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Surgical Outcomes in Patients With Endometriosis: A Systematic Review

Open AccessPublished:November 09, 2019DOI:https://doi.org/10.1016/j.jogc.2019.08.004

      Abstract

      Objective

      Among women treated surgically for endometriosis-associated pain, comprehensive data are lacking on the proportions of patients who experience little or no symptom relief, develop recurrent symptoms, or require further surgical treatment for endometriosis. The aim of this study was to assess the efficacy of surgical procedures used to treat endometriosis-associated pain.

      Methods

      Medline and Embase were searched on October 13, 2016. Articles referring to women undergoing surgery for the treatment of endometriosis-associated pain were screened by two independent investigators. For each included treatment arm, data were extracted for the proportion of patients reporting partial or no improvement after surgery for endometriosis-associated pain, pain recurrence, or requirement for further surgery.

      Results

      A total of 38 studies were included. Most studies did not report relevant outcomes to evaluate pain (71.1%) and recurrent surgery (68.4%). Of the women who underwent lesion excision, 11.8% reported no improvement in pain, and 22.6% underwent further surgery. Postoperative pain, recurrent pain, and adverse events were reported by 34.3%, 28.7%, and 14.8%, respectively, of patients who underwent excision or ablation of endometriosis combined with pelvic denervation and in 25.0%, 15.8%, and 8.1% of women who underwent lesion excision alone. Of the patients who were treated surgically for deep endometriosis affecting the bowel and/or bladder, 7.0% experienced recurrent symptoms, and 4.1% underwent further surgery.

      Conclusion

      This review supports the findings of previous studies and highlights the need for standardized reporting and more detailed follow-up after surgery for endometriosis-associated pain.

      Résumé

      Objectif

      Pour les femmes ayant reçu un traitement chirurgical des douleurs liées à l'endométriose, on observe un manque de données sur la proportion de patientes qui éprouvent un soulagement partiel ou inexistant de leurs symptômes, qui connaissent une récidive des symptômes ou qui nécessitent des traitements chirurgicaux supplémentaires. Cette étude visait à évaluer l'efficacité des interventions chirurgicales utilisées pour traiter les douleurs liées à l'endométriose.

      Méthodologie

      Des recherches ont été menées dans Medline et Embase le 13 octobre 2016. Deux chercheurs indépendants ont évalué des articles faisant référence aux femmes qui subissent une intervention chirurgicale pour traiter les douleurs liées à l'endométriose. Pour chaque volet de traitement retenu, les données ont été extraites pour la portion de patientes qui rapportaient une amélioration partielle ou inexistante après une intervention chirurgicale pour traiter les douleurs liées à l'endométriose, présentaient une récidive des douleurs ou nécessitaient une intervention chirurgicale supplémentaire.

      Résultats

      Un total de 38 études ont été retenues. La plupart des études ne rapportaient pas de données pertinentes pour évaluer les douleurs (71,1 %) ni les interventions chirurgicales supplémentaires (68,4 %). Parmi les femmes qui ont subi une excision des lésions, 11,8 % ont rapporté ne ressentir aucune amélioration des douleurs et 22,6 % ont dû subir une intervention chirurgicale supplémentaire. On a rapporté des douleurs postopératoires, des douleurs récidivantes et des événements défavorables respectivement chez 34,3 %, 28,7 % et 14,8 % des patientes qui ont subi une excision ou une ablation de l'endométriose combinée à une dénervation pelvienne et chez 25,0 %, 15,8 % et 8,1 % des patientes qui ont subi une excision des lésions seulement. Des patientes qui ont subi un traitement chirurgical d'une atteinte endométriosique profonde du côlon et/ou de la vessie, 7,0 % ont connu une récidive des symptômes et 4,1 % ont subi une intervention chirurgicale supplémentaire.

      Conclusion

      Cette revue corrobore les conclusions d'études précédentes et fait ressortir le besoin d'uniformisation des déclarations et d'un suivi postopératoire détaillé après un traitement chirurgical des douleurs liées à l'endométriose.

      Keywords

      INTRODUCTION

      Endometriotic lesions most commonly form on the peritoneum, ovaries, bowel, and bladder and can cause adhesions between pelvic organs.
      • Fauconnier A
      • Chapron C
      Endometriosis and pelvic pain: epidemiological evidence of the relationship and implications.
      For many women, endometriosis-associated pain (chronic pelvic pain, dysmenorrhoea, dyspareunia, dysuria, dyschezia) can have a significant impact on health-related quality of life.
      • Nnoaham KE
      • Hummelshoj L
      • Webster P
      • et al.
      Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries.
      • Sinaii N
      • Plumb K
      • Cotton L
      • et al.
      Differences in characteristics among 1,000 women with endometriosis based on extent of disease.
      The recommended surgical approach to manage endometriosis-associated pain depends on the type of lesion. Surgical excision or ablation is recommended for superficial lesions and full excision for deep endometriosis (previously termed “deep infiltrating endometriosis”) and endometriomas.
      • Johnson NP
      • Hummelshoj L
      World Endometriosis Society Montpellier Consortium
      Consensus on current management of endometriosis.
      In some cases, radical surgery may be required to alleviate endometriosis-associated pain, such as pre-sacral neurectomy or hysterectomy with removal of the ovaries.
      • Dunselman GA
      • Vermeulen N
      • Becker C
      • et al.
      ESHRE guideline: management of women with endometriosis.
      Conservative surgery, in which the uterus and at least one ovary are preserved, is the preferred approach in women who want to preserve fertility.
      • Kim SH
      • Chae HD
      • Kim CH
      • et al.
      Update on the treatment of endometriosis.
      Medical treatments such as analgesics and hormonal agents may also be given as a preoperative or postoperative adjunct to surgery or as an alternative treatment strategy.
      • Johnson NP
      • Hummelshoj L
      World Endometriosis Society Montpellier Consortium
      Consensus on current management of endometriosis.
      In clinical studies, 20% to 38% of patients reported no improvement in endometriosis-associated pain following surgery.
      • Abbott J
      • Hawe J
      • Hunter D
      • et al.
      Laparoscopic excision of endometriosis: a randomized, placebo-controlled trial.
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      The probability of pain recurrence was 24% at 3 years.
      • Vercellini P
      • Fedele L
      • Aimi G
      • et al.
      Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classification system.
      However, comprehensive data are lacking for the proportion of patients who experience little or no pain relief, develop recurrent pain, or require further surgical treatment for endometriosis. Comparisons of these parameters are hampered by a lack of standardized approaches to postsurgical therapy and by sparse use of validated, standardized assessment tools in endometriosis trials.
      The aim of this systematic review was to assess the response, recurrence, and reoperation rates for the full range of surgical procedures used to treat endometriosis-associated pain to determine their effectiveness and evaluate the need for new therapies.

      METHODS

       Search Strategy

      Medline and Embase were searched using Ovid on October 13, 2016, to identify all studies reporting response to surgery for the treatment of endometriosis-associated pain (Figure); the search strings are provided in online Table 1. After removal of duplicates, all identified references were screened and categorized by two independent investigators. Prospective or retrospective studies evaluating the surgical treatment of endometriosis and reporting any of the following outcomes of interest were included: treatment response according to type of surgery or location of lesions, recurrence rate of endometriosis-associated pain or lesions, and number of women requiring further surgical treatment.
      Figure
      FigurePRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flow diagram of systematic searches and selection process.
      AE: adverse event.
      Exclusion criteria were as follows: studies with fewer than 50 patients, follow-up duration of less than 6 months, studies of patients who received hormonal treatment after surgery, and articles that did not investigate endometriosis-associated pain as an outcome (Figure). The search was limited to English-language articles with an abstract available. No limit was set for the year of publication. The protocol has been registered with PROSPERO (ID: CRD42015017831). Articles were initially screened by title only; those meeting the exclusion criteria were removed. The remaining references were screened on the basis of abstracts and/or full text.

