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The effect of opportunistic salpingectomy for primary prevention of ovarian cancer on ovarian reserve: a systematic review and meta-analysis

Open AccessPublished:August 17, 2022DOI:https://doi.org/10.1016/j.maturitas.2022.08.002

      Highlights

      • Opportunistic salpingectomy is recommended as primary prevention for ovarian cancer.
      • Opportunistic salpingectomy may cause earlier onset of menopause.
      • Evidence on the long-term effects of opportunistic salpingectomy on menopausal onset is currently lacking.
      • Opportunistic salpingectomy does not result in a significant reduction of ovarian reserve in the short-term.

      Abstract

      Background

      Opportunistic salpingectomy (OS) is an attractive method for primary prevention of ovarian cancer. Although OS has not been associated with a higher complication rate, it may be associated with earlier onset of menopause.

      Objective

      To provide a systematic review and meta-analysis of the effect of OS on both age at menopause and ovarian reserve.

      Methods

      A search was conducted in the Cochrane Library, Embase and MEDLINE databases from inception until March 2022. We included randomized clinical trials and cohort studies investigating the effect of OS on onset of menopause and/or ovarian reserve through change in anti-Müllerian hormone (AMH), antral follicle count (AFC), estradiol (E2), follicle stimulating hormone (FSH) and luteinizing hormone (LH). Data was extracted independently by two researchers. Random-effects meta-analyses were conducted to estimate the pooled effect of OS on ovarian reserve.

      Results

      The initial search yielded 1047 studies. No studies were found investigating the effect of OS on age of menopause. Fifteen studies were included in the meta-analysis on ovarian reserve. Meta-analyses did not result in statistically significant differences in mean change in AMH (MD -0.07 ng/ml, 95%CI −0.18;0.05), AFC (MD 0.20 n, 95 % CI −4.91;5.30), E2 (MD 3.97 pg/ml, 95%CI −0.92;8.86), FSH (MD 0.33mIU/ml, 95%CI −0.15;0.81) and LH (MD 0.03mIU/ml; 95%CI −0.47;0.53).

      Conclusion

      Our study shows that OS does not result in a significant reduction of ovarian reserve in the short term. Further research is essential to confirm the absence of major effects of OS on menopausal onset since clear evidence on this subject is lacking.
      Registration number PROSPERO CRD42021260966.

      Abbreviations:

      AMH (Anti-Müllerian Hormone), AFC (Antral Follicle Count), E2 (Estradiol), EMP (Earlier menopause), EOC (Epithelial ovarian cancer), FSH (Follicle Stimulating Hormone), HGSC (High grade serous carcinoma), LH (Luteinizing Hormone), OS (Opportunistic Salpingectomy), RCT (Randomized controlled trial), RoB (Risk of Bias)

      Keywords

      1. Introduction

      Ovarian cancer has the highest mortality rate of all gynaecological malignancies. The disease is often detected at late stage and overall survival rate is low [
      • Lheureux S.
      • Gourley C.
      • Vergote I.
      • Oza A.M.
      Epithelial ovarian cancer.
      ]. Moreover, the prognosis remains poor through the absence of effective screening options [
      • Lheureux S.
      • Gourley C.
      • Vergote I.
      • Oza A.M.
      Epithelial ovarian cancer.
      ,
      • Menon U.
      • Gentry-Maharaj A.
      • Burnell M.
      • Singh N.
      • Ryan A.
      • Karpinskyj C.
      • Carlino G.
      • Taylor J.
      • Massingham S.K.
      • Raikou M.
      • Kalsi J.K.
      • Woolas R.
      • Manchanda R.
      • Arora R.
      • Casey L.
      • Dawnay A.
      • Dobbs S.
      • Leeson S.
      • Mould T.
      • Seif M.W.
      • Sharma A.
      • Williamson K.
      • Liu Y.
      • Fallowfield L.
      • McGuire A.J.
      • Campbell S.
      • Skates S.J.
      • Jacobs I.J.
      • Parmar M.
      Ovarian cancer population screening and mortality after long-term follow-up in the UK collaborative trial of ovarian cancer screening (UKCTOCS): a randomised controlled trial.
      ]. As recent advances in treatment methods have only slightly improved the prognosis, primary prevention might be the solution to reduce the incidence and subsequent burden of ovarian cancer [
      • Lheureux S.
      • Gourley C.
      • Vergote I.
      • Oza A.M.
      Epithelial ovarian cancer.
      ].
      Current insights on etiology of epithelial ovarian cancer (EOC) provide clues for developing a strategy to reduce EOC risk. Evidence suggests that the fallopian tube epithelium rather than the ovarian surface epithelium is the origin of the most common type of EOC, high grade serous carcinoma (HGSC) [
      • Labidi-Galy S.I.
      • Papp E.
      • Hallberg D.
      • Niknafs N.
      • Adleff V.
      • Noe M.
      • Bhattacharya R.
      • Novak M.
      • Jones S.
      • Phallen J.
      • Hruban C.A.
      • Hirsch M.S.
      • Lin D.I.
      • Schwartz L.
      • Maire C.L.
      • Tille J.-C.
      • Bowden M.
      • Ayhan A.
      • Wood L.D.
      • Scharpf R.B.
      • Kurman R.
      • Wang T.-L.
      • Shih I.-M.
      • Karchin R.
      • Drapkin R.
      • Velculescu V.E.
      High grade serous ovarian carcinomas originate in the fallopian tube.
      ,
      • Piek J.M.J.
      • Verheijen R.H.M.
      • Kenemans P.
      • Massuger L.F.
      • Bulten H.
      • Van Diest P.J.
      BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis.
      ]. By removing the fallopian tubes, HGSC may not be able to develop and its incidence might decrease [
      • Hanley G.E.
      • Pearce C.L.
      • Talhouk A.
      • Kwon J.S.
      • Finlayson S.J.
      • McAlpine J.N.
      • Huntsman D.G.
      • Miller D.
      Outcomes from opportunistic salpingectomy for ovarian cancer prevention.
      ]. Bilateral salpingectomy as addition to planned intra-abdominal surgery, a so-called opportunistic salpingectomy (OS) [
      • Chohan L.
      • Richardson D.L.
      ACOG COMMITTEE OPINION number 774 opportunistic salpingectomy as a strategy for epithelial ovarian cancer prevention.
      ], might therefore result in primary prevention of EOC. This theory is supported by large cohort studies that show a risk reduction ranging from 42 to 65 % after bilateral salpingectomy [
      • Madsen C.
      • Baandrup L.
      • Dehlendorff C.
      • Kjær S.K.
      Tubal ligation and salpingectomy and the risk of epithelial ovarian cancer and borderline ovarian tumors: a nationwide case-control study.
      ,
      • Lessard-Anderson C.R.
      • Handlogten K.S.
      • Molitor R.J.
      • Dowdy S.C.
      • Cliby W.A.
      • Weaver A.L.
      • St Sauver J.
      • Bakkum-Gamez J.N.
      Effect of tubal sterilization technique on risk for serous epithelial ovarian and primary peritoneal carcinoma: editorial comment.
      ,
      • Falconer H.
      • Yin L.
      • Grönberg H.
      • Altman D.
      Ovarian cancer risk after salpingectomy: a nationwide population-based study.
      ].
      In recent years, OS has increasingly been performed and is issued in clinical gynaecological guidelines of several countries [
      • Mandelbaum R.S.
      • Adams C.L.
      • Yoshihara K.
      • Nusbaum D.J.
      • Matsuzaki S.
      • Matsushima K.
      • Klar M.
      • Paulson R.J.
      • Roman L.D.
      • Wright J.D.
      • Matsuo K.
      The rapid adoption of opportunistic salpingectomy at the time of hysterectomy for benign gynecologic disease in the United States.
      ,
      • Lander B.
      • Wilcox E.
      • McAlpine J.N.
      • Finlayson S.J.
      • Huntsman D.G.
      • Miller D.
      • Hanley G.E.
      Changing clinical practice: evaluation of implementing recommendations for opportunistic salpingectomy in British Columbia and Ontario.
      ,
      • Ntoumanoglou-Schuiki A.
      • Tomasch G.
      • Laky R.
      • Taumberger N.
      • Bjelic-Radisic V.
      • Tamussino K.
      Opportunistic prophylactic salpingectomy for prevention of ovarian cancer: what do national societies advise?.
      ]. Although OS has not been associated with complications, there might be subtle long-term consequences [
      • Mills K.
      • Marchand G.
      • Sainz K.
      • Azadi A.
      • Ware K.
      • Vallejo J.
      • Anderson S.
      • King A.
      • Osborn A.
      • Ruther S.
      • Brazil G.
      • Cieminski K.
      • Hopewell S.
      • Rials L.
      • Klipp A.
      Salpingectomy vs tubal ligation for sterilization: a systematic review and meta-analysis.
      ,
      • van Lieshout L.A.M.
      • Steenbeek M.P.
      • De Hullu J.A.
      • Vos M.C.
      • Houterman S.
      • Wilkinson J.
      • Piek J.M.J.
      Hysterectomy with opportunistic salpingectomy versus hysterectomy alone.
      ]. Removing the shared blood supply between the fallopian tubes and ovaries could theoretically decrease oocyte quality and may cause earlier onset of menopause [
      • van Lieshout L.A.M.
      • Steenbeek M.P.
      • De Hullu J.A.
      • Vos M.C.
      • Houterman S.
      • Wilkinson J.
      • Piek J.M.J.
      Hysterectomy with opportunistic salpingectomy versus hysterectomy alone.
      ]. Given that premature menopause is associated with a higher risk of cardiovascular diseases, cognitive impairment and osteoporosis, this potential risk of OS might outweigh its preventive benefits [
      • Shuster L.T.
      • Rhodes D.J.
      • Gostout B.S.
      • Grossardt B.R.
      • Rocca W.A.
      Premature menopause or early menopause: long-term health consequences.
      ].
      To investigate whether OS affects onset of menopause, the age at which a woman enters menopause can be determined. In addition, several other surrogate markers may reflect the ovarian reserve and can provide an indication of menopausal age [
      • Penzias A.
      • Azziz R.
      • Bendikson K.
      • Falcone T.
      • Hansen K.
      • Hill M.
      • Hurd W.
      • Jindal S.
      • Kalra S.
      • Mersereau J.
      • Racowsky C.
      • Rebar R.
      • Reindollar R.
      • Shannon C.N.
      • Steiner A.
      • Stovall D.
      • Tanrikut C.
      • Taylor H.
      • Yauger B.
      Testing and interpreting measures of ovarian reserve: a committee opinion.
      ]. In this review, we aim to summarize and analyze current literature on the effect of OS on both menopausal age and ovarian reserve.

