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Recurrence in Deep Infiltrating Endometriosis: A Systematic Review of the Literature

  • Manuel Maria Ianieri
    Correspondence
    Corresponding author: Manuel Maria Ianieri, MD, Strada dei cipressi N 1, Chieti 66100, Italy.
    Affiliations
    Department of Obstetrics and Gynecology, Gynecologic Oncology and Minimally Invasive Pelvic Surgery, International School of Surgical Anatomy, Sacred Heart Hospital, Negrar, Verona, Italy

    Department of Medical and Oral Sciences and Biotechnologies, “G.D'Annunzio” University, Chieti, Italy
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  • Daniele Mautone
    Affiliations
    Department of Obstetrics and Gynecology, Gynecologic Oncology and Minimally Invasive Pelvic Surgery, International School of Surgical Anatomy, Sacred Heart Hospital, Negrar, Verona, Italy
    Search for articles by this author
  • Marcello Ceccaroni
    Affiliations
    Department of Obstetrics and Gynecology, Gynecologic Oncology and Minimally Invasive Pelvic Surgery, International School of Surgical Anatomy, Sacred Heart Hospital, Negrar, Verona, Italy
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Published:January 19, 2018DOI:https://doi.org/10.1016/j.jmig.2017.12.025

      Abstract

      Deep infiltrative endometriosis (DIE) is an enigmatic disease that typically impacts the rectovaginal septum, uterosacral ligaments, pararectal space, and vesicouterine fold but can involve the rectum, sigma, ileum, ureters, diaphragm, and other less common sites. Surgery is the treatment of choice because medical management alone commonly fails in controlling the symptoms although recurrence is very high after surgical treatment. The goal of the current study was to review recurrence rates and identify risk factors related to recurrence after surgery for DIE. The review involved searching the Cochrane Library, PubMed, and Google Scholar for relevant articles in accordance with the study's inclusion criteria; 45 studies were considered suitable. The results showed a wide heterogeneity regarding DIE recurrence because of inconsistent recurrence definitions and follow-up length. Younger age and high body mass index were found to be risk factors for DIE recurrence. Lack of complete surgical excision was another independent risk factor for recurrence of disease. In conclusion, there is a need for prospective studies and a more homogeneous standard for surgical treatment of DIE.

      Keywords

      Endometriosis is a chronic gynecologic condition that affects women primarily during the reproductive years causing infertility and pelvic pain although there are rare reported postmenopausal cases [
      • Ianieri M.M.
      • Buca D.I.
      • Panaccio P.
      • Cieri M.
      • Francomano F.
      • Liberati M.
      Retroperitoneal endometriosis in postmenopausal woman causing deep vein thrombosis: case report and review of the literature.
      ]. Essentially, 3 types of lesions are reported: ovarian endometriosis, superficial peritoneal endometriosis, and deep infiltrating endometriosis (DIE) [
      • Nisolle M.
      • Donnez J.
      Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities.
      ].
      DIE is defined as an invasion greater than 5 mm of the peritoneal surface by endometriotic lesions, most commonly located at the rectovaginal septum, uterosacral ligaments, pararectal space, and vesicouterine fold [
      • Scioscia M.
      • Bruni F.
      • Ceccaroni M.
      • Steinkasserer M.
      • Stepniewska A.
      • Minelli L.
      Distribution of endometriotic lesions in endometriosis stage IV supports the menstrual reflux theory and requires specific preoperative assessment and therapy.
      ]. These lesions differ from other peritoneal surface lesions because of histopathologic features and a strong pelvic pain correlation [
      • Koninckx P.R.
      • Oosterlynck D.
      • D'Hooghe T.
      • Meuleman C.
      Deeply infiltrating endometriosis is a disease whereas mild endometriosis could be considered a non-disease.
      ]. DIE can also infiltrate the rectum, sigma, ileum, bladder, and even the diaphragm and upper abdomen [
      • Scioscia M.
      • Bruni F.
      • Ceccaroni M.
      • Steinkasserer M.
      • Stepniewska A.
      • Minelli L.
      Distribution of endometriotic lesions in endometriosis stage IV supports the menstrual reflux theory and requires specific preoperative assessment and therapy.
      ]. Gastrointestinal involvement of endometriosis in the rectosigmoid, small bowel (distal ileum), cecum, and appendix is the most common extragenital location [
      • Scioscia M.
      • Bruni F.
      • Ceccaroni M.
      • Steinkasserer M.
      • Stepniewska A.
      • Minelli L.
      Distribution of endometriotic lesions in endometriosis stage IV supports the menstrual reflux theory and requires specific preoperative assessment and therapy.
      ,
      • 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.
      ].
      Surgery is the treatment of choice for DIE management because medical treatment alone fails to control symptoms; there is evidence that indicates that surgery reduces pain associated with endometriosis in all stages of the disease [
      • Duffy J.M.
      • Arambage K.
      • Correa F.J.
      • et al.
      Laparoscopic surgery for endometriosis.
      ]. After excisional surgery, recurrence of DIE varies between 2% and 43% depending on the length of follow-up [
      • 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.
      ,
      • Guo S.W.
      Recurrence of endometriosis and its control.
      ,
      • Dousset B.
      • Leconte M.
      • Borghese B.
      • et al.
      Complete surgery for low rectal endometriosis: long-term results of a 100-case prospective study.
      ,
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ,
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ,
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ,
      • Meuleman C.
      • Tomassetti C.
      • Wolthuis A.
      • et al.
      Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ,
      • Hanssens S.
      • Rubod C.
      • Kerdraon O.
      • et al.
      Pelvic endometriosis in women under 25: a specific management?.
      ]. The cause of this statistical fluctuation is unclear [
      • Guo S.W.
      Recurrence of endometriosis and its control.
      ] but may depend on the definition of recurrence, sample size, and study group. The aim of this review was to evaluate the recurrence rate and risks factors of recurrence after surgery for DIE with the goal of reducing relapses.