       Data Analysis

      For articles that were included in the study, data were extracted to calculate the proportions of patients reporting partial or no improvement in endometriosis-associated pain after surgery. Data for endometriosis-associated pain recurrence, reoperation rates, and adverse events (AEs) following surgery were also obtained.
      For data analysis, papers were categorized into seven groups, according to type of intervention: diagnostic surgery, lesion excision (including endometrioma excision), lesion ablation, endometrioma drainage without cyst excision (herein referred to as the endometrioma drainage group), pelvic denervation, hysterectomy with or without ovarian preservation, and excision of deep endometriosis. Online Table 2 lists all the surgical techniques by group. Patients in the diagnostic surgery group underwent laparoscopy for diagnostic purposes but did not receive any surgical treatment.
      In this review article, the findings are presented as medians (ranges are shown only in the tables and figures) or as single values.

      RESULTS

       Studies Meeting the Eligibility Criteria

      Of 2185 articles identified, 38 were included in this study
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Ruffo G
      • Scopelliti F
      • Manzoni A
      • et al.
      Long-term outcome after laparoscopic bowel resections for deep infiltrating endometriosis: a single-center experience after 900 cases.
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Mossa B
      • Ebano V
      • Tucci S
      • et al.
      Laparoscopic surgery for the management of ovarian endometriomas.
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Brouwer R
      • Woods RJ
      Rectal endometriosis: results of radical excision and review of published work.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      • Milingos S
      • Protopapas A
      • Kallipolitis G
      • et al.
      Endometriosis in patients with chronic pelvic pain: is staging predictive of the efficacy of laparoscopic surgery in pain relief?.
      • Keckstein J
      • Wiesinger H.
      Deep endometriosis, including intestinal involvement–the interdisciplinary approach.
      • Nardo LG
      • Moustafa M
      • Gareth Beynon DW
      Laparoscopic treatment of pelvic pain associated with minimal and mild endometriosis with use of the Helica Thermal Coagulator.
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Fedele L
      • Bianchi S
      • Zanconato G
      • et al.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Saleh A
      • Tulandi T.
      Reoperation after laparoscopic treatment of ovarian endometriomas by excision and by fenestration.
      • Chapron C
      • Dubuisson JB
      • Fritel X
      • et al.
      Operative management of deep endometriosis infiltrating the uterosacral ligaments.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      • Nezhat CH
      • Seidman DS
      • Nezhat FR
      • et al.
      Long-term outcome of laparoscopic presacral neurectomy for the treatment of central pelvic pain attributed to endometriosis.
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      • Sutton CJ
      • Ewen SP
      • Jacobs SA
      • et al.
      Laser laparoscopic surgery in the treatment of ovarian endometriomas.
      • Donnez J
      • Nisolle M
      • Gillerot S
      • et al.
      Rectovaginal septum adenomyotic nodules: a series of 500 cases.
      • Catalano GF
      • Marana R
      • Caruana P
      • et al.
      Laparoscopy versus microsurgery by laparotomy for excision of ovarian cysts in patients with moderate or severe endometriosis.
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Redwine DB.
      Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      • Lukic A
      • Di Properzio M
      • De Carlo S
      • et al.
      Quality of sex life in endometriosis patients with deep dyspareunia before and after laparoscopic treatment.
      • Fritzer N
      • Tammaa A
      • Haas D
      • et al.
      When sex is not on fire: a prospective multicentre study evaluating the short-term effects of radical resection of endometriosis on quality of sex life and dyspareunia.
      • Gallicchio L
      • Helzlsouer KJ
      • Audlin KM
      • et al.
      Change in pain and quality of life among women enrolled in a trial examining the use of narrow band imaging during laparoscopic surgery for suspected endometriosis.
      • Mettler L
      • Ruprai R
      • Alkatout I
      Impact of medical and surgical treatment of endometriosis on the cure of endometriosis and pain.
      • Afors K
      • Centini G
      • Fernandes R
      • et al.
      Segmental and discoid resection are preferential to bowel shaving for medium-term symptomatic relief in patients with bowel endometriosis.
      (Figure). The main reasons for exclusion were use of medical therapy (n = 353), insufficient cohort size (n = 253), gynaecological cancer studies (n = 252), and “other” (n = 691).