      2. Methods

      This study was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines [
      • Page M.J.
      • McKenzie J.E.
      • Bossuyt P.M.
      • Boutron I.
      • Hoffmann T.C.
      • Mulrow C.D.
      • Shamseer L.
      • Tetzlaff J.M.
      • Akl E.A.
      • Brennan S.E.
      • Chou R.
      • Glanville J.
      • Grimshaw J.M.
      • Hróbjartsson A.
      • Lalu M.M.
      • Li T.
      • Loder E.W.
      • Mayo-Wilson E.
      • McDonald S.
      • McGuinness L.A.
      • Stewart L.A.
      • Thomas J.
      • Tricco A.C.
      • Welch V.A.
      • Whiting P.
      • Moher D.
      The PRISMA 2020 statement: an updated guideline for reporting systematic reviews.
      ] (Table S1) and was registered in PROSPERO (registration number: CRD42021260966).

      2.1 Outcome measures

      Study outcomes were age of natural menopause and ovarian reserve. By natural menopause we refer to amenorrhea of 12 months without another explanatory reason [
      • Weismiller D.G.
      Menopause.
      ]. Ovarian reserve signifies the remaining number of oocytes in the ovary. Ovarian reserve was determined through assessment of the change (delta; Δ) in pre- and postoperative values of Anti-Müllerian Hormone (AMH), Antral Follicle Count (AFC), Estradiol (E2), Follicle Stimulating Hormone (FSH) and/or Luteinizing Hormone (LH) [
      • Penzias A.
      • Azziz R.
      • Bendikson K.
      • Falcone T.
      • Hansen K.
      • Hill M.
      • Hurd W.
      • Jindal S.
      • Kalra S.
      • Mersereau J.
      • Racowsky C.
      • Rebar R.
      • Reindollar R.
      • Shannon C.N.
      • Steiner A.
      • Stovall D.
      • Tanrikut C.
      • Taylor H.
      • Yauger B.
      Testing and interpreting measures of ovarian reserve: a committee opinion.
      ].

      2.2 Search

      A detailed search was conducted in the Cochrane Library, Embase and MEDLINE from inception until March 2022 to identify studies on the effect of OS on onset of menopause. Database searches were executed by means of the following terms: ‘Salpingectomy’ OR ‘Tubectomy’, AND ‘Menopause’, ‘Premature menopausal’, ‘Ovarian reserve’, ‘Ovarian function’, ‘Antral Follicle Count’, ‘Anti Mullerian Hormone’, ‘Estradiol’, ‘Follicle Stimulating Hormone’, OR ‘Luteinizing Hormone’. Table S2 provides a detailed elaboration of the searches.

      2.3 Study selection

      All randomized controlled trials (RCTs), cohort (prospective and retrospective) and cross-sectional studies that investigated the effect of OS on onset of menopause or ovarian reserve were considered for inclusion. Studies were only included if they were written in English. Studies were excluded if the study population involved patients within a fertility trajectory since these patients had an active desire to have children and often received ovarian stimulation. Studies including patients who had undergone bilateral oophorectomy or patients with a proven pathogenic variant germline gene mutation, increasing ovarian cancer risk, such as BRCA1/2 were excluded as well. These populations will enter menopause earlier due to (prophylactic)surgery or as a consequence of the germline gene mutation itself [
      • Titus S.
      • Li F.
      • Stobezki R.
      • Akula K.
      • Unsal E.
      • Jeong K.
      • Dickler M.
      • Robson M.
      • Moy F.
      • Goswami S.
      • Oktay K.
      Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans.
      ,
      • Finch A.
      • Metcalfe K.A.
      • Chiang J.K.
      • Elit L.
      • McLaughlin J.
      • Springate C.
      • Demsky R.
      • Murphy J.
      • Rosen B.
      • Narod S.A.
      The impact of prophylactic salpingo-oophorectomy on menopausal symptoms and sexual function in women who carry a BRCA mutation.
      ]. For ovarian reserve, studies were only included if they reported both pre- and postoperative values of surrogate marker and/or change in surrogate marker values.
      Studies identified by the search were imported into the reference manager database Rayyan [
      • Ouzzani M.
      • Hammady H.
      • Fedorowicz Z.
      • Elmagarmid A.
      Rayyan-a web and mobile app for systematic reviews.
      ]. Studies were independently screened and selected for eligibility on title and abstract by two reviewers (MG, LD). Full text of eligible studies was obtained, and the same reviewers independently assessed them for definitive inclusion. Disagreements were discussed with a third independent reviewer (JI) until consensus was reached. PRISMA flowchart in Fig. 1 illustrates the selection process.
      Fig. 1
      Fig. 1PRISMA flow diagram of study selection.

      2.4 Data extraction

      Data were extracted of all included studies independently by two reviewers(MG, LD) according to a standardized format including: study design, number of participants, participants characteristics, indicated procedure, outcomes and duration of follow-up. Disagreements were resolved by discussion. For one study, missing data concerning the OS group was retrieved by contacting its corresponding author [
      • Naaman Y.
      • Hazan Y.
      • Gillor M.
      • Marciano G.
      • Bardenstein R.
      • Shoham Z.
      • Ben-Arie A.
      Does the addition of salpingectomy or fimbriectomy to hysterectomy in premenopausal patients compromise ovarian reserve? A prospective study.
      ].

      2.5 Risk assessment

      Two reviewers (MG, LD) independently assessed the risk of bias (RoB) through the ROBINS-I tool in non-RCTs [
      • Sterne J.A.
      • Hernán M.A.
      • Reeves B.C.
      • Savović J.
      • Berkman N.D.
      • Viswanathan M.
      • Henry D.
      • Altman D.G.
      • Ansari M.T.
      • Boutron I.
      • Carpenter J.R.
      • Chan A.W.
      • Churchill R.
      • Deeks J.J.
      • Hróbjartsson A.
      • Kirkham J.
      • Jüni P.
      • Loke Y.K.
      • Pigott T.D.
      • Ramsay C.R.
      • Regidor D.
      • Rothstein H.R.
      • Sandhu L.
      • Santaguida P.L.
      • Schünemann H.J.
      • Shea B.
      • Shrier I.
      • Tugwell P.
      • Turner L.
      • Valentine J.C.
      • Waddington H.
      • Waters E.
      • Wells G.A.
      • Whiting P.F.
      • Higgins J.P.
      ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions.
      ], and RoB-II tool in RCTs [
      • Sterne J.A.C.
      • Savović J.
      • Page M.J.
      • Elbers R.G.
      • Blencowe N.S.
      • Boutron I.
      • Cates C.J.
      • Cheng H.Y.
      • Corbett M.S.
      • Eldridge S.M.
      • Emberson J.R.
      • Hernán M.A.
      • Hopewell S.
      • Hróbjartsson A.
      • Junqueira D.R.
      • Jüni P.
      • Kirkham J.J.
      • Lasserson T.
      • Li T.
      • McAleenan A.
      • Reeves B.C.
      • Shepperd S.
      • Shrier I.
      • Stewart L.A.
      • Tilling K.
      • White I.R.
      • Whiting P.F.
      • Higgins J.P.T.
      RoB 2: a revised tool for assessing risk of bias in randomised trials.
      ].