      Materials and Methods

      We conducted a review of literature electronically using PubMed, Cochrane Central Register of Controlled Trials, and Google Scholar to find studies on the recurrence and risk factors for DIE published between January 2000 and June 2017. The Medical Subject Headings terms “deep endometriosis,” “deep infiltrating endometriosis,” “bowel endometriosis,” “colorectal endometriosis,” “rectovaginal endometriosis,” “bladder endometriosis,” “ureteral endometriosis,” and “diaphragmatic endometriosis” were combined with “recurrence,” “relapse,” and “risk factors.” Reference lists from the relevant publications were searched for additional studies on the subject. The studies were screened by title and abstract, and if after reading the full text they met the inclusion criteria, they were selected by 2 authors.
      Inclusion criteria were articles published in English with the primary topic being DIE and clearly reported recurrence rates and/or risk factors of relapse after surgery. Exclusion criteria were case reports, those articles not providing a clear differentiation between superficial endometriosis and DIE, and studies evaluating specifically the effect of hormone therapy on the recurrence rate of DIE.
      A meta-analysis was not performed because the data were widely heterogeneous and incomplete with inconsistent definitions of DIE recurrence, inconsistent types of surgery, and other varying analyzed risk factors of relapse.

      Results

       Recurrence Rate of DIE: Overall Consideration

      One thousand five hundred twenty-six publications were identified. After duplicates were removed and studies were screened for inclusion and exclusion criteria, 38 articles were suitable for review [
      • 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.
      ,
      • Dousset B.
      • Leconte M.
      • Borghese B.
      • et al.
      Complete surgery for low rectal endometriosis: long-term results of a 100-case prospective study.
      ,
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ,
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ,
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ,
      • Meuleman C.
      • Tomassetti C.
      • Wolthuis A.
      • et al.
      Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ,
      • Hanssens S.
      • Rubod C.
      • Kerdraon O.
      • et al.
      Pelvic endometriosis in women under 25: a specific management?.
      ,
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ,
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      ,
      • Stepniewska A.
      • Pomini P.
      • Guerriero M.
      • Scioscia M.
      • Ruffo G.
      • Minelli L.
      Colorectal endometriosis: benefits of long-term follow-up in patients who underwent laparoscopic surgery.
      ,
      • Minelli L.
      • Fanfani F.
      • Fagotti A.
      • et al.
      Laparoscopic colorectal resection for bowel endometriosis: feasibility, complications, and clinical outcome.
      ,
      • Roman H.
      • Milles M.
      • Vassilieff M.
      • et al.
      Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis.
      ,
      • Fanfani F.
      • Fagotti A.
      • Gagliardi M.L.
      • et al.
      Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study.
      ,
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ,
      • 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.
      ,
      • Kavallaris A.
      • Chalvatzas N.
      • Hornemann A.
      • Banz C.
      • Diedrich K.
      • Agic A.
      94 months follow-up after laparoscopic assisted vaginal resection of septum rectovaginal and rectosigmoid in women with deep infiltrating endometriosis.
      ,
      • Soriano D.
      • Schonman R.
      • Nadu A.
      • et al.
      Multidisciplinary team approach to management of severe endometriosis affecting the ureter: long-term outcome data and treatment algorithm.
      ,
      • Uccella S.
      • Cromi A.
      • Casarin J.
      • et al.
      Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes.
      ,
      • Camanni M.
      • Bonino L.
      • Delpiano E.M.
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      ,
      • Frenna V.
      • Santos L.
      • Ohana E.
      • Bailey C.
      • Wattiez A.
      Laparoscopic management of ureteral endometriosis: our experience.
      ,
      • Mereu L.
      • Gagliardi M.L.
      • Clarizia R.
      • Mainardi P.
      • Landi S.
      • Minelli L.
      Laparoscopic management of ureteral endometriosis in case of moderate-severe hydroureteronephrosis.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bergamini V.
      • Berlanda N.
      • Carmignani L.
      Long-term follow-up after conservative surgery for bladder endometriosis.
      ,
      • Ciriaco P.
      • Negri G.
      • Libretti L.
      • et al.
      Surgical treatment of catamenial pneumothorax: a single centre experience.
      ,
      • Korom S.
      • Canyurt H.
      • Missbach A.
      • et al.
      Catamenial pneumothorax revisited: clinical approach and systematic review of the literature.
      ,
      • Alifano M.
      • Jablonski C.
      • Kadiri H.
      • et al.
      Catamenial and noncatamenial, endometriosis-related or nonendometriosis-related pneumothorax referred for surgery.
      ,
      • Attaran S.
      • Bille A.
      • Karenovics W.
      • Lang-Lazdunski L.
      Videothoracoscopic repair of diaphragm and pleurectomy/abrasion in patients with catamenial pneumothorax: a 9-year experience.
      ,
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      ,
      • Visouli A.N.
      • Darwiche K.
      • Mpakas A.
      • et al.
      Catamenial pneumothorax: a rare entity? Report of 5 cases and review of the literature.
      ,
      • Haga T.
      • Kurihara M.
      • Kataoka H.
      • Ebana H.
      Clinical-pathological findings of catamenial pneumothorax: comparison between recurrent cases and non-recurrent cases.
      ,
      • Chiantera V.
      • Dessole M.
      • Petrillo M.
      • et al.
      Laparoscopic en bloc right diaphragmatic peritonectomy for diaphragmatic endometriosis according to the Sugarbaker technique.
      ,
      • Nezhat C.
      • Main J.
      • Paka C.
      • Nezhat A.
      • Beyqui R.E.
      Multidisciplinary treatment for thoracic and abdominopelvic endometriosis.
      ,
      • Fukuoka M.
      • Kurihara M.
      • Haga T.
      • et al.
      Clinical characteristics of catamenial and non-catamenial thoracic endometriosis-related pneumothorax.
      ,
      • Alifano M.
      • Legras A.
      • Rousset-Jablonski C.
      • et al.
      Pneumothorax recurrence after surgery in women: clinicopathologic characteristics and management.
      ,
      • Rousset-Jablonski C.
      • Alifano M.
      • Plu-Bureau G.
      • et al.
      Catamenial pneumothorax and endometriosis-related pneumothorax.
      ].
      The reported risk of recurrence after surgery for DIE varies greatly among studies but overall does so because of the definition of recurrence and the length of follow-up. In particular, the recurrence rate of DIE has been reported in less than 50% of studies as shown by Meuleman et al [
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ]. The majority of studies report a short- or midterm follow-up of 2 to 4 years, with a tendency of an increased recurrence rate in studies with a longer follow-up [
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ,
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ,
      • Meuleman C.
      • Tomassetti C.
      • Wolthuis A.
      • et al.
      Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study.
      ]. According to Guo [