       Characteristics of Studies

      Of the 38 studies, 65.8% were prospective, including 11 randomized controlled trials (RCTs) and one extension of an RCT, whereas 11 (28.9%) were retrospective cohort analyses, and one (2.6%) was a longitudinal study (Table 1). When categorized by intervention type, the two groups with the greatest number of surgical techniques were the lesion excision (14 techniques) and deep endometriosis (11 techniques) groups (online Table 2). Median duration of follow-up varied widely across the seven groups, ranging from 9 months for lesion ablation to 92 months for hysterectomy (Table 1).
      Table 1Characteristics of studies included in the review
      Treatment typeNumber of studies (number of treatment arms)Study typeMedian number of patients
      The number of patients who completed the study.
      Total number of patientsMedian follow-up, monthsPublication year
      Diagnostic surgery2 (1)RCT (n = 1)
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      ; extension of RCT (n = 1)
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      31181994-1997
      Directed lesion excision25 (31)RCT (n = 9)
      • Mossa B
      • Ebano V
      • Tucci S
      • et al.
      Laparoscopic surgery for the management of ovarian endometriomas.
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      • Gallicchio L
      • Helzlsouer KJ
      • Audlin KM
      • et al.
      Change in pain and quality of life among women enrolled in a trial examining the use of narrow band imaging during laparoscopic surgery for suspected endometriosis.
      • Mettler L
      • Ruprai R
      • Alkatout I
      Impact of medical and surgical treatment of endometriosis on the cure of endometriosis and pain.
      ; prospective cohort study (n = 8)
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Milingos S
      • Protopapas A
      • Kallipolitis G
      • et al.
      Endometriosis in patients with chronic pelvic pain: is staging predictive of the efficacy of laparoscopic surgery in pain relief?.
      • Donnez J
      • Nisolle M
      • Gillerot S
      • et al.
      Rectovaginal septum adenomyotic nodules: a series of 500 cases.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      • Lukic A
      • Di Properzio M
      • De Carlo S
      • et al.
      Quality of sex life in endometriosis patients with deep dyspareunia before and after laparoscopic treatment.
      • Fritzer N
      • Tammaa A
      • Haas D
      • et al.
      When sex is not on fire: a prospective multicentre study evaluating the short-term effects of radical resection of endometriosis on quality of sex life and dyspareunia.
      ; retrospective cohort study (n = 7)
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      • Brouwer R
      • Woods RJ
      Rectal endometriosis: results of radical excision and review of published work.
      • Fedele L
      • Bianchi S
      • Zanconato G
      • et al.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      • Saleh A
      • Tulandi T.
      Reoperation after laparoscopic treatment of ovarian endometriomas by excision and by fenestration.
      • Chapron C
      • Dubuisson JB
      • Fritel X
      • et al.
      Operative management of deep endometriosis infiltrating the uterosacral ligaments.
      • Sutton CJ
      • Ewen SP
      • Jacobs SA
      • et al.
      Laser laparoscopic surgery in the treatment of ovarian endometriomas.
      • Catalano GF
      • Marana R
      • Caruana P
      • et al.
      Laparoscopy versus microsurgery by laparotomy for excision of ovarian cysts in patients with moderate or severe endometriosis.
      ; longitudinal unmatched study (n = 1)
      • Redwine DB.
      Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease.
      662652241988-2016
      Directed lesion ablation2 (2)Prospective cohort study (n = 1)
      • Nardo LG
      • Moustafa M
      • Gareth Beynon DW
      Laparoscopic treatment of pelvic pain associated with minimal and mild endometriosis with use of the Helica Thermal Coagulator.
      ; RCT (n = 1)
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      6412892005-2010
      Endometrioma drainage without cyst excision3 (3)RCT (n = 2)
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      ; retrospective cohort study (n = 1)
      • Saleh A
      • Tulandi T.
      Reoperation after laparoscopic treatment of ovarian endometriomas by excision and by fenestration.
      48150241998-2004
      Pelvic denervation7 (6)RCT (n = 4)
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      ; extension of RCT (n = 1)
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      ; prospective cohort study (n = 2)
      • Nezhat CH
      • Seidman DS
      • Nezhat FR
      • et al.
      Long-term outcome of laparoscopic presacral neurectomy for the treatment of central pelvic pain attributed to endometriosis.
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      57.5369241992-2003
      Hysterectomy1 (2)Retrospective cohort study (n = 1)
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      48.597922008
      Deep endometriosis affecting the bowel and/or bladder8 (11)Retrospective cohort study (n = 4)
      • Ruffo G
      • Scopelliti F
      • Manzoni A
      • et al.
      Long-term outcome after laparoscopic bowel resections for deep infiltrating endometriosis: a single-center experience after 900 cases.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      • Afors K
      • Centini G
      • Fernandes R
      • et al.
      Segmental and discoid resection are preferential to bowel shaving for medium-term symptomatic relief in patients with bowel endometriosis.
      ; prospective cohort study (n = 3)
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      • Keckstein J
      • Wiesinger H.
      Deep endometriosis, including intestinal involvement–the interdisciplinary approach.
      ; RCT (n = 1)
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      631553302005-2016
      RCT: randomized clinical trial.
      a The number of patients who completed the study.
      The pelvic denervation group included seven studies; uterine nerve ablation in an RCT (data were pooled with the extension study),
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      uterosacral ligament resection in another RCT,
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      and pre-sacral neurectomy in four studies
      • Nezhat CH
      • Seidman DS
      • Nezhat FR
      • et al.
      Long-term outcome of laparoscopic presacral neurectomy for the treatment of central pelvic pain attributed to endometriosis.
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      (online Table 2). Pelvic denervation was performed in combination with lesion excision or ablation in four studies. Directed lesion excision was the most common treatment class, reported in 25 studies and across 31 treatment arms. The effectiveness of hysterectomy was investigated in only one study.
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      Eight studies exclusively included women with deep endometriosis; all studies in this group assessed the efficacy of lesion excision.
      The effect of surgical treatment on endometriosis-associated pain was investigated in 23 studies,
      • Ruffo G
      • Scopelliti F
      • Manzoni A
      • et al.
      Long-term outcome after laparoscopic bowel resections for deep infiltrating endometriosis: a single-center experience after 900 cases.
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      • Keckstein J
      • Wiesinger H.
      Deep endometriosis, including intestinal involvement–the interdisciplinary approach.
      • Nardo LG
      • Moustafa M
      • Gareth Beynon DW
      Laparoscopic treatment of pelvic pain associated with minimal and mild endometriosis with use of the Helica Thermal Coagulator.
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Chapron C
      • Dubuisson JB
      • Fritel X
      • et al.
      Operative management of deep endometriosis infiltrating the uterosacral ligaments.
      • Sutton CJ
      • Ewen SP
      • Jacobs SA
      • et al.
      Laser laparoscopic surgery in the treatment of ovarian endometriomas.
      • Redwine DB.
      Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      • Lukic A
      • Di Properzio M
      • De Carlo S
      • et al.
      Quality of sex life in endometriosis patients with deep dyspareunia before and after laparoscopic treatment.
      • Fritzer N
      • Tammaa A
      • Haas D
      • et al.
      When sex is not on fire: a prospective multicentre study evaluating the short-term effects of radical resection of endometriosis on quality of sex life and dyspareunia.
      • Gallicchio L
      • Helzlsouer KJ
      • Audlin KM
      • et al.
      Change in pain and quality of life among women enrolled in a trial examining the use of narrow band imaging during laparoscopic surgery for suspected endometriosis.
      whereas the remaining 15 studies investigated AEs and/or other symptom recurrence.
      • Mossa B
      • Ebano V
      • Tucci S
      • et al.
      Laparoscopic surgery for the management of ovarian endometriomas.
      • Brouwer R
      • Woods RJ
      Rectal endometriosis: results of radical excision and review of published work.
      • Milingos S
      • Protopapas A
      • Kallipolitis G
      • et al.
      Endometriosis in patients with chronic pelvic pain: is staging predictive of the efficacy of laparoscopic surgery in pain relief?.
      • Fedele L
      • Bianchi S
      • Zanconato G
      • et al.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      • Saleh A
      • Tulandi T.
      Reoperation after laparoscopic treatment of ovarian endometriomas by excision and by fenestration.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      • Nezhat CH
      • Seidman DS
      • Nezhat FR
      • et al.
      Long-term outcome of laparoscopic presacral neurectomy for the treatment of central pelvic pain attributed to endometriosis.
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      • Donnez J
      • Nisolle M
      • Gillerot S
      • et al.
      Rectovaginal septum adenomyotic nodules: a series of 500 cases.
      • Catalano GF
      • Marana R
      • Caruana P
      • et al.
      Laparoscopy versus microsurgery by laparotomy for excision of ovarian cysts in patients with moderate or severe endometriosis.
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      • Mettler L
      • Ruprai R
      • Alkatout I
      Impact of medical and surgical treatment of endometriosis on the cure of endometriosis and pain.
      • Afors K
      • Centini G
      • Fernandes R
      • et al.
      Segmental and discoid resection are preferential to bowel shaving for medium-term symptomatic relief in patients with bowel endometriosis.
      Quantitative assessments of endometriosis-associated pain before and/or after treatment were performed in 20 of the 23 studies that investigated this outcome: 18 (90.0%) used a 10-cm visual analogue scale (VAS),
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Ruffo G
      • Scopelliti F
      • Manzoni A
      • et al.
      Long-term outcome after laparoscopic bowel resections for deep infiltrating endometriosis: a single-center experience after 900 cases.
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Brouwer R
      • Woods RJ
      Rectal endometriosis: results of radical excision and review of published work.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      • Milingos S
      • Protopapas A
      • Kallipolitis G
      • et al.
      Endometriosis in patients with chronic pelvic pain: is staging predictive of the efficacy of laparoscopic surgery in pain relief?.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Redwine DB.
      Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      • Lukic A
      • Di Properzio M
      • De Carlo S
      • et al.
      Quality of sex life in endometriosis patients with deep dyspareunia before and after laparoscopic treatment.
      • Fritzer N
      • Tammaa A
      • Haas D
      • et al.
      When sex is not on fire: a prospective multicentre study evaluating the short-term effects of radical resection of endometriosis on quality of sex life and dyspareunia.
      • Gallicchio L
      • Helzlsouer KJ
      • Audlin KM
      • et al.
      Change in pain and quality of life among women enrolled in a trial examining the use of narrow band imaging during laparoscopic surgery for suspected endometriosis.
      and two (10.0%) used the Visick score or a 10-point subjective scale.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Sutton CJ
      • Ewen SP
      • Jacobs SA
      • et al.
      Laser laparoscopic surgery in the treatment of ovarian endometriomas.
      Only 14 studies reported both baseline and postoperative VAS scores for endometriosis-associated pain.