      2.6 (statistical) analysis

      As the search did not result in studies on age at onset of menopause, we only analysed the effect of OS on ovarian reserve. In most studies, ovarian reserve was reported as mean change-from-baseline in surrogate marker, with corresponding standard deviation. If the mean change was not available, the median change-from-baseline was used as an estimate of the mean change-from-baseline, and the corresponding standard deviation was derived from the interquartile range using formula 15 of Wan et al., 2014 [
      • Wan X.
      • Wang W.
      • Liu J.
      • Tong T.
      Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range.
      ]. When only mean preoperative and postoperative values were available, the mean change-from-baseline was calculated as: ‘mean postoperative – mean preoperative’. The corresponding standard deviation was derived as follows:√(SDpreoperative2 + SDpostoperative2–2·r·SDpreoperative·SDpostoperative) [
      • Higgins J.P.T.
      • Li T.
      • Deeks J.J.
      Choosing effect measures and computing estimates of effect.
      ], in which the group correlation r was calculated with formula 6 of Papadimitropoulou et al., 2020 [
      • Papadimitropoulou K.
      • Stijnen T.
      • Riley R.D.
      • Dekkers O.M.
      • le Cessie S.
      Meta-analysis of continuous outcomes: using pseudo IPD created from aggregate data to adjust for baseline imbalance and assess treatment-by-baseline modification.
      ], using studies that reported both preoperative and postoperative SDs and the SD of the change from baseline.
      To estimate the pooled effect of OS on ovarian reserve, we conducted random-effects meta-analyses, using the inverse variance method, a restricted maximum-likelihood estimator for the between-study heterogeneity τ2, and the Q-profile method for the confidence interval for τ2 . [
      • Viechtbauer W.
      • López-López J.A.
      • Sánchez-Meca J.
      • Marín-Martínez F.
      A Comparison of Procedures to Test for Moderators in Mixed-effects Meta-regression Models.
      ] Hartung-Knapp-Sidik-Jonkman adjustments were applied to control for uncertainties in the estimation of the between-study heterogeneity [
      • Inthout J.
      • Ioannidis J.P.
      • Borm G.F.
      The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method.
      ]. Sensitivity analyses were conducted if heterogeneity between studies was moderate or high, excluding all outliers from analysis. A study was considered an outlier when the 95 % confidence interval lies outside the 95 % confidence interval of the pooled effect [
      • Viechtbauer W.
      • Cheung M.W.
      Outlier and influence diagnostics for meta-analysis.
      ]. Subgroup analyses were performed based on study design (RCT; prospective cohort studies; retrospective cohort studies), indicated procedure (hysterectomy; caesarean section; myomectomy), duration of follow-up (ranging between 4 and 6 weeks and 9 months) and risk of bias (low; moderate/some concerns; high; no information). Meta-regression was conducted to examine if the mean ages of the study populations could be used for prediction of effect size. Results of the meta-analyses are presented as mean differences with 95 % confidence interval. Heterogeneity across studies was assessed with prediction intervals and I2 (<30 %; low level of heterogeneity, 30–60 % moderate level of heterogeneity; >60 % substantial to considerable level of heterogeneity) [
      • Deeks J.J.
      • Higgins J.P.T.
      • Altman D.G.
      • Group C.S.M.
      Analysing data and undertaking meta-analyses.
      ]. Funnel plots were made to examine possible publication bias. Statistical significance was defined as a two-sided p ≤ 0.05. We used the ‘meta’ package (version 4.19–1) in R (software version 4.1.2) [
      R Core Team
      R: A language and environment for statistical computing.
      ].

      3. Results

      3.1 Study selection and characteristics

      In total 1047 records were retrieved. After identifying duplicate records, 303 records were removed resulting in 744 records which were screened on title and abstract. Full text was obtained from 38 studies, and 23 studies were excluded after reading full text. A total of 15 studies were included in the final assessment. Fig. 1 shows the selection process.
      Table IOverview of included studies and their study characteristics.
      Study referenceStudy designCountryPatient characteristicsIndicated surgeryN total at baselineAge (years)Outcome measure(s)Duration of follow-up
      Behnamfar et al., 2017 (Behnamfar and Jabbari, 2017)RCTIranInclusion criteria:

      • -
        undergoing hysterectomy with bilateral salpingectomy for benign reasons (myxomatosis uterus or menorrhagia)
      • -
        premenopausal women
      • -
        regular menstruation
      • -
        no history of malignancy


      Exclusion criteria:

      • -
        operation cancelled
      • -
        hormone measurement before or after operation inaccessible
      • -
        postsurgical pathology of malignancy
      Intervention group: Hysterectomy with OS



      Control group:

      Hysterectomy
      40

      (OS 18, non-OS 22)
      OS 48.5 (SD 2.0), non-OS 47.8 (SD 3.0)Ovarian reserve:

      • -
        FSH (mIU/ml)
      analysed by chemiluminescence immunoassay COBAS e411 auto-analyser (Roche Diagnostics, USA)

      • -
        LH (mIU/ml)
      analysed by chemiluminescence immunoassay COBAS e411 auto-analyser (Roche Diagnostics, USA)
      6 months
      Findley et al., 2013 (Findley et al., 2013)RCTUnited StatesInclusion criteria

      • -
        undergoing laparoscopic hysterectomy
      • -
        aged 18–45 years
      • -
        premenopausal women


      Exclusion criteria:

      • -
        personal history of gynaecologic malignancy
      • -
        BRCA1/2 carriers
      • -
        non-English speaking
      Intervention group: Laparoscopic hysterectomy with OS



      Control group:

      Laparoscopic hysterectomy
      30

      (OS 15, non-OS 15)
      OS 36.6 (SD 4.5), non-OS 37.8 (SD 5.0)Ovarian reserve:

      • -
        AMH (ng/ml)
        analysed by the Ultra-Sensitive AMH/MIS ELISA
      6–8 weeks and 3 months
      Ganer Herman et al., 2017 (Ganer Herman et al., 2017)RCTIsraelInclusion criteria:

      • -
        referred for elective caesarean section and who requested tubal ligation for sterilization
      • -
        aged 18–45 years


      Exclusion criteria:

      • -
        previous tubal surgery
      • -
        emergent caesarean section
      • -
        personal history of breast carcinoma
      • -
        familial history of ovarian carcinoma
      • -
        BRCA carrier
      Intervention group:

      Caesarean section with OS



      Control group:

      Caesarean section with tubal ligation
      48

      (OS 22, non-OS 24)
      OS 37.0 (SD 3.9), non-OS 34.3 (SD 4.1)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      6–8 weeks
      Ida et al., 2021 (Ida et al., 2021)Prospective cohort studyJapanInclusion criteria:

      • -
        women who underwent caesarean section after 35 week


      Exclusion criteria:

      • -
        underwent surgeries of the ovary during caesarean section or had previously undergone an ipsilateral oophorectomy
      • -
        defaulted follow-up before the 3-month assessment were excluded from the analysis.
      Intervention group:

      Caesarean section with OS



      Control group:

      Caesarean section
      50

      (OS 20, non-OS 30)
      OS 36.9 (SD 3.9), non-OS 34.6 (SD 5.0)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the two-step immunoassay Lumipulse G AMH (Fujirebio)
      3 months and 6 months
      Lieshout et al., 2018 (Van Lieshout et al., 2018)RCTThe NetherlandsInclusion criteria:

      • -
        indication for either laparoscopic or abdominal hysterectomy for benign indications
      • -
        aged 30–55 years
      • -
        premenopausal women


      Exclusion criteria:

      • -
        history of gynaecological malignancy or salpingitis
      • -
        form of hereditary cancer in the family history
      • -
        germline BRCA 1/2 gene mutation
      • -
        use of hormones in the three weeks prior to surgery
      Intervention group: Laparoscopic hysterectomy with OS



      Control group:

      Laparoscopic hysterectomy
      104

      (OS 52, non-OS 52)
      OS 44.5 (41.3–46.8), non-OS 44.0 (42.3–48.0)Ovarian reserve:

      • -
        AMH (pmol/L)
        analysed by electrochemiluminescence immunoassay (Roche diagnostics)
      6 months
      Morelli et al., 2013 (Morelli et al., 2013)Retrospective cohort studyItalyInclusion criteria:

      • -
        underwent total laparoscopic hysterectomy for abnormal uterine bleeding related to benign pathology


      Exclusion criteria:

      • -
        aged >50 years
      • -
        history of previous uterine or ovarian surgeries
      • -
        family history of ovarian cancer
      • -
        BRCA positive
      • -
        presence of menopausal symptoms
      • -
        irregular menstrual cycle
      • -
        basal FSH value of >20 IU/mL and/or E2 levels >60 pg/mL
      • -
        hormone replacement treatment and/or hormonal contraception for the last 3 months
      • -
        imaging suggestive of ovarian cyst or tubal pathology at transvaginal ultrasound.
      Intervention group: Laparoscopic hysterectomy with OS



      Control group:

      Laparoscopic hysterectomy
      158



      (OS 79, non-OS 79)
      OS 46.5 (SD 2.9), non-OS 45.8 (SD 2.4)Ovarian reserve:

      • -
        AMH (ng/ml)
        analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      • -
        FSH (mIU/ml)
        analysed by chemiluminescence immunoassay COBAS e411 auto-analyser (Roche Diagnostics, USA)
      • -
        AFC (n)
      measured by transvaginal ultrasound
      3 months
      Naaman et al., 2017 (Naaman et al., 2017)Prospective cohort studyIsraelInclusion criteria:

      • -
        elective hysterectomy (without oophorectomy)
      • -
        aged <45 years
      • -
        absence of menopausal symptoms
      • -
        baseline FSH value of <10 IU/mL.