      • Guo S.W.
      Recurrence of endometriosis and its control.
      ], Doussett et al [
      • Dousset B.
      • Leconte M.
      • Borghese B.
      • et al.
      Complete surgery for low rectal endometriosis: long-term results of a 100-case prospective study.
      ], and Vignali et al [
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ], the recurrence rate in women with DIE varies between 2% and 43.5% and is higher when the symptom recurrence noted is pain rather than surgical findings as the definition of relapse [
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ,
      • Hanssens S.
      • Rubod C.
      • Kerdraon O.
      • et al.
      Pelvic endometriosis in women under 25: a specific management?.
      ]. In addition to these differing factors, the majority of randomized controlled or retrospective studies [
      • Parazzini F.
      • Bertulessi C.
      • Pasini A.
      • et al.
      Determinants of short term recurrence rate of endometriosis.
      ,
      • Stratton P.
      • Sinaii N.
      • Segars J.
      • et al.
      Return of chronic pelvic pain from endometriosis after raloxifene treatment: a randomized controlled trial.
      ] do not focus on DIE recurrence but use a matched rate for superficial endometriosis and DIE as per the revised American Fertility Society classification [
      • American Society for Reproductive Medicine
      Revised American Society for Reproductive Medicine classification of endometriosis: 1996.
      ]. The articles summarized in the current review evaluate the DIE recurrence rate and recurrence risks factors after DIE surgery and are summarized in Table [
      • 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.
      ,
      • Dousset B.
      • Leconte M.
      • Borghese B.
      • et al.
      Complete surgery for low rectal endometriosis: long-term results of a 100-case prospective study.
      ,
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ,
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ,
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ,
      • Meuleman C.
      • Tomassetti C.
      • Wolthuis A.
      • et al.
      Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ,
      • Hanssens S.
      • Rubod C.
      • Kerdraon O.
      • et al.
      Pelvic endometriosis in women under 25: a specific management?.
      ,
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ,
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      ,
      • Stepniewska A.
      • Pomini P.
      • Guerriero M.
      • Scioscia M.
      • Ruffo G.
      • Minelli L.
      Colorectal endometriosis: benefits of long-term follow-up in patients who underwent laparoscopic surgery.
      ,
      • Minelli L.
      • Fanfani F.
      • Fagotti A.
      • et al.
      Laparoscopic colorectal resection for bowel endometriosis: feasibility, complications, and clinical outcome.
      ,
      • Roman H.
      • Milles M.
      • Vassilieff M.
      • et al.
      Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis.
      ,
      • Fanfani F.
      • Fagotti A.
      • Gagliardi M.L.
      • et al.
      Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study.
      ,
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ,
      • 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.
      ,
      • Kavallaris A.
      • Chalvatzas N.
      • Hornemann A.
      • Banz C.
      • Diedrich K.
      • Agic A.
      94 months follow-up after laparoscopic assisted vaginal resection of septum rectovaginal and rectosigmoid in women with deep infiltrating endometriosis.
      ,
      • Soriano D.
      • Schonman R.
      • Nadu A.
      • et al.
      Multidisciplinary team approach to management of severe endometriosis affecting the ureter: long-term outcome data and treatment algorithm.
      ,
      • Uccella S.
      • Cromi A.
      • Casarin J.
      • et al.
      Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes.
      ,
      • Camanni M.
      • Bonino L.
      • Delpiano E.M.
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      ,
      • Frenna V.
      • Santos L.
      • Ohana E.
      • Bailey C.
      • Wattiez A.
      Laparoscopic management of ureteral endometriosis: our experience.
      ,
      • Mereu L.
      • Gagliardi M.L.
      • Clarizia R.
      • Mainardi P.
      • Landi S.
      • Minelli L.
      Laparoscopic management of ureteral endometriosis in case of moderate-severe hydroureteronephrosis.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bergamini V.
      • Berlanda N.
      • Carmignani L.
      Long-term follow-up after conservative surgery for bladder endometriosis.
      ,
      • Ciriaco P.
      • Negri G.
      • Libretti L.
      • et al.
      Surgical treatment of catamenial pneumothorax: a single centre experience.
      ,
      • Korom S.
      • Canyurt H.
      • Missbach A.
      • et al.
      Catamenial pneumothorax revisited: clinical approach and systematic review of the literature.
      ,
      • Alifano M.
      • Jablonski C.
      • Kadiri H.
      • et al.
      Catamenial and noncatamenial, endometriosis-related or nonendometriosis-related pneumothorax referred for surgery.
      ,
      • Attaran S.
      • Bille A.
      • Karenovics W.
      • Lang-Lazdunski L.
      Videothoracoscopic repair of diaphragm and pleurectomy/abrasion in patients with catamenial pneumothorax: a 9-year experience.
      ,
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      ,
      • Visouli A.N.
      • Darwiche K.
      • Mpakas A.
      • et al.
      Catamenial pneumothorax: a rare entity? Report of 5 cases and review of the literature.
      ,
      • Haga T.
      • Kurihara M.
      • Kataoka H.
      • Ebana H.
      Clinical-pathological findings of catamenial pneumothorax: comparison between recurrent cases and non-recurrent cases.
      ,
      • Chiantera V.
      • Dessole M.
      • Petrillo M.
      • et al.
      Laparoscopic en bloc right diaphragmatic peritonectomy for diaphragmatic endometriosis according to the Sugarbaker technique.
      ,
      • Nezhat C.
      • Main J.
      • Paka C.
      • Nezhat A.
      • Beyqui R.E.
      Multidisciplinary treatment for thoracic and abdominopelvic endometriosis.
      ,
      • Fukuoka M.
      • Kurihara M.
      • Haga T.
      • et al.
      Clinical characteristics of catamenial and non-catamenial thoracic endometriosis-related pneumothorax.
      ,
      • Alifano M.
      • Legras A.
      • Rousset-Jablonski C.
      • et al.
      Pneumothorax recurrence after surgery in women: clinicopathologic characteristics and management.
      ,
      • Rousset-Jablonski C.
      • Alifano M.
      • Plu-Bureau G.
      • et al.
      Catamenial pneumothorax and endometriosis-related pneumothorax.
      ].
      TableThe recurrence rate as reported by various published studies
      Author and Year of PublicationType of Study and Sample SizeType of EndometriosisDefinition of RecurrenceRecurrence (%)Length of Follow-up
      Ruffo et al, 2014
      • 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.
      Retrospective, N = 900Bowel endometriosisSymptom recurrence, reintervention2.91–120 months
      Dousset et al, 2010
      • Dousset B.
      • Leconte M.
      • Borghese B.
      • et al.
      Complete surgery for low rectal endometriosis: long-term results of a 100-case prospective study.
      Prospective, N = 100Bowel endometriosisReintervention263–93 months
      Vignali et al, 2005
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      Retrospective, N = 150DIESymptom recurrence, clinical findings, ultrasoundSymptom recurrence after 36 months: 20.5