       Proportion of Patients With No Reduction in Endometriosis-Associated Pain

      Only 11 studies (28.9%) reported the number of women with no reduction in endometriosis-associated pain immediately after surgery. Most women (77.4%) who underwent diagnostic surgery (one treatment arm; n = 31) reported no reduction in pain (Table 2, online Table 3, online Figure 1A).
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      Few women experienced no reduction in pain immediately following lesion excision (median 11.8%; five treatment arms; n = 371),
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Chapron C
      • Dubuisson JB
      • Fritel X
      • et al.
      Operative management of deep endometriosis infiltrating the uterosacral ligaments.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      lesion ablation (11.4%; one treatment arm; n = 79),
      • Nardo LG
      • Moustafa M
      • Gareth Beynon DW
      Laparoscopic treatment of pelvic pain associated with minimal and mild endometriosis with use of the Helica Thermal Coagulator.
      pelvic denervation (median 6.7%; three treatment arms; n = 184),
      • Nezhat CH
      • Seidman DS
      • Nezhat FR
      • et al.
      Long-term outcome of laparoscopic presacral neurectomy for the treatment of central pelvic pain attributed to endometriosis.
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      or surgery for deep endometriosis (median 0%; three treatment arms; n = 276).
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      Table 2Main outcome measures by surgery type
      Surgery typeNo reduction in pain, %Persistence of pain after surgery, %Recurrent pain, %Recurrent surgery, %Change in VAS score from baseline, cmAEs/women, n/N
      Diagnostic surgery77.4NDND77.4+0.30/31
      Lesion excision11.8 (3.6–22.2)25.0 (4.4–41.7)15.8 (0.0–42.0)22.6 (5.8–56.9)−3.6124/1527
      Lesion ablation11.4NDNDND−2.40/79
      Endometrioma drainage onlyNDND54.8 (52.9–75.0)51.5 (22.9–80.0)ND0/32
      Pelvic denervation6.7 (5.8–15.0)34.3 (8.6–48.1)28.7 (10.0–36.0)12.5−2.227/182
      Hysterectomy with ovarian preservationNDNDND19.1NDND
      Hysterectomy without ovarian preservationNDNDND8.0NDND
      Deep endometriosis affecting the bowel and/or bladder0.0 (0.0–4.4)2.3 (2.2–4.4)7.04.1 (1.3–27.6)−6.263/779
      AE: adverse event; ND: no data; VAS: visual analogue scale.
      Values are median proportion of women (range) except for change in pain VAS score and AEs.
      Table S1Summary of search of MEDLINE® and Embase®, performed using Ovid® on October 13, 2016
      #Search historyResults
      1[Terms for endometriosis]0
      2ENDOMETRIOSIS/49 624
      3(adenomyo$ or endometrio$).tw.64 559
      4chocolate cyst$.tw.328
      5or/2-473 165
      6[Terms for surgery]0
      7SURGERY/766 685
      8surgery.tw.2 135 307
      9surgical.tw.1 791 424
      10EXCISION/55 727
      11excis$.tw.335 491
      12ablation.tw.171 603
      13adhesioly$.tw.3384
      14cystectomy.tw.28 893
      15CYSTECTOMY/28 604
      16nodulectomy.tw.182
      17NODULECTOMY/10
      18resect$.tw.674 757
      19presacral neurectomy.tw.210
      20(uterosacral nerve ablation or LUNA).tw.1955
      21(plasmajet or plasma jet).tw.502
      22HYSTERECTOMY/70 401
      23hysterectomy.tw.71 471
      24LAPAROSCOPY/142 496
      25laparoscop$.tw.253 729
      26or/7-254 174 725
      27[Terms for symptoms]0
      28PAIN/491 678
      29pain$.tw.1 316 769
      30PELVIC PAIN/7959
      31pelvic pain.tw.18 272
      32CHRONIC PELVIC PAIN/11 741
      33chronic pelvic pain.tw.7661
      34((adenomyo$ or endometriosis$) adj2 pain$).tw.1255
      35dyspareunia.tw.8503
      36dysmenorrh?ea.tw.10 755
      37dyschezia.tw.636
      38dysuria.tw.8989
      39LESION/265
      40lesion$.tw.1 667 361
      41cyst?.tw.225 529
      42nodule?.tw.160 173
      43recurr#n$.tw.1 075 904
      44or/28-434 119 259
      45[Terms for outcomes]0
      46(re-operation or reoperation).tw.59 154
      47improv$.tw.4 269 583
      48reduc$.tw.6 002 399
      49effect$.tw.12 372 399
      50(relief or reliev$).tw.277 973
      51outcome.tw.1 810 512
      52complication$.tw.1 723 876
      53rate?.tw.5 192 973
      54or/46-5321 395 247
      555 and 26 and 44 and 549610
      56[Filters]0
      5755 and (wom#n or patient?).tw.8787
      5857 and (randomi$ or clinic$ or trial$ or observation$ or database or prospective or retrospective or cohort or study or series).tw.6685
      5958 not (mice or murine or mouse or baboon$ or monkey$ or animal$ or rabbit$ or polymorphi$ or apopto$).tw.6483
      60conference abstract.af.2 355 040
      6159 not 604925
      62limit 61 to abstracts4912
      63limit 62 to English language4319
      64limit 63 to "review"549
      6563 not 643770
      66remove duplicates from 652185
      Table S2Surgical techniques used in each treatment group
      Treatment groupSurgical techniques
      The inclusion of surgical techniques was based on the treatment arms in the studies. Not all of the studies differentiated between laparoscopy and laparotomy.
      (number of studies)
      Diagnostic surgeryDiagnostic laparoscopy (n = 1)
      Lesion excisionLaparoscopic lesion excision (n = 15); laser laparoscopy (n = 4); conservative surgery (n = 3); segmental colorectal resection (n = 3); laparoscopic partial cystectomy (n = 2); laparotomy (n = 2); cystectomy (n = 1); dissection of endometriosis from rectal wall (n = 1); full-thickness excision of anterior rectal wall (n = 1); laparoscopic stripping technique (n = 1); laparoscopic ureterolysis (n = 1); partial bladder resection (n = 1); segmental ureteral resection and ureteroureterostomy (n = 1); ureterectomy and ureterocystoneostomy (n = 1)
      Lesion ablationLaparoscopic ablation (n = 1); cauterization/ablation with Helica thermal coagulator (n = 1)
      Endometrioma drainage onlyFenestration and coagulation (n = 3)
      Pelvic denervationPresacral neurectomy (n = 4); uterine nerve ablation (n = 2); uterosacral ligament resection (n = 1)
      HysterectomyHysterectomy with ovarian preservation (n = 1); hysterectomy without ovarian preservation (n = 1)
      Deep endometriosisBowel resection (n = 6); ureterolysis (n = 3); full/partial cystectomy (n = 3); lesion excision (n = 3); salpingo-oophorectomy (n = 2); hysterectomy (n = 2); ureteroneocystostomy (n = 1); unilateral salpingectomy (n = 1); uterine nerve ablation (n = 1); ureteral reimplantation (n = 1); rectal shaving (n = 1)
      a The inclusion of surgical techniques was based on the treatment arms in the studies. Not all of the studies differentiated between laparoscopy and laparotomy.
      Table S3Proportion of patients with no reduction in pain following surgical treatment of endometriosis
      Treatment classStudyTotal symptoms, %Dysmenorrhoea, %Pelvic pain, %Dyspareunia, %Dyschezia, %Other, %Median non-response rate (range), %Number of patients
      The number of patients who completed the study. There were no data for patients who underwent endometrioma drainage only or hysterectomy with/without ovarian preservation.
      Total number of patients
      Diagnostic surgerySutton et al., 1997a77.4NDNDNDNDND77.43131
      Lesion excisionSeracchioli et al., 20103.6NDNDNDNDND11.8 (3.6–22.2)56371
      Darai et al., 2007ND8.2ND12.319.422.271
      Ferrero et al., 2007NDNDND4.4NDND68
      Chapron et al., 1999ND17.6ND11.8NDND110
      Davis & Brooks, 19886.1NDNDNDNDND66
      Lesion ablationNardo et al., 200511.4NDNDNDNDND11.47979
      Pelvic denervationSutton et al., 1997a6.3NDNDNDNDND6.7 (5.8–15.0)32184
      Nezhat et al., 1998ND15.06.7NDNDND100
      Nezhat & Nezhat, 1992ND7.75.8NDNDND52
      Deep endometriosisChe et al., 20140.0NDNDNDNDND0.0 (0.0–4.4)63276
      Che et al., 20144.4NDNDNDNDND45
      Pereira et al., 20090.00.00.00.00.00.0168
      ND: no data.
      a The number of patients who completed the study.There were no data for patients who underwent endometrioma drainage only or hysterectomy with/without ovarian preservation.