      Exclusion criteria:

      • -
        history of dysfunctional uterine bleeding within the 6 months preceding surgery
      • -
        presurgical evidence of malignancy
      Intervention group: Hysterectomy with fimbriectomy or OS



      Control group:

      Hysterectomy
      38

      (OS 22, non-OS 16)
      OS 45.4 (SD 3.9), non-OS 45.8 (SD 4.1)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)

      • -
        FSH (IU/L)
      analysed by chemiluminescence immunoassay COBAS e411 auto-analyser (Roche Diagnostics, USA)
      6 weeks
      Poonam et al., 2020 (Poonam et al., 2020)RCTIndiaInclusion criteria:

      • -
        indication for hysterectomy
      • -
        premenopausal women
      • -
        aged <45 years
      • -
        baseline FSH value of <10 IU/ml


      Exclusion criteria:

      • -
        gynaecological malignancy
      • -
        ovarian cyst
      • -
        history of hormone treatment in last 3 months
      Intervention group: Hysterectomy with OS



      Control group:

      Hysterectomy
      50

      (OS 25, non-OS 25)
      OS 40.1 (SD 2.5), and 40.0 (SD 3.5)Ovarian reserve:

      • -
        FSH (mIU/ml)
      analysed by and chemiluminescence commercial kit (Beckman Coulter)

      • -
        LH (mIU/ml)
        analysed by and chemiluminescence commercial kit (Beckman Coulter)
      • -
        E2 (pg/ml)
        analysed by and chemiluminescence commercial kit (Beckman Coulter)
      3 months
      Sezik et al. 2007 (Sezik et al., 2007)RCTTurkeyInclusion criteria

      • -
        selected for hysterectomy (without oophorectomy)
      • -
        aged <43 years
      • -
        absence of menopausal symptoms
      • -
        regular menstrual cycles
      • -
        baseline FSH value of <10
      • -
        mean ovarian volume of >5 cm3


      Exclusion criteria:

      • -
        present or past smoking history
      • -
        history of pelvic surgery, cardiovascular disease
      • -
        hormone replacement treatment and/or hormonal contraception for the last 6 months
      • -
        cystic or any solid ovarian mass in transvaginal ultrasound
      Intervention group: Abdominal hysterectomy with OS



      Control group:

      Abdominal hysterectomy
      24

      (OS 12, non-OS 12)
      OS 41.6 (SD 1.7), non-OS 41.1 (SD 1.4)Ovarian reserve:

      • -
        FSH (IU/L)
      measure method not reported in publication

      • -
        LH (IU/L)
        measure method not reported in publication
      • -
        E2 (pg/ml)
      measure method not reported in publication
      6 months
      Song et al., 2017a (Song, Lee, et al., 2017)Retrospective cohort studyKoreaInclusion criteria:

      • -
        aged >38 years
      • -
        regular menstruation
      • -
        available pre- and postoperative measurements for serum AMH


      Exclusion criteria:

      • -
        concurrent ovarian surgery at the time of laparoscopic myomectomy
      • -
        history of prior salpingectomy or salpingo-oophorectomy
      • -
        pregnant or postmenopausal status at the time of surgery
      • -
        preoperative serum AMH <0.20 ng/ml
      • -
        intrauterine device
      • -
        use of any medications such as oral contraceptives, gonadotrophin-releasing hormone agonists, or other sex hormonal agents within 3 months before surgery
      • -
        other endocrine disease
      Intervention group: Laparoscopic myomectomy with OS



      Control group:

      Laparoscopic

      myomectomy
      106

      (OS 41, non-OS 65)
      OS 42.7 (SD 2.7), non-OS 43.1 (SD 2.3)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      3 months
      Song et al., 2017b (Song, Kim, et al., 2017)RCTKoreaInclusion criteria:

      • -
        aged 19–52 years
      • -
        regular menstruation
      • -
        appropriate medical status for laparoscopic surgery (American Society of Anaesthesiologists Physical Status classification 1 or 2)


      Exclusion criteria:

      • -
        history of prior salpingectomy or salpingo-oophorectomy
      • -
        pregnant or menopausal status
      • -
        preoperative serum anti-Mullerian hormone (AMH) <0.30 ng/ml
      • -
        use of hormonal treatments within 3 months before surgery
      • -
        any other endocrine disease (such as uncontrolled thyroid dysfunction, hyperprolactinaemia or Cushing syndrome)
      • -
        any ovarian cysts requiring ovarian surgery
      • -
        any suspicious findings of malignant gynaecologic diseases
      • -
        inability to understand and provide written informed consent
      Intervention group: Laparoscopic hysterectomy with OS



      Control group:

      Laparoscopic hysterectomy
      68

      (OS 34, non-OS 34)
      OS 43.0 (IQR 41–47), non-OS 44.0 (IQR 41–46)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      3 months
      Suneja et al., 2020 (Suneja et al., 2020)Prospective cohort studyIndiaInclusion criteria:

      • -
        aged 35–50 years
      • -
        premenopausal women


      Exclusion criteria:

      • -
        malignant gynaecological disease
      • -
        history of salpingectomy/ ovarian surgery
      • -
        ovarian mass (cystic/solid) on ultrasonography
      Intervention group: Hysterectomy with OS



      Control group:

      Hysterectomy
      40

      (OS 20, non-OS 20)
      OS 40.0 (SD 3.8),

      Non-OS 40.1 (SD 4.2)
      Ovarian reserve:

      • -
        AMH
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      3 months
      Tehranian et al., 2017 (Tehranian et al., 2017)RCTTehranInclusion criteria

      • -
        elective abdominal hysterectomy (without oophorectomy)
      • -
        aged 18–45 years
      • -
        premenopausal women
      • -
        absence of menopausal symptoms
      • -
        baseline FSH value of <10 IU/mL.


      Exclusion criteria:

      • -
        history of pelvic surgery, cystic (>10 mm) or any solid ovarian mass in transvaginal ultrasound
      • -
        hormone replacement treatment and/or hormonal contraception for the last 6 months
      • -
        history of pelvic surgery
      • -
        present or past smoking history
      Intervention group: Abdominal hysterectomy with OS



      Control group:

      Abdominal hysterectomy
      30

      (OS 15, non-OS 15)
      OS 39.8 (SD 3.7), non-OS 40.5 (SD 3.0)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      3 months
      Vahedpour et al., 2020 (Vahedpour et al., 2020)RCTIranInclusion criteria:

      • -
        indication of abdominal hysterectomy
      • -
        aged 30–50 years
      • -
        regular menstruation
      • -
        no history of tubal ligation, oophorectomy, gynaecological malignancies, or hormone replacement therapy


      Exclusion criteria:

      • -
        loss to follow-up
      • -
        oophorectomy during hysterectomy were considered as exclusion criteria
      Intervention group:Abdominal hysterectomy with OS



      Control group:

      Abdominal hysterectomy
      90

      (OS 45, non-OS 45)
      OS 44.4 (SD 4.2), non-OS 45.7 (SD 2.9)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)
      3 months
      Wang et al., 2021 (Wang and Gu, 2021)Retrospective cohort studyChinaInclusion criteria:

      • -
        laparoscopic hysterectomy with ovarian preservation for newly diagnosed and previously untreated benign uterine disease.
      • -
        aged 30–45 years
      • -
        regular menstruation


      Exclusion criteria:

      • -
        personal or family history of malignancies
      • -
        concurrent ovarian or tubal tumors
      • -
        reproductive endocrinology-related diseases
      • -
        failure to follow up after surgery
      • -
        incomplete medical records.
      Intervention group: Laparoscopic hysterectomy with OS



      Control group:

      Laparoscopic hysterectomy
      373

      (OS 171, non-OS 202)
      OS 41.3 (SD 2.7), non-OS 41.5 (SD2.7)Ovarian reserve:

      • -
        AMH (ng/ml)
      analysed by the AMH Gen II enzyme-linked immunosorbent assay (Elisa) kit (Beckman Coulter)

      • -
        FSH (mIU/ml)
      analysed by and chemiluminescence commercial kit (Beckman Coulter)

      • -
        LH (mIU/ml)
      analysed by and chemiuminescence commercial kit (Beckman Coulter)

      • -
        E2 (pg/ml)
      analysed by and chemiluminescence commercial kit (Beckman Coulter)