      Clinical recurrence after 36 months: 9

      Symptom recurrence after 60 months: 43.5

      Clinical recurrence after 60 months: 28
      10–60 months
      Meuleman et al, 2011
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      Retrospective, N = 45Bowel endometriosisReinterventionAfter 12-month follow-up: 2.2

      After 26-month follow-up: 4.4
      12–36 months
      Busacca et al, 2006
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      Retrospective, N = 1106

      Ovarian endometriosis, n = 367

      Peritoneal endometriosis, n = 198

      DIE, n = 152

      Peritoneal + ovarian endometriosis, n = 320
      Ovarian, peritoneal, DIE, ovarian + peritoneal endometriosisSymptom recurrence, clinical findings, ultrasound, increased cancer antigen 125DIE group after 48 months: 30.6

      DIE group after 96 months: 43.3
      96 months
      Meuleman et al, 2014
      • Meuleman C.
      • Tomassetti C.
      • Wolthuis A.
      • et al.
      Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study.
      Prospective, N = 203DIE with or without bowel endometriosisReinterventionAfter 12-month follow-up: 1

      After 24-month follow-up: 7

      After 36-month follow-up: 10
      12–36 months
      Fedele et al, 2004
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      Retrospective, N = 83DIE, bowel endometriosisClinical findings, ultrasound, reinterventionPain recurrence: 28

      Clinical recurrence: 34

      Reintervention: 27
      36 months
      Hanssens et al, 2015
      • Hanssens S.
      • Rubod C.
      • Kerdraon O.
      • et al.
      Pelvic endometriosis in women under 25: a specific management?.
      Retrospective, N = 108

      DIE group, n = 49

      SE, n = 59
      DIESymptom recurrence, reinterventionDIE group symptom recurrence: 50

      DIE group reintervention: 35.7

      SE group symptom recurrence: 21.7

      SE group reintervention: 19.6
      6–80 months
      Nirgianakis et al, 2014
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      Retrospective, N = 81Bowel endometriosisReintervention1612–120 months
      Nezhat et al, 2011
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      Retrospective, N = 193Bowel endometriosisReintervention1012–96 months
      Donnez et al, 2010
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      Prospective, N = 500Bowel endometriosisSymptom recurrence824–76 months
      Stepniewska et al, 2010
      • Stepniewska A.
      • Pomini P.
      • Guerriero M.
      • Scioscia M.
      • Ruffo G.
      • Minelli L.
      Colorectal endometriosis: benefits of long-term follow-up in patients who underwent laparoscopic surgery.
      Retrospective

      Segmental resection

      (A), n = 60

      DIE without bowel surgery

      (B), n = 40

      DIE (no bowel endometriosis)

      (C), n = 55
      Bowel endometriosis

      DIE without bowel endometriosis
      Symptom recurrence, radiologic evaluation, ultrasound, reinterventionSymptom recurrence

      Group A: 10

      Group B: 35

      Group C: not specified

      Radiologic recurrence

      Group A: 7

      Group B: 23

      Group C: 5

      Reintervention

      Group A: 7

      Group B: 15

      Group C: 0
      48 months
      Minelli et al, 2009
      • Minelli L.
      • Fanfani F.
      • Fagotti A.
      • et al.
      Laparoscopic colorectal resection for bowel endometriosis: feasibility, complications, and clinical outcome.
      Retrospective, N = 357Bowel endometriosisSymptom recurrence, radiologic evaluation, ultrasound, reintervention8.46–48 months
      Roman et al, 2016
      • Roman H.
      • Milles M.
      • Vassilieff M.
      • et al.
      Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis.
      Retrospective, N = 71

      Group 1: shaving, n = 46

      Group 2: bowel resection, n = 25
      Bowel endometriosisReinterventionGroup 1: shaving: 8.6

      Group 2: bowel resection: 0
      60–120 months
      Fanfani et al, 2010
      • Fanfani F.
      • Fagotti A.
      • Gagliardi M.L.
      • et al.
      Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study.
      Prospective case-control study

      Discoid resection (case), n = 48

      Segmental resection (control), n = 88
      Bowel endometriosisSymptom recurrence, radiologic evaluation, ultrasoundDiscoid resection group: 13.8

      Segmental resection group: 11.5
      16–46 months
      Koh et al, 2012
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      Retrospective, N = 91Bowel endometriosisReintervention1112–116 months
      Mabrouk et al, 2012
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      Retrospective, N = 47Bowel endometriosisSymptom recurrence196–35 months
      Roman et al, 2016
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      Prospective, N = 103

      Women without BOME, n = 88

      Women with BOME, n = 15
      Bowel endometriosisReinterventionPatients without BOME: 0

      Patients with BOME: 6.6
      Relapse was reported in 9 cases in the peritoneum and/or ovaries and 2 cases in the rectovaginal septum, and 1 case required a new bowel resection.
      12–36 months
      Afors et al, 2016
      • 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.
      Retrospective, N = 92

      Group 1: shaving, n = 47

      Group 2: discoid resection, n = 15

      Group 3: segmental resection, n = 30
      Bowel endometriosisSymptom recurrence, reinterventionGroup 1: shaving: 27.6

      Group 2: discoid resection: 13.3

      Group 3: segmental resection: 6.6
      24 months
      Kavallaris et al, 2011
      • Kavallaris A.
      • Chalvatzas N.
      • Hornemann A.
      • Banz C.
      • Diedrich K.
      • Agic A.
      94 months follow-up after laparoscopic assisted vaginal resection of septum rectovaginal and rectosigmoid in women with deep infiltrating endometriosis.
      Retrospective, N = 55Bowel endometriosisSymptom recurrence6.694 months
      Soriano et al, 2011
      • Soriano D.
      • Schonman R.
      • Nadu A.
      • et al.
      Multidisciplinary team approach to management of severe endometriosis affecting the ureter: long-term outcome data and treatment algorithm.
      Prospective, N = 45