       Proportion of Patients With Persistent Endometriosis-Associated Pain After Surgery

      Nine studies (23.7%) reported the number of women who experienced some, but not complete, pain relief following surgery. The proportions of women who experienced incomplete relief of pain were as follows: 34.3% in the pelvic denervation group (two treatment arms; n = 87),
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      25.0% in the lesion excision group (six treatment arms; n = 407),
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Chapron C
      • Dubuisson JB
      • Fritel X
      • et al.
      Operative management of deep endometriosis infiltrating the uterosacral ligaments.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      and 2.3% in the deep endometriosis group (two treatment arms; n = 213)
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      (Table 2, online Table 4, online Figure 1B).
      Table S4Proportion of patients with persistence of pain following surgical treatment of endometriosis
      Treatment classStudyTotal symptoms, %Dysmenorrhoea, %Pelvic pain, %Dyspareunia, %Dyschezia, %Other, %Median (range), %Number of patients
      The number of patients who completed the study. There were no data for patients who underwent diagnostic surgery, lesion ablation surgery, endometrioma drainage only or hysterectomy with/without ovarian preservation.
      Total number of patients
      Lesion excisionSeracchioli et al., 2010NDNDNDNDND32.125.0 (4.4–41.7)56407
      Darai et al., 2007ND36.6ND29.623.935.271
      Ferrero et al., 2007NDNDND4.4NDND68
      Chapron et al., 1999ND31.8ND22.4NDND110
      Candiani et al., 1992ND41.713.919.4NDND36
      Davis & Brooks, 1988NDND25.05.6NDND66
      Pelvic denervationNezhat & Nezhat, 1992ND48.148.1NDNDND34.3 (8.6–48.1)5287
      Candiani et al., 1992ND34.38.611.4NDND35
      Deep endometriosisChe et al., 2014ND4.42.22.2NDND2.3 (2.2–4.4)45213
      Pereira et al., 20092.4NDNDNDNDND168
      ND: no data.
      a The number of patients who completed the study.There were no data for patients who underwent diagnostic surgery, lesion ablation surgery, endometrioma drainage only or hysterectomy with/without ovarian preservation.
      Figure S1
      Figure S1Response to therapy and symptom recurrence after surgical treatment for endometriosis.
      Data are presented as median (range) or single values; median follow-up time (Figure S1C only); total numbers of women who completed the study. DE: deep endometriosis; ND: no data.

       Proportion of Patients With Recurrent Endometriosis-Associated Pain

      Twelve studies (31.6%) reported data on recurrence of endometriosis-associated pain following surgery. More than one half (54.8%) of the women who underwent endometrioma drainage (two treatment arms; n = 80)
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      experienced recurrence of pain (Table 2, online Table 5, online Figure 1C). In other treatment groups, the proportions of women who experienced pain recurrence were as follows: 28.7% in the pelvic denervation group (three treatment arms; n = 157),
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      15.8% in the lesion excision group (12 treatment arms; n = 921),
      • Mossa B
      • Ebano V
      • Tucci S
      • et al.
      Laparoscopic surgery for the management of ovarian endometriomas.
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Fedele L
      • Bianchi S
      • Zanconato G
      • et al.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      • Sutton CJ
      • Ewen SP
      • Jacobs SA
      • et al.
      Laser laparoscopic surgery in the treatment of ovarian endometriomas.
      • Donnez J
      • Nisolle M
      • Gillerot S
      • et al.
      Rectovaginal septum adenomyotic nodules: a series of 500 cases.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      • Mettler L
      • Ruprai R
      • Alkatout I
      Impact of medical and surgical treatment of endometriosis on the cure of endometriosis and pain.
      and 7.0% in the deep endometriosis group (one treatment arm; n = 54).
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      Table S5Proportion of patients with recurrence of pain following surgical treatment of endometriosis
      Treatment classStudy
      Different treatment arms within the same study are listed individually.
      Total symptoms,Dysmenorrhoea, %Pelvic pain, %Dyspareunia, %Median (range), %Number of patients
      The number of patients who completed the study. There were no data for patients who underwent diagnostic surgery, lesion ablation surgery or hysterectomy with/without ovarian preservation.
      Total number of patientsFollow-up, monthsMedian follow-up (range), months
      Lesion excisionMossa et al., 2010ND6.42.12.115.8 (0.0–42.0)479211222 (6.0–37.5)
      Mossa et al., 2010ND4.70.02.34312
      Alborzi et al., 200415.8NDNDND5224
      Fedele et al., 200428.025.319.325.38337.5
      Vercellini et al., 2003ND32.0NDND9036
      Beretta et al., 1998ND15.810.0203219.5
      Donnez et al., 1997NDND3.71.224224
      Sutton et al., 1997b30.0NDNDND6424
      Sutton et al., 1997b12.5NDNDND2936
      Candiani et al., 1992ND42.042.0ND3612
      Davis & Brooks, 19887.6NDNDND6612
      Mettler et al., 2014ND20.024.015.01376
      Endometrioma drainageAlborzi et al., 200456.7NDNDND54.8 (52.9–75.0)48802422 (20–24)
      Beretta et al., 1998ND52.952.975.03220
      Pelvic denervationVercellini et al., 2003ND36.0NDND28.7 (10.0–36.0)901573618 (12–36)
      Candiani et al., 1992ND34.323.0ND3512
      Sutton et al., 1997a10.0NDNDND3218
      Deep endometriosisFrenna et al., 20077.0NDNDND7.0545499
      ND: no data.
      a Different treatment arms within the same study are listed individually.
      b The number of patients who completed the study.There were no data for patients who underwent diagnostic surgery, lesion ablation surgery or hysterectomy with/without ovarian preservation.

       Proportion of Patients Requiring Further Surgery

      Twelve studies (31.6%) reported the proportion of women who required further surgery. Most women who underwent diagnostic surgery (77.4%; one treatment arm; n = 31)
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      or endometrioma drainage (51.5%; two treatment arms; n = 118)
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Saleh A
      • Tulandi T.
      Reoperation after laparoscopic treatment of ovarian endometriomas by excision and by fenestration.
      required further surgery (Table 2, online Table 6, online Figure 2). Further surgical procedures were required by 22.6% of women after lesion excision (five treatment arms; n = 747),
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      • Alborzi S
      • Momtahan M
      • Parsanezhad ME
      • et al.
      A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas.
      • Saleh A
      • Tulandi T.
      Reoperation after laparoscopic treatment of ovarian endometriomas by excision and by fenestration.
      • Redwine DB.
      Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      12.5% after pelvic denervation to reduce endometriosis-associated pain (one treatment arm; n = 32),
      • Sutton CJ
      • Pooley AS
      • Ewen SP
      • et al.
      Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis.
      19.1% after hysterectomy with ovarian preservation (one treatment arm; n = 47) and 8.0% without ovarian preservation (one treatment arm; n = 50),
      • Shakiba K
      • Bena JF
      • McGill KM
      • et al.
      Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery.
      and 4.1% in the deep endometriosis group (eight treatment arms; n = 514).
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      • Afors K
      • Centini G
      • Fernandes R
      • et al.
      Segmental and discoid resection are preferential to bowel shaving for medium-term symptomatic relief in patients with bowel endometriosis.
      Table S6Proportion of patients requiring further surgical treatment for endometriosis
      Treatment classStudyProportion, %Median (range), %Number of patients
      The number of patients who completed the study. There were no data for patients who underwent lesion ablation surgery.
      Total number of patientsFollow-up, monthsMedian follow-up (range), months
      Diagnostic surgerySutton et al., 1997a77.477.431311818
      Lesion excisionShakiba et al., 200856.922.6 (5.8–56.9)1097479224 (12–92)
      Alborzi et al., 20045.85224
      Saleh & Tulandi, 199923.016136
      Redwine, 199122.635924
      Davis & Brooks, 198821.26612
      Endometrioma drainageAlborzi et al., 200422.951.5 (22.9–80.0)481182430 (24–36)
      Saleh & Tulandi, 199980.07036
      Pelvic denervationSutton et al., 1997a12.512.532321818
      Hysterectomy (with ovarian preservation)Shakiba et al., 200819.119.147479292
      Hysterectomy (without ovarian preservation)Shakiba et al., 20088.08.050509292
      Deep endometriosisChe et al., 20144.44.1 (1.3–27.6)455142130 (9–60)
      Chapron et al., 20101.37560
      Camanni et al., 20092.58022
      Pereira et al., 20093.616837
      Frenna et al., 20073.7549
      Afors et al., 201627.64730
      Afors et al., 201613.31530
      Afors et al., 20166.63030
      ND: no data.
      a The number of patients who completed the study.There were no data for patients who underwent lesion ablation surgery.
      Figure S2
      Figure S2Proportion of patients requiring further surgical treatment for endometriosis.
      Data are presented as median (range) or single values; median follow-up time; total numbers of women who completed the study. DE: deep endometriosis; ND: no data.
      Only one study reported outcomes following reoperation: complete resolution of disease was achieved in two patients with ureteral endometriosis in the deep endometriosis group.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.