      • -
        AFC (n)
      measured by transvaginal ultrasound
      3 months
      Between 2007 and 2021, 15 included studies were conducted in eight different countries. Nine were RCTs [
      • Behnamfar F.
      • Jabbari H.
      Evaluation of ovarian function after hysterectomy with or without salpingectomy: a feasible study.
      ,
      • Findley A.D.
      • Siedhoff M.T.
      • Hobbs K.A.
      • Steege J.F.
      • Carey E.T.
      • McCall C.A.
      • Steiner A.Z.
      Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial.
      ,
      • Herman H.Ganer
      • Gluck O.
      • Keidar R.
      • Kerner R.
      • Kovo M.
      • Levran D.
      • Bar J.
      • Sagiv R.
      Ovarian reserve following cesarean section with salpingectomy vs tubal ligation: a randomized trial.
      ,
      • Van Lieshout L.A.M.
      • Pijlman B.
      • Vos M.C.
      • de Groot M.J.M.
      • Houterman S.
      • Coppus S.F.P.J.
      • Harmsen M.G.
      • Vandenput I.
      • Piek J.M.J.
      Opportunistic salpingectomy in women undergoing hysterectomy: results from the HYSTUB randomised controlled trial.
      ,
      • Poonam L.
      • Ranjeet M.
      • Urvashi M.
      • Anil L.
      • Shalini G.
      • Kadam V.K.
      Comparative study of ovarian function in patients undergoing hysterectomy with or without bilateral complete salpingectomy.
      ,
      • Sezik M.
      • Ozkaya O.
      • Demir F.
      • Sezik H.T.
      • Kaya H.
      Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
      ,
      • Song T.
      • Kim M.K.
      • Kim M.L.
      • Jung Y.W.
      • Yun B.S.
      • Seong S.J.
      • Kwon S.H.
      Impact of opportunistic salpingectomy on anti-Müllerian hormone in patients undergoing laparoscopic hysterectomy: a multicentre randomised controlled trial.
      ,
      • Tehranian A.
      • Zangbar R.H.
      • Aghajani F.
      • Sepidarkish M.
      • Rafiei S.
      • Esfidani T.
      Effects of salpingectomy during abdominal hysterectomy on ovarian reserve: a randomized controlled trial.
      ,
      • Vahedpour Z.
      • Abedzadeh- Kalahroudi M.
      • Sehat M.
      • Allamezadeh- Davani S.
      The effects of salpingectomy on the serum level of anti-Müllerian hormone: a single-blind randomized controlled trial.
      ], and six were cohort studies (three prospective [
      • Naaman Y.
      • Hazan Y.
      • Gillor M.
      • Marciano G.
      • Bardenstein R.
      • Shoham Z.
      • Ben-Arie A.
      Does the addition of salpingectomy or fimbriectomy to hysterectomy in premenopausal patients compromise ovarian reserve? A prospective study.
      ,
      • Ida T.
      • Fujiwara H.
      • Taniguchi Y.
      • Kohyama A.
      Longitudinal assessment of anti-Müllerian hormone after cesarean section and influence of bilateral salpingectomy on ovarian reserve.
      ,
      • Suneja A.
      • Garg A.
      • Bhatt S.
      • Guleria K.
      • Madhu S.V.
      • Sharma R.
      Impact of opportunistic salpingectomy on ovarian reserve and vascularity in patients undergoing hysterectomy, indian.
      ] and three retrospective [
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • Di Cello A.
      • Rania E.
      • Lico D.
      • D’Alessandro P.
      • Zullo F.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      ,
      • Song T.
      • Lee S.H.
      • Kim W.Y.
      • Heo E.J.
      • Kim T.J.
      Opportunistic salpingectomy does not affect ovarian reserve or surgical outcomes in patients undergoing laparoscopic myomectomy.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ]). All studies included premenopausal women who underwent OS during abdominal surgery. The majority of the studies (12/15) included women who underwent a hysterectomy for benign indication [
      • Naaman Y.
      • Hazan Y.
      • Gillor M.
      • Marciano G.
      • Bardenstein R.
      • Shoham Z.
      • Ben-Arie A.
      Does the addition of salpingectomy or fimbriectomy to hysterectomy in premenopausal patients compromise ovarian reserve? A prospective study.
      ,
      • Behnamfar F.
      • Jabbari H.
      Evaluation of ovarian function after hysterectomy with or without salpingectomy: a feasible study.
      ,
      • Findley A.D.
      • Siedhoff M.T.
      • Hobbs K.A.
      • Steege J.F.
      • Carey E.T.
      • McCall C.A.
      • Steiner A.Z.
      Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial.
      ,
      • Van Lieshout L.A.M.
      • Pijlman B.
      • Vos M.C.
      • de Groot M.J.M.
      • Houterman S.
      • Coppus S.F.P.J.
      • Harmsen M.G.
      • Vandenput I.
      • Piek J.M.J.
      Opportunistic salpingectomy in women undergoing hysterectomy: results from the HYSTUB randomised controlled trial.
      ,
      • Poonam L.
      • Ranjeet M.
      • Urvashi M.
      • Anil L.
      • Shalini G.
      • Kadam V.K.
      Comparative study of ovarian function in patients undergoing hysterectomy with or without bilateral complete salpingectomy.
      ,
      • Sezik M.
      • Ozkaya O.
      • Demir F.
      • Sezik H.T.
      • Kaya H.
      Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
      ,
      • Song T.
      • Kim M.K.
      • Kim M.L.
      • Jung Y.W.
      • Yun B.S.
      • Seong S.J.
      • Kwon S.H.
      Impact of opportunistic salpingectomy on anti-Müllerian hormone in patients undergoing laparoscopic hysterectomy: a multicentre randomised controlled trial.
      ,
      • Tehranian A.
      • Zangbar R.H.
      • Aghajani F.
      • Sepidarkish M.
      • Rafiei S.
      • Esfidani T.
      Effects of salpingectomy during abdominal hysterectomy on ovarian reserve: a randomized controlled trial.
      ,
      • Vahedpour Z.
      • Abedzadeh- Kalahroudi M.
      • Sehat M.
      • Allamezadeh- Davani S.
      The effects of salpingectomy on the serum level of anti-Müllerian hormone: a single-blind randomized controlled trial.
      ,
      • Suneja A.
      • Garg A.
      • Bhatt S.
      • Guleria K.
      • Madhu S.V.
      • Sharma R.
      Impact of opportunistic salpingectomy on ovarian reserve and vascularity in patients undergoing hysterectomy, indian.
      ,
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • Di Cello A.
      • Rania E.
      • Lico D.
      • D’Alessandro P.
      • Zullo F.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ]. The other three studies concerned women who underwent a caesarean section (n = 2) [
      • Herman H.Ganer
      • Gluck O.
      • Keidar R.
      • Kerner R.
      • Kovo M.
      • Levran D.
      • Bar J.
      • Sagiv R.
      Ovarian reserve following cesarean section with salpingectomy vs tubal ligation: a randomized trial.
      ,
      • Ida T.
      • Fujiwara H.
      • Taniguchi Y.
      • Kohyama A.
      Longitudinal assessment of anti-Müllerian hormone after cesarean section and influence of bilateral salpingectomy on ovarian reserve.
      ] or myomectomy (n = 1) [
      • Song T.
      • Lee S.H.
      • Kim W.Y.
      • Heo E.J.
      • Kim T.J.
      Opportunistic salpingectomy does not affect ovarian reserve or surgical outcomes in patients undergoing laparoscopic myomectomy.
      ]. All studies except one had a control group who underwent the indicated procedure without OS; one study had a control group that underwent tubal ligation instead of OS as sterilization method [
      • Herman H.Ganer
      • Gluck O.
      • Keidar R.
      • Kerner R.
      • Kovo M.
      • Levran D.
      • Bar J.
      • Sagiv R.
      Ovarian reserve following cesarean section with salpingectomy vs tubal ligation: a randomized trial.
      ]. Mean age of the study populations ranged between 35 and 48 years. Study characteristics of included studies are presented in Table 1.

      3.2 Age of menopause

      No studies were found that determined the effect of OS on menopausal age. Two protocols of ongoing trials were identified that prospectively investigate long-term effects of OS on menopausal age [
      • Idahl A.
      • Darelius A.
      • Sundfeldt K.
      • Pålsson M.
      • Strandell A.
      Hysterectomy and opportunistic salpingectomy (HOPPSA): study protocol for a register-based randomized controlled trial.
      ,
      • Gelderblom M.E.
      • IntHout J.
      • Hermens R.P.M.
      • Coppus S.F.P.J.
      • Ebisch I.
      • van Ginkel A.A.
      • van de Laar R.
      • de Lange N.
      • Maassen M.
      • Pijlman B.
      • Smedts D.
      • Vos M.C.
      • Beerendonk C.C.M.
      • de Hullu J.A.
      • Piek J.M.J.
      STop OVarian CAncer (STOPOVCA) young: protocol for a multicenter follow-up study to determine the long-term effects of opportunistic salpingectomy on age at menopause.
      ].