      Ureterolysis, n = 41

      Ureterocystoneostomy, n = 4
      Ureteral endometriosisReinterventionUreterolysis: 4.8

      Ureterocystoneostomy: 0
      13–33 months
      Uccella et al, 2014
      • Uccella S.
      • Cromi A.
      • Casarin J.
      • et al.
      Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes.
      Retrospective (ureterolysis), N = 109 (follow-up >12 months only for 80 women)Ureteral endometriosisReintervention8.615–109 months
      Camanni et al, 2009
      • Camanni M.
      • Bonino L.
      • Delpiano E.M.
      • et al.
      Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to ureterolysis.
      Retrospective, N = 80

      Ureterolysis, n = 76

      Ureterocystoneostomy, n = 4
      Ureteral endometriosisReinterventionUreterolysis: 2.6

      Ureterocystoneostomy: 0
      7–24 months
      Frenna et al, 2007
      • Frenna V.
      • Santos L.
      • Ohana E.
      • Bailey C.
      • Wattiez A.
      Laparoscopic management of ureteral endometriosis: our experience.
      Retrospective (ureterolysis), N = 54Ureteral endometriosisClinical findings75–12 months
      Mereu et al, 2010
      • Mereu L.
      • Gagliardi M.L.
      • Clarizia R.
      • Mainardi P.
      • Landi S.
      • Minelli L.
      Laparoscopic management of ureteral endometriosis in case of moderate-severe hydroureteronephrosis.
      Prospective, N = 56

      Laparoscopic ureteroureterostomy, n = 17

      Ureterolysis, n = 35

      Ureterocystoneostomy, n = 2

      Nephrectomy, n = 2
      Ureteral endometriosisClinical findings, ultrasound, reinterventionLaparoscopic ureteroureterostomy: 0

      Ureterolysis: 21.4

      Ureterocystoneostomy: 0
      10–62 months
      Fedele et al, 2005
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bergamini V.
      • Berlanda N.
      • Carmignani L.
      Long-term follow-up after conservative surgery for bladder endometriosis.
      Retrospective, N = 47

      Base vesical lesion, n = 33

      Dome vesical lesion, n = 14
      Bladder endometriosisClinical findings, symptom recurrence, radiologic evaluationBase lesion symptoms recurrence: 24.7

      Base lesion clinical/instrumental recurrence: 15.5

      Dome lesion symptom recurrence: 0

      Dome lesion clinical/instrumental recurrence: 0
      24–108 months
      Ciriaco et al, 2009
      • Ciriaco P.
      • Negri G.
      • Libretti L.
      • et al.
      Surgical treatment of catamenial pneumothorax: a single centre experience.
      Retrospective, N = 10Diaphragmatic endometriosisSymptom recurrence4014–168 months
      Korom et al, 2004
      • Korom S.
      • Canyurt H.
      • Missbach A.
      • et al.
      Catamenial pneumothorax revisited: clinical approach and systematic review of the literature.
      Retrospective, N = 3Diaphragmatic endometriosisSymptom recurrence013–22 months
      Alifano et al, 2007
      • Alifano M.
      • Jablonski C.
      • Kadiri H.
      • et al.
      Catamenial and noncatamenial, endometriosis-related or nonendometriosis-related pneumothorax referred for surgery.
      Retrospective, N = 114

      Catamenial pneumothorax, n = 28

      Noncatamenial pneumothorax, n = 86
      Diaphragmatic endometriosisSymptom recurrenceCatamenial pneumothorax: 32

      Noncatamenial pneumothorax endometriosis related: 27

      Noncatamenial pneumothorax/not endometriosis related: 5.3
      32.7 months
      Attaran et al, 2013
      • Attaran S.
      • Bille A.
      • Karenovics W.
      • Lang-Lazdunski L.
      Videothoracoscopic repair of diaphragm and pleurectomy/abrasion in patients with catamenial pneumothorax: a 9-year experience.
      Retrospective, N = 12Diaphragmatic endometriosisSymptom recurrence8.317–73 months
      Ceccaroni et al, 2013
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      Retrospective, N = 46Diaphragmatic endometriosisSymptom recurrence, radiological evaluationNot specified84 months
      Visouli et al, 2012
      • Visouli A.N.
      • Darwiche K.
      • Mpakas A.
      • et al.
      Catamenial pneumothorax: a rare entity? Report of 5 cases and review of the literature.
      Retrospective, N = 5Diaphragmatic endometriosisSymptom recurrence, radiologic evaluationRecurrence of pneumothorax: 2016–46

      months
      Haga et al, 2014
      • Haga T.
      • Kurihara M.
      • Kataoka H.
      • Ebana H.
      Clinical-pathological findings of catamenial pneumothorax: comparison between recurrent cases and non-recurrent cases.
      Retrospective, N = 92Diaphragmatic endometriosisSymptom recurrence39.125–63 months
      Chiantera et al, 2016
      • Chiantera V.
      • Dessole M.
      • Petrillo M.
      • et al.
      Laparoscopic en bloc right diaphragmatic peritonectomy for diaphragmatic endometriosis according to the Sugarbaker technique.
      Retrospective, N = 9Diaphragmatic endometriosisSymptom recurrence06 months
      Nezhat et al, 2014
      • Nezhat C.
      • Main J.
      • Paka C.
      • Nezhat A.
      • Beyqui R.E.
      Multidisciplinary treatment for thoracic and abdominopelvic endometriosis.
      Retrospective, N = 25Diaphragmatic endometriosisSymptom recurrence, radiologic evaluation83–18 months
      Fukuoka et al, 2015
      • Fukuoka M.
      • Kurihara M.
      • Haga T.
      • et al.
      Clinical characteristics of catamenial and non-catamenial thoracic endometriosis-related pneumothorax.
      Retrospective, N = 150Diaphragmatic endometriosisNot specified348–48 months
      Alifano et al, 2011
      • Alifano M.
      • Legras A.
      • Rousset-Jablonski C.
      • et al.
      Pneumothorax recurrence after surgery in women: clinicopathologic characteristics and management.
      Retrospective, N = 35Diaphragmatic endometriosisSymptom recurrence, radiologic evaluation17.11.5–138 months
      Rousset-Jablonski et al, 2011
      • Rousset-Jablonski C.
      • Alifano M.
      • Plu-Bureau G.
      • et al.
      Catamenial pneumothorax and endometriosis-related pneumothorax.
      Retrospective, N = 156Diaphragmatic endometriosisSymptom recurrence, radiologic evaluation2520–100 months
      BOME = bowel occult microscopic endometriosis; DIE = deep infiltrating endometriosis; SE = superficial endometriosis.
      * Relapse was reported in 9 cases in the peritoneum and/or ovaries and 2 cases in the rectovaginal septum, and 1 case required a new bowel resection.