       Reduction in Visual Analogue Scale Score From Baseline

      More than one third of studies (36.8%) reported both baseline and postoperative VAS scores for endometriosis-associated pain. The median reduction in VAS 10-cm scores from baseline to the end of follow-up (median 12 months, unless specified otherwise) was as follows: −6.2 cm in the deep endometriosis group (22 months follow-up; 11 treatment arms; n = 263),
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      −3.6 cm in the lesion excision group (25 treatment arms; n = 713),
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Ferrero S
      • Abbamonte LH
      • Giordano M
      • et al.
      Deep dyspareunia and sex life after laparoscopic excision of endometriosis.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      • Lukic A
      • Di Properzio M
      • De Carlo S
      • et al.
      Quality of sex life in endometriosis patients with deep dyspareunia before and after laparoscopic treatment.
      • Fritzer N
      • Tammaa A
      • Haas D
      • et al.
      When sex is not on fire: a prospective multicentre study evaluating the short-term effects of radical resection of endometriosis on quality of sex life and dyspareunia.
      • Gallicchio L
      • Helzlsouer KJ
      • Audlin KM
      • et al.
      Change in pain and quality of life among women enrolled in a trial examining the use of narrow band imaging during laparoscopic surgery for suspected endometriosis.
      −2.4 cm in the lesion ablation group (six treatment arms; n = 49),
      • Healey M
      • Ang WC
      • Cheng C
      Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.
      and −2.2 cm in the pelvic denervation group (seven treatment arms; n = 185)
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Vercellini P
      • Aimi G
      • Busacca M
      • et al.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      (Table 2, online Table 7, online Figure 3). Women who underwent diagnostic surgery experienced a 0.3-cm increase in VAS score from 7.5 cm (6 months follow-up; one treatment arm; n = 31).
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      Table S7VAS score (cm) for pain symptoms at baseline and after follow-up
      Treatment classStudy
      Different treatment arms within the same study are listed individually.
      Number of patients
      The number of patients who completed the study.
      Follow-up, monthsPain symptomBaseline VAS, cmFollow-up VAS, cmMedian baseline VAS, cmMedian follow-up VAS, cmChange in median VAS from baseline to follow-up, cmTotal number of patientsMedian follow-up (range), months
      Diagnostic surgerySutton et al., 1994316Total symptoms7.57.87.57.8+0.3316
      Lesion excisionHealey et al., 20105412Dysmenorrhoea6.43.85.5 (1.2–8.1)1.9 (0.1–5.4)–3.671312 (6–55)
      Healey et al., 2010Dyspareunia5.61.9
      Healey et al., 2010Dysuria1.20.6
      Healey et al., 2010Dyschezia3.61.8
      Healey et al., 2010Total symptoms5.52.4
      Healey et al., 2010Pelvic pain6.03.2
      Seracchioli et al., 20105655Dysuria4.00.1
      Seracchioli et al., 2010Other3.10.6
      Darai et al., 20077124Dysmenorrhoea7.51.8
      Darai et al., 2007Dyspareunia5.61.8
      Darai et al., 2007Dyschezia3.41.7
      Darai et al., 2007Other4.82.2
      Darai et al., 2007Other4.51.9
      Darai et al., 2007Other4.51.4
      Ferrero et al., 20076812Dyspareunia7.62.6
      Vercellini et al., 20039036Dysmenorrhoea7.64.0
      Vercellini et al., 2003Dyspareunia5.41.8
      Vercellini et al., 2003Pelvic pain3.52.0
      Zullo et al., 20036312Dysmenorrhoea8.15.4
      Zullo et al., 2003Dyspareunia6.34.9
      Zullo et al., 2003Pelvic pain6.25.0
      Lukic et al., 2016676Dyspareunia7.83.5
      Gallichio et al., 20151006Pelvic pain5.01.1
      Gallichio et al., 2015386Pelvic pain4.01.0
      Fritzer et al., 2016968Dyspareunia6.22.5
      Lesion ablationHealey et al., 20104912Total symptoms6.23.25.7 (1.7–7.1)3.3 (0.9–4.8)–2.44912
      Healey et al., 2010Pelvic pain6.84.0
      Healey et al., 2010Dysmenorrhoea7.14.8
      Healey et al., 2010Dyspareunia5.23.3
      Healey et al., 2010Dysuria1.70.9
      Healey et al., 2010Dyschezia2.92.3
      Pelvic denervationSutton et al., 1994326Total symptoms8.54.86.5 (5.5–8.5)4.3 (2.2–4.8)–2.218512 (6–36)
      Vercellini et al., 20039036Pelvic pain5.52.5
      Vercellini et al., 2003Dysmenorrhoea7.83.8
      Vercellini et al., 2003Dyspareunia6.02.2
      Zullo et al., 20036312Pelvic pain6.34.3
      Zullo et al., 2003Dysmenorrhoea8.34.6
      Zullo et al., 2003Dyspareunia6.54.4
      Deep endometriosisChe et al., 20146322Total symptoms7.11.86.8 (2.8–8.0)0.6 (0.0–2.2)–6.226322 (21–60)
      Che et al., 20144521Total symptoms6.82.1
      Chapron et al., 20107560Pelvic pain2.80.8
      Chapron et al., 2010Dysmenorrhoea7.82.2
      Chapron et al., 2010Dyspareunia6.00.9
      Chapron et al., 2010Other3.10.6
      Chapron et al., 2010Other5.90.4
      Camanni et al., 20098022Dysmenorrhoea8.00.0
      Camanni et al., 2009Dyspareunia6.00.0
      Camanni et al., 2009Dysuria7.00.0
      Camanni et al., 2009Dyschezia7.00.0
      VAS: visual analogue scale.
      a Different treatment arms within the same study are listed individually.
      b The number of patients who completed the study.
      Figure S3
      Figure S3VAS score (cm) for total pain symptoms at baseline and after follow-up.
      VAS scores shown as median (range). Follow-up data shown as median follow-up time (range); total numbers of women who completed the study; number of treatment arm(s). DE: deep endometriosis; VAS: visual analogue scale.