      3.3 Ovarian reserve

      3.3.1 Anti-Müllerian hormone (AMH)

      The majority of included studies (n = 12) [
      • Naaman Y.
      • Hazan Y.
      • Gillor M.
      • Marciano G.
      • Bardenstein R.
      • Shoham Z.
      • Ben-Arie A.
      Does the addition of salpingectomy or fimbriectomy to hysterectomy in premenopausal patients compromise ovarian reserve? A prospective study.
      ,
      • Findley A.D.
      • Siedhoff M.T.
      • Hobbs K.A.
      • Steege J.F.
      • Carey E.T.
      • McCall C.A.
      • Steiner A.Z.
      Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial.
      ,
      • Herman H.Ganer
      • Gluck O.
      • Keidar R.
      • Kerner R.
      • Kovo M.
      • Levran D.
      • Bar J.
      • Sagiv R.
      Ovarian reserve following cesarean section with salpingectomy vs tubal ligation: a randomized trial.
      ,
      • Van Lieshout L.A.M.
      • Pijlman B.
      • Vos M.C.
      • de Groot M.J.M.
      • Houterman S.
      • Coppus S.F.P.J.
      • Harmsen M.G.
      • Vandenput I.
      • Piek J.M.J.
      Opportunistic salpingectomy in women undergoing hysterectomy: results from the HYSTUB randomised controlled trial.
      ,
      • Song T.
      • Kim M.K.
      • Kim M.L.
      • Jung Y.W.
      • Yun B.S.
      • Seong S.J.
      • Kwon S.H.
      Impact of opportunistic salpingectomy on anti-Müllerian hormone in patients undergoing laparoscopic hysterectomy: a multicentre randomised controlled trial.
      ,
      • Tehranian A.
      • Zangbar R.H.
      • Aghajani F.
      • Sepidarkish M.
      • Rafiei S.
      • Esfidani T.
      Effects of salpingectomy during abdominal hysterectomy on ovarian reserve: a randomized controlled trial.
      ,
      • Vahedpour Z.
      • Abedzadeh- Kalahroudi M.
      • Sehat M.
      • Allamezadeh- Davani S.
      The effects of salpingectomy on the serum level of anti-Müllerian hormone: a single-blind randomized controlled trial.
      ,
      • Ida T.
      • Fujiwara H.
      • Taniguchi Y.
      • Kohyama A.
      Longitudinal assessment of anti-Müllerian hormone after cesarean section and influence of bilateral salpingectomy on ovarian reserve.
      ,
      • Suneja A.
      • Garg A.
      • Bhatt S.
      • Guleria K.
      • Madhu S.V.
      • Sharma R.
      Impact of opportunistic salpingectomy on ovarian reserve and vascularity in patients undergoing hysterectomy, indian.
      ,
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • Di Cello A.
      • Rania E.
      • Lico D.
      • D’Alessandro P.
      • Zullo F.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      ,
      • Song T.
      • Lee S.H.
      • Kim W.Y.
      • Heo E.J.
      • Kim T.J.
      Opportunistic salpingectomy does not affect ovarian reserve or surgical outcomes in patients undergoing laparoscopic myomectomy.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ] investigated the effect of OS on ovarian reserve through AMH.
      Fig. 2
      Fig. 2Forest plots presenting random-effects meta-analyses of mean change in ovarian reserve comparing women who did and did not have OS.
      Anti-Müllerian Hormone (AMH), Antral Follicle Count (AFC), Earlier onset of menopause (EMP), Estradiol (E2), Follicle Stimulating Hormone (FSH), Luteinizing Hormone (LH), Opportunistic Salpingectomy (OS).
      Fig. 3
      Fig. 3Forest plots presenting subgroup random-effects meta-analyses of mean change in AMH (ng/ml) comparing women who did and did not have OS.
      Anti-Müllerian Hormone (AMH), Earlier onset of menopause (EMP), Opportunistic Salpingectomy (OS).
      As shown in Fig. 2a, meta-analysis of the 12 studies that investigated the effect of OS on ovarian reserve through changes in AMH did not result in a statistically significant difference in reduction of AMH compared to no OS (MD −0.07 ng/ml, 95 % CI −0.18;0.05; p = 0.22, I2 = 56 %, 1082 participants). Funnel plot did not suggest any presence of publication bias. Since I2 indicated moderate heterogeneity between studies, a sensitivity analysis was conducted removing outliers from the analysis. After exclusion of the study of Song et al., 2017b [
      • Song T.
      • Kim M.K.
      • Kim M.L.
      • Jung Y.W.
      • Yun B.S.
      • Seong S.J.
      • Kwon S.H.
      Impact of opportunistic salpingectomy on anti-Müllerian hormone in patients undergoing laparoscopic hysterectomy: a multicentre randomised controlled trial.
      ], results did not notably change (MD 0.01 ng/ml, with 95 % CI −0.02;0.04; p = 0.53, I2 = 0 %). Subgroup analyses for study design, indicated procedure, duration of follow-up and RoB did not show any significant differences in effect of OS on AMH (test for subgroup differences p = 0.29; p = 0.33; p = 0.62; p = 0.50; Fig. 3). Meta-regression did not result in a statistically significant association between mean age and the treatment effect size (p = 0.44, Fig. S1).

      3.3.2 Antral follicle count (AFC)

      Two studies investigated the effect of OS on change in AFC assessed during early follicular phase [
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • Di Cello A.
      • Rania E.
      • Lico D.
      • D’Alessandro P.
      • Zullo F.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ]. Both studies were retrospectively performed in patients who underwent hysterectomy. Meta-analysis did not result in statistically significant difference in reduction of AFC in patients who underwent OS compared to no OS (MD 0.20 n, 95 % CI −4.91;5.30, p = 0.71, I2 = 78 %, 531 participants, Fig. 2b). Funnel plot did not suggest any presence of publication bias.
      Fig. 4
      Fig. 4Unweighted risk assessment of all included studies by ROBINS-I and RoB-II.

      3.3.3 Estradiol (E2)

      Three studies investigated the effect of OS on ovarian reserve by E2 assessed during early follicular phase [
      • Poonam L.
      • Ranjeet M.
      • Urvashi M.
      • Anil L.
      • Shalini G.
      • Kadam V.K.
      Comparative study of ovarian function in patients undergoing hysterectomy with or without bilateral complete salpingectomy.
      ,
      • Sezik M.
      • Ozkaya O.
      • Demir F.
      • Sezik H.T.
      • Kaya H.
      Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ]. All three studies were performed in patients who underwent hysterectomy as indicated procedure. E2 levels would decrease when menopause occurs and increase when ovarian reserve is diminished due to early development of a dominant follicle. Meta-analysis of these three studies did not result in a statistically significant difference in neither reduction nor increase of E2 compared to no OS (MD 3.97 pg/ml, 95 % CI −0.92;8.86; p = 0.11, I2 = 0 %, 447 participants, Fig. 2c). Funnel plot did not suggest any presence of publication bias. Subgroup analyses for study design, duration of follow-up and RoB showed no significant differences in effect of OS on E2 (test of subgroup differences p = 0.66; p = 0.92; p = 0.66; Fig. S2).

      3.3.4 Follicle stimulating hormone (FSH)

      Six studies investigated the effect of OS on ovarian reserve by FSH assessed during early follicular phase [
      • Naaman Y.
      • Hazan Y.
      • Gillor M.
      • Marciano G.
      • Bardenstein R.
      • Shoham Z.
      • Ben-Arie A.
      Does the addition of salpingectomy or fimbriectomy to hysterectomy in premenopausal patients compromise ovarian reserve? A prospective study.
      ,
      • Behnamfar F.
      • Jabbari H.
      Evaluation of ovarian function after hysterectomy with or without salpingectomy: a feasible study.
      ,
      • Poonam L.
      • Ranjeet M.
      • Urvashi M.
      • Anil L.
      • Shalini G.
      • Kadam V.K.
      Comparative study of ovarian function in patients undergoing hysterectomy with or without bilateral complete salpingectomy.
      ,
      • Sezik M.
      • Ozkaya O.
      • Demir F.
      • Sezik H.T.
      • Kaya H.
      Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
      ,
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • Di Cello A.
      • Rania E.
      • Lico D.
      • D’Alessandro P.
      • Zullo F.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ]. Indicated procedure for included patients was hysterectomy in all studies. Meta-analysis assessing the effect of OS did not result in a statistically significant difference in increase of FSH compared to no OS (MD 0.33mIU/ml, 95 % CI −0.15;0.81; p = 0.14, I2 = 49 %, 677 participants, Fig. 2d). Funnel plot did not suggest any presence of publication bias. Subgroup analyses for study design, duration of follow-up, and RoB did not result in significant differences in effect of OS on FSH (test of subgroup differences p = 0.08; p = 0.17; p = 0.13; Fig. S3).