       Recurrence and Risk Factors of Relapse of DIE, Bowel Endometriosis, Colorectal Endometriosis, and Rectovaginal Endometriosis

      From an accurate evaluation of the literature, 3 risk factors for recurrence of DIE involving the bowel were found to be modifiable and nonmodifiable factors: age, weight, and type of surgery. Younger age at primary surgery for DIE excision is recognized by several authors as a risk factor for recurrence of DIE [
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ]. It is well-known that the incidence of laparoscopically confirmed endometriosis decreases with increasing age [
      • Missmer S.A.
      • Hankinson S.E.
      • Spiegelman D.
      • Barbieri R.L.
      • Marshall L.M.
      • Hunter D.J.
      Incidence of laparoscopically confirmed endometriosis by demographic, anthropometric, and lifestyle factors.
      ]. Busacca et al [
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ] have reported that women ≥34 years old have a decreased recurrence rate compared with woman ≤33 years old. Similar results have been reported in a retrospective study by Nirgianakis et al [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ] in which women <31 years old independently predicted DIE recurrence.
      Body mass index (BMI) is another independent risk factor for disease recurrence [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ]. Obese women have a significantly higher rate (p = .002) of recurrence compared with those with normal BMI [
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ]. In the study by Nirgianakis et al [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ], BMI ≥23 kg/m2 was associated with a higher recurrence risk (p < .001).
      Several authors have concluded that pregnancy after surgery seems to reduce recurrence of DIE [
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ]. In 2010, Donnez and Squifflet [
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      ] reported that the recurrence rate of pelvic pain was significantly lower in women who became pregnant after surgery for DIE.
      Incomplete excision during surgery for DIE seems to be an independent risk factor for the recurrence of symptoms [
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ,
      • Stepniewska A.
      • Pomini P.
      • Guerriero M.
      • Scioscia M.
      • Ruffo G.
      • Minelli L.
      Colorectal endometriosis: benefits of long-term follow-up in patients who underwent laparoscopic surgery.
      ,
      • Stepniewska A.
      • Pomini P.
      • Bruni F.
      • et al.
      Laparoscopic treatment of bowel endometriosis in infertile women.
      ]. A retrospective study by Vignali et al [
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ] has shown that reoperation for DIE was predicted only by incomplete excision during the first operation (odds ratio = 21.9; 95% confidence interval, 3.2–146.5; p < .001).
      Concerning the type of surgical treatment for DIE, 2 approaches are being practiced: radical bowel surgery and conservative bowel surgery [
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      ,
      • Minelli L.
      • Fanfani F.
      • Fagotti A.
      • et al.
      Laparoscopic colorectal resection for bowel endometriosis: feasibility, complications, and clinical outcome.
      ,
      • Roman H.
      • Milles M.
      • Vassilieff M.
      • et al.
      Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis.
      ,
      • Fanfani F.
      • Fagotti A.
      • Gagliardi M.L.
      • et al.
      Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study.
      ,
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ,
      • 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.
      ,
      • Stepniewska A.
      • Pomini P.
      • Bruni F.
      • et al.
      Laparoscopic treatment of bowel endometriosis in infertile women.
      ,
      • Darwish B.
      • Roman H.
      Surgical treatment of deep infiltrating rectal endometriosis: in favor of less aggressive surgery.
      ,
      • Ceccaroni M.
      • Clarizia R.
      • Bruni F.
      • et al.
      Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial.
      ,
      • Kondo W.
      • Ribeiro R.
      • Zomer M.T.
      • Hayashi R.
      Laparoscopic double discoid resection with a circular stapler for bowel endometriosis.
      ,
      • Badescu A.
      • Roman H.
      • Aziz M.
      • et al.
      Mapping of bowel occult microscopic endometriosis implants surrounding deep endometriosis nodules infiltrating the bowel.
      ]. Radical rectal surgery includes colorectal resection by complete excision of the rectal segment affected by the disease [
      • Minelli L.
      • Fanfani F.
      • Fagotti A.
      • et al.
      Laparoscopic colorectal resection for bowel endometriosis: feasibility, complications, and clinical outcome.
      ,
      • Ceccaroni M.
      • Clarizia R.
      • Bruni F.
      • et al.
      Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial.
      ]. Conservative techniques may be performed by the practice of rectal shaving in which the rectum is not opened [
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      ,
      • Roman H.
      • Milles M.
      • Vassilieff M.
      • et al.
      Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis.
      ] or by full excision in which the endometriosis nodule along with the surrounding rectal wall are removed [
      • Fanfani F.
      • Fagotti A.
      • Gagliardi M.L.
      • et al.
      Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study.
      ,
      • Kondo W.
      • Ribeiro R.
      • Zomer M.T.
      • Hayashi R.
      Laparoscopic double discoid resection with a circular stapler for bowel endometriosis.
      ].
      Because the causes for recurrence are still not completely clear, there are conflicting opinions regarding the role of clear bowel resection margins and disease recurrence. We found only 4 reports that focused on the correlation between the histopathological margins collected from the resected tissue and the risk of recurrence of DIE or symptoms of DIE [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ]. Nirgianakis et al [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ] found 38.5% positive bowel resection margins in women with disease recurrence compared with 13.2% positive bowel resection in women without recurrence during a median follow-up period of 53 months (range, 12–120; p < .05). Other authors failed to demonstrate a correlation between positive bowel resection margins and higher risk of recurrence [
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ].
      There is a possible explanation for these conflicting results. Bowel occult microscopic endometriosis is detected in a visually normal peritoneum with an estimated prevalence up to 19% [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ]. Despite these data, bowel occult microscopic endometriosis seems to have no impact on either pelvic or digestive symptoms or recurrence of DIE after surgery [
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ].
      Regarding the type of surgery, there is some evidence to support the idea that conservative bowel surgery can lead to a higher risk of recurrence [
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ]. A large meta-analysis pooled more than 1600 patients from 49 retrospective studies. Seventy-one percent of patients underwent colorectal resection (10% full excision and 17% treated with superficial surgery) [
      • Meuleman C.
      • Tomassetti C.
      • D'Hoore A.
      • et al.
      Surgical treatment of deeply infiltrating endometriosis with colorectal involvement.
      ]. Overall, the proven endometriosis recurrence rate appeared to be significantly lower in the resection anastomosis group (2.5%, 20/812) compared with the conservative group (5.7%, 49/865).
      Afors et al [
      • 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.
      ] have compared symptoms and the need for reintervention retrospectively after segmental resection, discoid resection, or the shaving technique in 106 patients who underwent surgery for bowel endometriosis. Data showed a higher rate of reintervention for recurrence in the shaving group compared with discoid or segmental resection (27.6%, 13.3%, and 6.6%, respectively). Similar results have been reported by Roman et al [
      • Roman H.
      • Milles M.
      • Vassilieff M.
      • et al.
      Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis.
      ] in 2016, who found the recurrence rate after conservative surgery to be 8.6% versus 0% for patients who underwent colorectal resection in a mean follow-up period of 80 months. Different results have been reported in a case-control study comparing recurrence rates after bowel or discoid resection after a medium follow-up of 30 months with no significant difference in recurrence between radical bowel surgery and conservative surgery (13.8% vs 11.5%) [
      • Fanfani F.
      • Fagotti A.
      • Gagliardi M.L.
      • et al.
      Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study.
      ].