       Adverse Events Following Surgery for Endometriosis

      Twenty-three studies (60.5%) reported on AEs following surgery. In the pelvic denervation group (four treatment arms), 27 AEs were reported in 182 patients (AE rate, 14.8%) (Table 2, online Table 8).
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Nezhat C
      • Nezhat F.
      A simplified method of laparoscopic presacral neurectomy for the treatment of central pelvic pain due to endometriosis.
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      The most common AEs in this group were severe constipation (n = 16) and urinary retention (n = 4). Rare AEs included retroperitoneal pre-sacral hematoma (n = 1), hemorrhage from the middle sacral vein (n = 1), and painless labour (n = 1). In the lesion excision group (17 treatment arms), 124 AEs were reported in 1527 patients (8.1%).
      • Mossa B
      • Ebano V
      • Tucci S
      • et al.
      Laparoscopic surgery for the management of ovarian endometriomas.
      • Seracchioli R
      • Mabrouk M
      • Montanari G
      • et al.
      Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up.
      • Darai E
      • Ackerman G
      • Bazot M
      • et al.
      Laparoscopic segmental colorectal resection for endometriosis: limits and complications.
      • Brouwer R
      • Woods RJ
      Rectal endometriosis: results of radical excision and review of published work.
      • Chapron C
      • Dubuisson JB
      • Fritel X
      • et al.
      Operative management of deep endometriosis infiltrating the uterosacral ligaments.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      • Sutton CJ
      • Ewen SP
      • Jacobs SA
      • et al.
      Laser laparoscopic surgery in the treatment of ovarian endometriomas.
      • Donnez J
      • Nisolle M
      • Gillerot S
      • et al.
      Rectovaginal septum adenomyotic nodules: a series of 500 cases.
      • Catalano GF
      • Marana R
      • Caruana P
      • et al.
      Laparoscopy versus microsurgery by laparotomy for excision of ovarian cysts in patients with moderate or severe endometriosis.
      • Redwine DB.
      Conservative laparoscopic excision of endometriosis by sharp dissection: life table analysis of reoperation and persistent or recurrent disease.
      • Davis GD
      • Brooks RA.
      Excision of pelvic endometriosis with the carbon dioxide laser laparoscope.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      The most common AEs were blood loss (n = 43), postoperative fever (n = 9), and urinary retention (n = 9). Sixty-three AEs in 779 patients (8.1%) were reported in the deep endometriosis group (10 treatment arms). The most common AEs were urinary retention (n = 13), leakage of the bowel anastomosis (n = 7), and severe stenosis of the anastomosis (n = 6).
      • Che X
      • Huang X
      • Zhang J
      • et al.
      Is nerve-sparing surgery suitable for deeply infiltrating endometriosis?.
      • Chapron C
      • Bourret A
      • Chopin N
      • et al.
      Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions.
      • Camanni M
      • Bonino L
      • Delpiano EM
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      • Pereira RM
      • Zanatta A
      • Preti CD
      • et al.
      Should the gynecologist perform laparoscopic bowel resection to treat endometriosis? Results over 7 years in 168 patients.
      • Frenna V
      • Santos L
      • Ohana E
      • et al.
      Laparoscopic management of ureteral endometriosis: our experience.
      • Keckstein J
      • Wiesinger H.
      Deep endometriosis, including intestinal involvement–the interdisciplinary approach.
      • Afors K
      • Centini G
      • Fernandes R
      • et al.
      Segmental and discoid resection are preferential to bowel shaving for medium-term symptomatic relief in patients with bowel endometriosis.
      No complications were reported following laparoscopy for lesion ablation (one treatment arm; n = 79),
      • Nardo LG
      • Moustafa M
      • Gareth Beynon DW
      Laparoscopic treatment of pelvic pain associated with minimal and mild endometriosis with use of the Helica Thermal Coagulator.
      endometrioma drainage (one treatment arm; n = 32),
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      or diagnostic surgery (one treatment arm; n = 31).
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      Table S8Number of adverse events in different treatment groups
      Treatment typeStudy
      Different treatment arms within the same study are listed individually.
      Number of patientsNumber of AEsFollow-up time, monthsTotal number of patients
      The number of patients who completed the study.
      Total number of AEsMedian follow-up time (range), months
      Diagnostic surgerySutton et al., 199431063106
      Lesion excisionMossa et al., 201047312152712424 (12–68)
      Mossa et al., 2010433212
      Seracchioli et al., 2010561255
      Darai et al., 200771924
      Brouwer & Woods, 200718368
      Brouwer & Woods, 200758268
      Brouwer & Woods, 20071371168
      Chapron et al., 1999110921
      Beretta et al., 199832020
      Donnez et al., 19972421024
      Sutton et al., 1997b64036
      Sutton et al., 1997b29036
      Catalano et al., 199683132
      Catalano et al., 199649935
      Redwine, 1991359224
      Davis & Brooks, 1988662112
      Zullo et al., 200363012
      Lesion ablationNardo et al., 200579067906
      Endometrioma drainageBeretta et al., 199832019.532019.5
      Pelvic denervationNezhat & Nezhat, 1992527121822712 (6–12)
      Candiani et al., 1992351712
      Zullo et al., 200363312
      Sutton et al., 19943206
      Deep endometriosis affecting the bowel and/or bladderChe et al., 2014639227796330 (9–60)
      Che et al., 201445021
      Chapron et al., 201075260
      Camanni et al., 200980322
      Pereira et al., 20091681337
      Frenna et al., 20075449
      Keckstein & Wiesinger, 200520215ND
      Afors et al., 2016471030
      Afors et al., 201615330
      Afors et al., 201630430
      AE: adverse event; ND: no data.
      a Different treatment arms within the same study are listed individually.
      b The number of patients who completed the study.