      3.3.5 Luteinizing hormone (LH)

      Four studies investigated the effect of OS on ovarian reserve through LH in patients who underwent hysterectomy [
      • Behnamfar F.
      • Jabbari H.
      Evaluation of ovarian function after hysterectomy with or without salpingectomy: a feasible study.
      ,
      • Poonam L.
      • Ranjeet M.
      • Urvashi M.
      • Anil L.
      • Shalini G.
      • Kadam V.K.
      Comparative study of ovarian function in patients undergoing hysterectomy with or without bilateral complete salpingectomy.
      ,
      • Sezik M.
      • Ozkaya O.
      • Demir F.
      • Sezik H.T.
      • Kaya H.
      Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
      ,
      • Wang S.
      • Gu J.
      The effect of prophylactic bilateral salpingectomy on ovarian reserve in patients who underwent laparoscopic hysterectomy.
      ]. All LH levels were assessed during early follicular phase. The funnel plot did not suggest any presence of publication bias. Meta-analysis did not result in a statistically significant difference in increase of LH compared to no OS (MD 0.03mIU/ml; 95 % CI −0.47;0.53; p = 0.85, I2 = 40 %, 481 participants, Fig. 2e). Subgroup analyses for study design, duration of follow-up, and risk of bias showed no significant differences in effect of OS on LH (test of subgroup differences p = 0.75; p = 0.75; p = 0.20; Fig. S4).

      3.4 Risk assessment

      Overall risk of bias of the included studies was mainly assessed as moderate/some concerns. The majority of included studies had a low risk of bias from randomization, selection of participants, classification of intervention, deviations from intended interventions and measurement of outcome (Fig. 4). We considered seven studies to be at moderate risk/some concerns regarding bias due to missing data since the loss to follow-up was >5 % and information on handling missing data and performance of a sensitivity analysis was missing. In addition, three other studies did not mention any information on missing data or loss to follow-up. Risk of selective reporting was considered moderate in three studies due to no or post hoc registration of trial protocol, and high in three studies due to change or omission of intended outcome. Fig. 4 provides the quality assessment of included studies. An overview on complete risk assessment of each included study per domain is given in Fig. S5.

      4. Discussion

      Systematic review and meta-analyses were conducted to determine the effect of OS on onset of menopause compared to no OS. At present, no studies are published concerning the effect of OS on age of menopausal onset. However, our analyses did not show a significant short-term impact of OS on reduction of ovarian reserve measured by changes in surrogate markers AMH, AFC, E2, FSH and LH during abdominal surgeries compared to no OS.
      OS has the potential risk of damaging ovarian (micro)circulation and thereby compromising the blood flow to the ovaries which may lead to an earlier onset of menopause. Ovarian reserve can be useful as predictor for age at menopause, since ovarian reserve will decline as women mature [
      • Lambalk C.B.
      • van Disseldorp J.
      • de Koning C.H.
      • Broekmans F.J.
      Testing ovarian reserve to predict age at menopause.
      ]. However, given that the damage may have only a subtle impact, a reduction in ovarian perfusion and thereby decrease in steroid production and follicular development could occur without short-term reflection in diminished ovarian reserve [
      • Kotlyar A.
      • Gingold J.
      • Shue S.
      • Falcone T.
      The effect of salpingectomy on ovarian function.
      ]. As the risk of all-cause mortality increases with each year of earlier menopause [
      • Ossewaarde M.E.
      • Bots M.L.
      • Verbeek A.L.M.
      • Peeters P.H.M.
      • Van Der Graaf Y.
      • Grobbee D.E.
      • Van Der Schouw Y.T.
      Age at menopause, cause-specific mortality and total life expectancy.
      ], investigating the actual effect of OS on the menopausal age is vital.
      A decrease in AMH and AFC, and elevation of FSH may indicate diminished ovarian reserve and consequently earlier onset of menopause. [49]Given the unclear associations between E2 and LH with age, these surrogate markers of ovarian reserve do not appear to be good predictors of age of menopause [
      • Lambalk C.B.
      • van Disseldorp J.
      • de Koning C.H.
      • Broekmans F.J.
      Testing ovarian reserve to predict age at menopause.
      ]. AMH is currently the most indicative marker to estimate ovarian reserve and predict menopausal age. However, AMH levels should be interpreted with caution as also AMH may vary due to the use of hormonal contraception [
      • Dólleman M.
      • Verschuren W.M.M.
      • Eijkemans M.J.C.
      • Dollé M.E.T.
      • Jansen E.H.J.M.
      • Broekmans F.J.M.
      • Van Der Schouw Y.T.
      Reproductive and lifestyle determinants of anti-müllerian hormone in a large population-based study.
      ], and appears a weak predictor for onset of menopause in older women [
      • Dólleman M.
      • Depmann M.
      • Eijkemans M.J.C.
      • Heimensem J.
      • Broer S.L.
      • Van Der Stroom E.M.
      • Laven J.S.E.
      • Van Rooij I.A.J.
      • Scheffer G.J.
      • Peeters P.H.M.
      • Van Der Schouw Y.T.
      • Lambalk C.B.
      • Broekmans F.J.M.
      Anti-Müllerian hormone is a more accurate predictor of individual time to menopause than mother's age at menopause.
      ]. Nevertheless, other used surrogate markers such as FSH and AFC have a high inter- and intracycle variability and therefore lower sensitivity [
      • Penzias A.
      • Azziz R.
      • Bendikson K.
      • Falcone T.
      • Hansen K.
      • Hill M.
      • Hurd W.
      • Jindal S.
      • Kalra S.
      • Mersereau J.
      • Racowsky C.
      • Rebar R.
      • Reindollar R.
      • Shannon C.N.
      • Steiner A.
      • Stovall D.
      • Tanrikut C.
      • Taylor H.
      • Yauger B.
      Testing and interpreting measures of ovarian reserve: a committee opinion.
      ]. Moreover, elevation of FSH is a late predictor of menopause as it start to increase only in the last 10 years before menopause [
      • Lambalk C.B.
      • van Disseldorp J.
      • de Koning C.H.
      • Broekmans F.J.
      Testing ovarian reserve to predict age at menopause.
      ].
      Lack of long-term evidence may be explained by recommendations regarding OS issued in 2011, since the fallopian tube as origin for HGSC became known early in 21st century [
      • Piek J.M.J.
      • Verheijen R.H.M.
      • Kenemans P.
      • Massuger L.F.
      • Bulten H.
      • Van Diest P.J.
      BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis.
      ,
      • Ntoumanoglou-Schuiki A.
      • Tomasch G.
      • Laky R.
      • Taumberger N.
      • Bjelic-Radisic V.
      • Tamussino K.
      Opportunistic prophylactic salpingectomy for prevention of ovarian cancer: what do national societies advise?.
      ]. Women eligible for OS are primarily between the age of 35–45, meaning it will take them years to enter menopause, and at least a decade to collect data. The ongoing SALSTER (NCT0386080) and STOPOVCAyoung [
      • Gelderblom M.E.
      • IntHout J.
      • Hermens R.P.M.
      • Coppus S.F.P.J.
      • Ebisch I.
      • van Ginkel A.A.
      • van de Laar R.
      • de Lange N.
      • Maassen M.
      • Pijlman B.
      • Smedts D.
      • Vos M.C.
      • Beerendonk C.C.M.
      • de Hullu J.A.
      • Piek J.M.J.
      STop OVarian CAncer (STOPOVCA) young: protocol for a multicenter follow-up study to determine the long-term effects of opportunistic salpingectomy on age at menopause.
      ] (NCT04757922) trials will examine the effect of OS as sterilization method on the age at menopause compared to tubal ligation (SALSTER) and tubal ligation/no sterilization (STOPOVCAyoung). Age at menopause will be determined through questionnaires on bleeding pattern (SALSTER) and menstruation cycle (STOPOVCAyoung). Results of these trials are to be expected in about 15 to 30 years.
      Our findings are in contrast with the retrospective study of Collins et al., 2019 that indicated an increased risk of climacteric symptoms one year after OS during hysterectomy compared to hysterectomy alone [
      • Collins E.
      • Strandell A.
      • Granåsen G.
      • Idahl A.
      Menopausal symptoms and surgical complications after opportunistic bilateral salpingectomy, a register-based cohort study.
      ]. Nonetheless, our findings reflect those of Hanley et al., 2020 who found no differences regarding hormone replacement therapy use and physicians' visits for menopause between OS during hysterectomy or as sterilization method compared to no OS [
      • Hanley G.E.
      • Kwon J.S.
      • McAlpine J.N.
      • Huntsman D.G.
      • Finlayson S.J.
      • Miller D.
      Examining indicators of early menopause following opportunistic salpingectomy: a cohort study from British Columbia, Canada.
      ]. In accordance with the present study, van Lieshout et al., 2019 showed no significant difference in ovarian reserve by AMH after OS during hysterectomy compared to hysterectomy alone [
      • van Lieshout L.A.M.
      • Steenbeek M.P.
      • De Hullu J.A.
      • Vos M.C.
      • Houterman S.
      • Wilkinson J.
      • Piek J.M.J.
      Hysterectomy with opportunistic salpingectomy versus hysterectomy alone.
      ]. Notably, this study demonstrated a trend towards decreased AMH in women who underwent hysterectomy with OS, which might indicate earlier onset of menopause with a maximum of two years [
      • van Lieshout L.A.M.
      • Steenbeek M.P.
      • De Hullu J.A.
      • Vos M.C.
      • Houterman S.
      • Wilkinson J.
      • Piek J.M.J.
      Hysterectomy with opportunistic salpingectomy versus hysterectomy alone.
      ]. The association between reduction in ovarian reserve and actual onset of menopause is yet unclear [
      • De Kat A.C.
      • Van Der Schouw Y.T.
      • Eijkemans M.J.C.
      • Broer S.L.
      • Verschuren W.M.M.
      • Broekmans F.J.M.
      Can menopause prediction be improved with multiple AMH measurements? Results from the prospective Doetinchem cohort study.
      ]. Future studies on intermediate term such as the HOPPSA trial [
      • Idahl A.
      • Darelius A.
      • Sundfeldt K.
      • Pålsson M.
      • Strandell A.
      Hysterectomy and opportunistic salpingectomy (HOPPSA): study protocol for a register-based randomized controlled trial.
      ] are therefore recommended to investigate if OS increases climacteric symptoms and HRT use, and to monitor whether the benefits continue to outweigh the risks.
      With respect to whether age at OS is related to earlier menopause, meta-regression did not show an association between mean age and the effect of OS. However, the power of meta-regression is known to be poor [
      • Belias M.
      • Rovers M.M.
      • Reitsma J.B.
      • Debray T.P.A.
      • Inthout J.
      Statistical approaches to identify subgroups in meta-analysis of individual participant data: a simulation study.
      ] and only data on mean ages of study populations were used instead of individual ages. Previous studies have shown that physicians experience a barrier to counsel for OS especially with young women as they might have a reduced blood supply to the ovaries for a prolonged period of time [
      • Gelderblom M.E.
      • Stevens K.Y.R.
      • Houterman S.
      • Weyers S.
      • Schoot B.C.
      Prediction models in gynaecology: transparent reporting needed for clinical application.
      ]. A potentially adverse effect on ovarian reserve and menopause would therefore accumulate, increasing the risk on long-term health consequences [
      • Ossewaarde M.E.
      • Bots M.L.
      • Verbeek A.L.M.
      • Peeters P.H.M.
      • Van Der Graaf Y.
      • Grobbee D.E.
      • Van Der Schouw Y.T.
      Age at menopause, cause-specific mortality and total life expectancy.
      ]. Yet, there are also theories suggesting that young women who undergo OS are actually less at risk because they will form anastomoses to allow their ovaries to function as desired [
      • Sezik M.
      • Ozkaya O.
      • Demir F.
      • Sezik H.T.
      • Kaya H.
      Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
      ]. However, both hypotheses require validation through further long-term follow-up studies.
      Our findings might suggest no major impact on earlier onset of menopause is to be expected. Therefore, including the option of OS during counselling in premenopausal women with completed childbearing seems justified. Counselling (material) should contain information concerning the absence of evidence on the effect of OS on age at menopause, until long-term research is conducted. In this way, women can weigh the benefits and risks of OS themselves, and make a well-informed decision. A counselling tool such as a decision aid developed within the STOPOVCA-implementation project could support both women and professionals in this decision process [
      • van Lieshout L.A.M.
      • Gelderblom M.E.
      • de Hullu J.A.
      • The R.
      • van Ginkel A.A.
      • Oerlemans A.J.M.
      • Smeets K.M.W.H.
      • Schreurs M.P.H.
      • Piek J.M.J.
      • Hermens R.P.M.G.
      Primary prevention of ovarian cancer: a patient decision aid for opportunistic salpingectomy.
      ].