       Recurrence and Risk Factors of Relapse for Urinary Tract Endometriosis

      Urinary tract endometriosis is a form of DIE affecting 0.3% to 12% of all women suffering from endometriosis [
      • Badescu A.
      • Roman H.
      • Aziz M.
      • et al.
      Mapping of bowel occult microscopic endometriosis implants surrounding deep endometriosis nodules infiltrating the bowel.
      ]. The recurrence rate of ureteral endometriosis ranges between 0% and 12% [
      • Soriano D.
      • Schonman R.
      • Nadu A.
      • et al.
      Multidisciplinary team approach to management of severe endometriosis affecting the ureter: long-term outcome data and treatment algorithm.
      ,
      • Uccella S.
      • Cromi A.
      • Casarin J.
      • et al.
      Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes.
      ,
      • Maccagnano C.
      • Pellucchi F.
      • Rocchini L.
      • et al.
      Ureteral endometriosis: proposal for a diagnostic and therapeutic algorithm with a review of the literature.
      ,
      • Cavaco-Gomes J.
      • Martinho M.
      • Gilabert-Aguilar J.
      • Gilabert-Estelles J.
      Laparoscopic management of ureteral endometriosis: a systematic review.
      ].
      There are poor data regarding the risk factors associated with a higher recurrence rate after ureterolysis or ureterocystoneostomy. Uccella et al [
      • Uccella S.
      • Cromi A.
      • Casarin J.
      • et al.
      Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes.
      ] have shown that younger age (32.4 vs 37.6 years) at the time of ureterolysis (p = .004) and hydronephrosis grade ≥2 (p = .02) were associated with recurrence of symptoms after a long-term follow-up (i.e., 52 months).
      Radical surgery seems to lower recurrence of DIE in patients with ureteral endometriosis [
      • Frenna V.
      • Santos L.
      • Ohana E.
      • Bailey C.
      • Wattiez A.
      Laparoscopic management of ureteral endometriosis: our experience.
      ,
      • Mereu L.
      • Gagliardi M.L.
      • Clarizia R.
      • Mainardi P.
      • Landi S.
      • Minelli L.
      Laparoscopic management of ureteral endometriosis in case of moderate-severe hydroureteronephrosis.
      ,
      • Cavaco-Gomes J.
      • Martinho M.
      • Gilabert-Aguilar J.
      • Gilabert-Estelles J.
      Laparoscopic management of ureteral endometriosis: a systematic review.
      ]. A recent review comparing ureterolysis with ureterocystoneostomy has shown a recurrence rate or reoperation for DIE persistence of 3.9% in the conservative management group and 0% in the ureteral reimplantation group [
      • Cavaco-Gomes J.
      • Martinho M.
      • Gilabert-Aguilar J.
      • Gilabert-Estelles J.
      Laparoscopic management of ureteral endometriosis: a systematic review.
      ].
      Fedele et al [
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bergamini V.
      • Berlanda N.
      • Carmignani L.
      Long-term follow-up after conservative surgery for bladder endometriosis.
      ] have evaluated the risk factor for recurrence of bladder endometriosis and have found the extent of surgical excision to be impactful. When the resection included both the bladder lesion and the 0.5- to 1-cm-deep portion of the adjacent myometrium, recurrence was less frequent compared with the removal of the bladder lesion only (7% vs 37% for symptom recurrence) [
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bergamini V.
      • Berlanda N.
      • Carmignani L.
      Long-term follow-up after conservative surgery for bladder endometriosis.
      ].

       Recurrence and Risk Factors of Relapse for Diaphragmatic and Thoracic Endometriosis

