biostatistics, School of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran. 5Department of Business Systems & Operations, University of Northampton, Northampton, UK. Received: 17 April 2020 Accepted: 10 September 2020

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