      4.1 Strengths and limitations

      This study provides a clear overview of the current evidence regarding OS and its effect on menopause by menopausal age and ovarian reserve. We opted for ovarian reserve measured by mean change-from-baseline in hormone level as this allows us to determine the actual effect of OS on potential reduction in ovarian reserve. Comparing solely postoperative surrogate levels, does not take into account preoperative levels, which can make it difficult to interpret the results. Moreover, we included all abdominal surgical procedures in which OS could be performed, and both RCT's and cohort studies in order to evaluate the evidence comprehensively. A potential drawback of this strength is that study populations of included studies are heterogeneous due to different indicated procedures. Several studies included hysterectomy of which is known that itself results in an earlier menopause [
      • Moorman P.G.
      • Myers E.R.
      • Schildkraut J.M.
      • Iversen E.S.
      • Wang F.
      • Warren N.
      Effect of hysterectomy with ovarian preservation on ovarian function.
      ] and sharp drop of AMH-levels on short-term [
      • Hehenkamp W.J.K.
      • Volkers N.A.
      • Broekmans F.J.M.
      • de Jong F.H.
      • Themmen A.P.N.
      • Birnie E.
      • Reekers J.A.
      • Ankum W.M.
      Loss of ovarian reserve after uterine artery embolization: a randomized comparison with hysterectomy.
      ]. Additionally, two studies were included within meta-analysis of AMH with a pregnant/postpartum study population. Naturally, AMH decreases during pregnancy indicating ovarian suppression and increases four days postpartum [
      • Pankhurst M.W.
      • Clark C.A.
      • Zarek J.
      • Laskin C.A.
      • McLennan I.S.
      Changes in circulating ProAMH and total AMH during healthy pregnancy and post-partum: a longitudinal study.
      ]. This could result in a greater positive change in AMH potentially shading any negative effect by OS on ovarian reserve. Yet, subgroup analysis investigating the effect of the indicated procedure did not result in significant differences.
      Another limitation of the study is that the longest follow-up of nine months was performed by only one study, and many had a follow-up of maximum 3 months. Since a previous study has shown recovered AMH levels six months after hysterectomy [
      • Hehenkamp W.J.K.
      • Volkers N.A.
      • Broekmans F.J.M.
      • de Jong F.H.
      • Themmen A.P.N.
      • Birnie E.
      • Reekers J.A.
      • Ankum W.M.
      Loss of ovarian reserve after uterine artery embolization: a randomized comparison with hysterectomy.
      ], our findings could even be overestimated to the detriment of OS.

      5. Conclusion

      To date, clear evidence on the effect of OS on menopausal onset is lacking. Since earlier onset of menopause may have serious consequences for women's health, accurate data on the effect of OS on menopausal age is vital in determination of whether the substantial benefits of OS outweigh its long-term risks. Therefore, further research is an essential next step to confirm the absence of major effects of OS on menopausal onset. However, our findings show no reduction of ovarian reserve by OS on short-term. For this reason shared decision making on OS in premenopausal women with completed childbearing seems justified with the caveat that counselling contains information concerning the lack of evidence on long-term consequences on menopausal onset.
      Supplementary Fig. S2
      Supplementary Fig. S2Forest plots presenting subgroup random-effects meta-analyses of mean change in E2 (pg/ml) comparing women who did and did not have OS Estradiol (E2), Earlier onset of menopause (EMP), Opportunistic salpingectomy (OS).
      Supplementary Fig. S3
      Supplementary Fig. S3Forest plots presenting subgroup random-effects meta-analyses of mean change in FSH (mIU/ml) comparing women who did and did not have OS Follicle Stimulating Hormone (FSH), earlier onset of menopause (EMP), Opportunistic Salpingectomy (OS).
      Supplementary Fig. S4
      Supplementary Fig. S4Forest plots presenting subgroup random-effects meta-analyses of mean change in LH (mIU/ml) comparing women who did and did not have OS Luteinizing Hormone (LH), earlier onset of menopause (EMP), Opportunistic Salpingectomy (OS).

      Contributors

      M.E. Gelderblom contributed to the design of the study, performed the screening, data collection, and risk assessment of included studies, contributed to data analysis and interpretation, and drafted and edited the manuscript.
      J. IntHout contributed to data analysis and interpretation, and revision of the manuscript.
      L. Dagovic performed the screening, data collection, and risk assessment of included studies, and contributed to revision of the manuscript.
      R.P.M.G. Hermens contributed to the design of the study, and revision of the manuscript.
      J.M.J. Piek contributed to the design of the study and to revision of the manuscript.
      J.A. de Hullu contributed to the design of the study and to revision of the manuscript.
      All authors contributed to the discussion section of the manuscript, have approved the final version of the manuscript submitted for peer review, and are in agreement to be accountable for all aspects of the work.

      Funding

      No funding from an external source was received for the preparation of this review.
      Provenance and peer review.
      This article was not commissioned and was externally peer reviewed.

      Declaration of competing interest

      The authors declare that they have no competing interest.

      Acknowledgements

      The authors sincerely thank Y. Naaman for his contribution to our study by providing additional data of his research reported in Naaman et al., 2016. Moreover, we thank OnYing Chan (Radboud) for her contribution by helping to conduct our electronic medical search.

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