      DISCUSSION

       Main Findings and Interpretation

      Surgery represents one of the pillars of modern management of endometriosis-associated pain.
      • Johnson NP
      • Hummelshoj L
      World Endometriosis Society Montpellier Consortium
      Consensus on current management of endometriosis.
      However, the surgical outcomes were not reported in most of the 38 clinical studies identified as relevant in this systematic review. Less than one third of studies reported the number of women without a reduction in pain, with incomplete pain relief, with recurrence of pain, or with need for further surgery. Approximately 40% of studies did not report AE data. Three studies reported that there were no complications following laparoscopy for lesion ablation, endometrioma drainage, or diagnostic surgery.
      • Sutton CJ
      • Ewen SP
      • Whitelaw N
      • et al.
      Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis.
      • Nardo LG
      • Moustafa M
      • Gareth Beynon DW
      Laparoscopic treatment of pelvic pain associated with minimal and mild endometriosis with use of the Helica Thermal Coagulator.
      • Beretta P
      • Franchi M
      • Ghezzi F
      • et al.
      Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation.
      Although laparoscopy is not without risk, it is considered to be the gold standard surgical treatment because of its lower morbidity and shorter hospital stays than laparotomy.
      • Chapron C
      • Querleu D
      • Bruhat MA
      • et al.
      Surgical complications of diagnostic and operative gynaecological laparoscopy: a series of 29,966 cases.
      The available data suggest that one fourth of women who underwent lesion excision reported having some remaining endometriosis-associated pain following surgery and that, in general, more than 10% reported no improvement in pain. More than 15% of women experienced recurrent endometriosis-associated pain, and one fifth underwent further surgery. Data were insufficient to draw direct comparisons regarding the efficacy of lesion excision and ablation, although one 5-year study showed that patients were less likely to need medical therapy for endometriosis after lesion excision than after lesion ablation.
      • Healey M
      • Cheng C
      • Kaur H
      To excise or ablate endometriosis? A prospective randomized double-blinded trial after 5-year follow-up.
      Moreover, our study does suggest that patients who receive lesion ablation therapy experience fewer AEs than patients whose lesions are excised. Similarly, only 6% of clinicians who responded to a survey thought that lesion excision is safer than lesion ablation.
      • Moses SH
      • Clark TJ.
      Current practice for the laparoscopic diagnosis and treatment of endometriosis: a national questionnaire survey of consultant gynaecologists in UK.
      In two systematic reviews of RCTs, uterine nerve ablation did not provide greater pain relief than excision of endometriotic lesions.
      • Proctor ML
      • Latthe PM
      • Farquhar CM
      • et al.
      Surgical interruption of pelvic nerve pathways for primary and secondary dysmenorrhoea.
      • Latthe PM
      • Proctor ML
      • Farquhar CM
      • et al.
      Surgical interruption of pelvic nerve pathways in dysmenorrhea: a systematic review of effectiveness.
      In contrast, pre-sacral neurectomy with conservative surgery provides superior pain relief to conservative surgery alone at 12 months,
      • Candiani GB
      • Fedele L
      • Vercellini P
      • et al.
      Presacral neurectomy for the treatment of pelvic pain associated with endometriosis: a controlled study.
      • Zullo F
      • Palomba S
      • Zupi E
      • et al.
      Effectiveness of presacral neurectomy in women with severe dysmenorrhea caused by endometriosis who were treated with laparoscopic conservative surgery: a 1-year prospective randomized double-blind controlled trial.
      although the technique should only be performed by highly skilled surgeons owing to the high risk of AEs.
      • Johnson NP
      • Hummelshoj L
      World Endometriosis Society Montpellier Consortium
      Consensus on current management of endometriosis.
      • Dunselman GA
      • Vermeulen N
      • Becker C
      • et al.
      ESHRE guideline: management of women with endometriosis.
      In this study, uterine nerve ablation and pre-sacral neurectomy were combined into a single treatment group because of the limited number of available studies and low patient numbers. Overall, few women (6.7%) who underwent pelvic denervation reported no reduction in endometriosis-associated pain following treatment; however, one third experienced an incomplete response, and one third reported symptom recurrence. Furthermore, AEs were common in this group, with more than one half being severe constipation.
      Previous studies have reported that surgical treatment of bowel deep endometriosis leads to substantial pain relief, with low recurrence rates (3% to 7%).
      • Wolthuis AM
      • Meuleman C
      • Tomassetti C
      • et al.
      Bowel endometriosis: colorectal surgeon's perspective in a multidisciplinary surgical team.
      • De Cicco C
      • Corona R
      • Schonman R
      • et al.
      Bowel resection for deep endometriosis: a systematic review.
      Consistent with this, our study showed that women with deep endometriosis have a good prognosis following surgery. Few women with deep endometriosis experienced incomplete relief or no relief of endometriosis-associated pain, recurrence of pain symptoms, or AEs after surgery. Indeed, surgical treatment of deep endometriosis provided the most benefit with respect to endometriosis-associated pain reduction as measured by VAS. However, the deep endometriosis studies were performed by experts in high-volume centres, meaning that these results may not represent the real-world expertise of gynaecologists globally and that their generalizability is limited.
      In this review, patients who underwent hysterectomy with ovarian preservation were more than twice as likely to require further surgical treatment than patients who underwent hysterectomy without ovarian preservation (18.1% vs. 9.0%). It has been reported previously that, compared with bilateral oophorectomy, ovarian preservation is associated with a six-fold increase in recurrence of endometriosis-associated pain and an eight-fold greater risk of reoperation.
      • Rizk B
      • Fischer AS
      • Lotfy HA
      • et al.
      Recurrence of endometriosis after hysterectomy.
      Given the occurrence of serious AEs,
      • McPherson K
      • Metcalfe MA
      • Herbert A
      • et al.
      Severe complications of hysterectomy: the VALUE study.
      however, hysterectomy with bilateral oophorectomy is often reserved for women whose symptoms did not respond to earlier therapy.
      • Dunselman GA
      • Vermeulen N
      • Becker C
      • et al.
      ESHRE guideline: management of women with endometriosis.
      The findings of this study highlight the need for greater, more detailed, and more consistent reporting of the efficacy of surgical interventions for endometriosis-associated pain. We found limited data for the proportion of patients who experienced incomplete endometriosis-associated pain reduction, pain recurrence, or reoperation in the hysterectomy and lesion ablation groups. Most outcomes were reported in one third of studies or less, and evaluation of the outcomes data was difficult because of the diversity of parameters investigated. This finding is consistent with a previous systematic review in which 29 trials, 32 outcomes, and 24 measures were used to assess endometriosis-associated pain.
      • Hirsch M
      • Duffy JM
      • Kusznir JO
      • et al.
      Variation in outcome reporting in endometriosis trials: a systematic review.
      Such incomplete and inconsistent reporting makes it difficult to draw conclusions regarding the effectiveness and safety of these treatments. Therefore, initiatives such as Core Outcomes in Women's and Newborn Health (CROWN), which was developed to harmonize outcome reporting in women's health research, and the World Endometriosis Research Foundation (WERF) Endometriosis Phenome and Biobanking Harmonisation Project (EPHect), which was developed to standardize data and sample collection in endometriosis, are essential for progress in the future.
      • Khan K.
      The CROWN Initiative: journal editors invite researchers to develop core outcomes in women's health.
      • Becker CM
      • Laufer MR
      • Stratton P
      • et al.
      World Endometriosis Research Foundation Endometriosis Phenome and Biobanking Harmonisation Project: I.
      The medical management of endometriosis-associated pain is well recognized as a beneficial intervention either as a prelude to considering surgical management or postoperatively to prevent the recurrence of pain.
      • Dunselman GA
      • Vermeulen N
      • Becker C
      • et al.
      ESHRE guideline: management of women with endometriosis.
      The endometriosis-associated pain VAS scores reported at baseline in this review (5.5–7.5 cm) were similar to those found in our previous systematic review exploring the treatment of endometriosis with various medical therapies (5.5–6.1 cm).
      • Becker CM
      • Gattrell WT
      • Gude K
      • et al.
      Reevaluating response and failure of medical treatment of endometriosis: a systematic review.
      Moreover, the combined findings of our systematic reviews indicate that there is a lack of clear, consistent data concerning the long-term pain relief that patients may expect following medical or surgical treatment for endometriosis. Thus, providing women with clear, evidence-based recommendations regarding the most appropriate treatment options remains difficult.
      • Becker CM
      • Gattrell WT
      • Gude K
      • et al.
      Reevaluating response and failure of medical treatment of endometriosis: a systematic review.

       Strengths, Limitations, and Sources of Bias in the Findings

      This systematic review provides useful information on surgical practices and outcomes in women with endometriosis. However, it is important to note that this review focused on surgical interventions only. In clinical practice, physicians most commonly combine medical and surgical interventions to treat endometriosis-associated pain. It is possible, therefore, that differences in medical treatment patterns may have introduced bias in relation to the effectiveness of surgery in this review and in the source studies. Furthermore, because many of the published studies were conducted at centres of expertise specializing in endometriosis management, the findings may not be generalizable throughout the gynaecology community.
      Other factors that may have influenced or biased the findings include the designs of the source studies (e.g., the presence or absence of blinding or randomization), patient characteristics, and lack of consistency among the source studies when reporting lesion locations and outcomes. Several different surgical techniques were used to treat endometriosis-associated pain, particularly in the lesion excision and deep endometriosis groups. Efficacy and AEs were not analyzed by route of surgery because the surgical technique was not consistently reported in all studies. Furthermore, the diversity of the patient cohorts, even within individual studies, is likely to have influenced our findings. For example, young age at disease onset, chronic endometriosis-associated pain, time following treatment, and more severe disease are risk factors for multiple surgical interventions for endometriosis.
      • Cheong Y
      • Tay P
      • Luk F
      • et al.
      Laparoscopic surgery for endometriosis: how often do we need to re-operate?.
      Patient characteristics such as age will also have influenced the choice of surgical treatment. Although the heterogeneity of the patient population reflects clinical practice, it complicates direct comparisons across studies or treatment groups, and it may account for the wide ranges in some data. In addition, evaluation of the outcomes data was complicated because of the diversity of methods used to assess endometriosis-associated pain. Further factors impeding comparison among studies, and which could have introduced bias in the findings, include differences in follow-up times and changing standards of care over the study period.

      CONCLUSION

      To improve the care provided to women experiencing endometriosis-associated pain, a systematic and defined approach to the study of interventions is required. Research on the long-term effectiveness of surgery appears to be in its infancy, and, as a result, the ability to counsel women on outcomes of management is limited at this time.

      Acknowledgement

      The authors thank Andreas Leidenroth, PhD for assisting in the screening of article abstracts.

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