      Recurrence of thoracic endometriosis lesions or catamenial pneumothorax after surgery were noted in 12 studies [
      • Ciriaco P.
      • Negri G.
      • Libretti L.
      • et al.
      Surgical treatment of catamenial pneumothorax: a single centre experience.
      ,
      • Korom S.
      • Canyurt H.
      • Missbach A.
      • et al.
      Catamenial pneumothorax revisited: clinical approach and systematic review of the literature.
      ,
      • Alifano M.
      • Jablonski C.
      • Kadiri H.
      • et al.
      Catamenial and noncatamenial, endometriosis-related or nonendometriosis-related pneumothorax referred for surgery.
      ,
      • Attaran S.
      • Bille A.
      • Karenovics W.
      • Lang-Lazdunski L.
      Videothoracoscopic repair of diaphragm and pleurectomy/abrasion in patients with catamenial pneumothorax: a 9-year experience.
      ,
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      ,
      • Visouli A.N.
      • Darwiche K.
      • Mpakas A.
      • et al.
      Catamenial pneumothorax: a rare entity? Report of 5 cases and review of the literature.
      ,
      • Haga T.
      • Kurihara M.
      • Kataoka H.
      • Ebana H.
      Clinical-pathological findings of catamenial pneumothorax: comparison between recurrent cases and non-recurrent cases.
      ,
      • Chiantera V.
      • Dessole M.
      • Petrillo M.
      • et al.
      Laparoscopic en bloc right diaphragmatic peritonectomy for diaphragmatic endometriosis according to the Sugarbaker technique.
      ,
      • Nezhat C.
      • Main J.
      • Paka C.
      • Nezhat A.
      • Beyqui R.E.
      Multidisciplinary treatment for thoracic and abdominopelvic endometriosis.
      ,
      • Fukuoka M.
      • Kurihara M.
      • Haga T.
      • et al.
      Clinical characteristics of catamenial and non-catamenial thoracic endometriosis-related pneumothorax.
      ,
      • Alifano M.
      • Legras A.
      • Rousset-Jablonski C.
      • et al.
      Pneumothorax recurrence after surgery in women: clinicopathologic characteristics and management.
      ,
      • Rousset-Jablonski C.
      • Alifano M.
      • Plu-Bureau G.
      • et al.
      Catamenial pneumothorax and endometriosis-related pneumothorax.
      ]. The rate of pneumothorax recurrence was widely heterogeneous, varying between 0% and 40% [
      • Ciriaco P.
      • Negri G.
      • Libretti L.
      • et al.
      Surgical treatment of catamenial pneumothorax: a single centre experience.
      ,
      • Alifano M.
      • Jablonski C.
      • Kadiri H.
      • et al.
      Catamenial and noncatamenial, endometriosis-related or nonendometriosis-related pneumothorax referred for surgery.
      ,
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      ,
      • Haga T.
      • Kurihara M.
      • Kataoka H.
      • Ebana H.
      Clinical-pathological findings of catamenial pneumothorax: comparison between recurrent cases and non-recurrent cases.
      ]. According to Korom et al [
      • Korom S.
      • Canyurt H.
      • Missbach A.
      • et al.
      Catamenial pneumothorax revisited: clinical approach and systematic review of the literature.
      ], the mean time to recurrence is 24 months after diaphragm removal with or without pleurodesis and 61 months after pleurodesis. These results appear to not be associated with the extent of the procedure but rather with the presence of diaphragmatic defects on the increased rate of recurrence [
      • Visouli A.N.
      • Darwiche K.
      • Mpakas A.
      • et al.
      Catamenial pneumothorax: a rare entity? Report of 5 cases and review of the literature.
      ]. According to Ceccaroni et al [
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      ], laparoscopy is another possible approach for the treatment of diaphragmatic endometriosis and gives the opportunity to adequately investigate the diaphragmatic surfaces with or without completely mobilizing the liver.

      Discussion

      The challenge in evaluating the literature stemmed from the inconsistent definitions of DIE recurrence depending on author determination, varying clinical examination [
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ,
      • Donnez J.
      • Squifflet J.
      Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules.
      ,
      • Kavallaris A.
      • Chalvatzas N.
      • Hornemann A.
      • Banz C.
      • Diedrich K.
      • Agic A.
      94 months follow-up after laparoscopic assisted vaginal resection of septum rectovaginal and rectosigmoid in women with deep infiltrating endometriosis.
      ], and histologic variation in proving endometriosis recurrence [
      • Meuleman C.
      • Tomassetti C.
      • Wolthuis A.
      • et al.
      Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study.
      ,
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ,
      • 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.
      ]. Recurrence is higher if the follow-up is longer [
      • Guo S.W.
      Recurrence of endometriosis and its control.
      ,
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ]. Two risk factors were identified as risk factors for recurrence: an elevated BMI [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ] and a younger age at primary surgery [
      • Vignali M.
      • Bianchi S.
      • Candiani M.
      • Spadaccini G.
      • Oggioni G.
      • Busacca M.
      Surgical treatment of deep endometriosis and risk of recurrence.
      ,
      • Busacca M.
      • Chiaffarino F.
      • Candiani M.
      • et al.
      Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis.
      ,
      • Fedele L.
      • Bianchi S.
      • Zanconato G.
      • Bettoni G.
      • Gutsch F.
      Long-term follow-up after conservative surgery for rectovaginal endometriosis.
      ,
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ] although a universal cutoff age was not noted. Moreover, we believe that another risk linked to younger age could be the rejection of postoperative hormonal therapy because of the wish for pregnancy.
      The higher risk of recurrence for obese or overweight women is probably because of the presence of more adipose tissue and, consequently, a higher output of estrogen produced by the aromatase activity in those tissues [
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence.
      ]. In addition, although the recurrence of superficial peritoneal endometriosis could be different than that of DIE, Taylor and Williams [
      • Taylor E.
      • Williams C.
      Surgical treatment of endometriosis: location and patterns of disease at reoperation.
      ] reported that recurrence is more likely to be related to the cluster of disease from the original area of involvement and reflects that incomplete excision at the initial surgery is an important risk factor for recurrence.
      There is some evidence that positive bowel surgical resection margins are associated with a higher risk of recurrence [
      • Nirgianakis K.
      • McKinnon B.
      • Imboden S.
      • Knabben L.
      • Gloor B.
      • Mueller M.D.
      Laparoscopic management of bowel endometriosis: resection margins as a predictor of recurrence.
      ] although several authors were unable to demonstrate a clear correlation [
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ]. Available data concerning the microscopic satellite lesions near the resection margins could explain the inconsistent results regarding positive resection margins and risk of recurrence [
      • Koh C.E.
      • Juszczyk K.
      • Cooper M.J.
      • Solomon M.J.
      Management of deeply infiltrating endometriosis involving the rectum.
      ,
      • Mabrouk M.
      • Spagnolo E.
      • Raimondo D.
      • et al.
      Segmental bowel resection for colorectal endometriosis: is there a correlation between histological pattern and clinical outcomes?.
      ,
      • Roman H.
      • Hennetier C.
      • Darwish B.
      • et al.
      Bowel occult microscopic endometriosis in resection margins in deep colorectal endometriosis specimens has no impact on short-term postoperative outcomes.
      ].
      In a recent article, Darwish and Roman [
      • Darwish B.
      • Roman H.
      Surgical treatment of deep infiltrating rectal endometriosis: in favor of less aggressive surgery.
      ] have compared the evolution of oncologic conservative surgery in the oncologic field with that of radical DIE nerve-sparing or fertility-sparing surgery. Actually, there are no available data to recommend a conservative approach for bowel endometriosis. The debate concerning the best surgical approach in the treatment of DIE of the bowel is far from over, warranting the need for prospective follow-up studies with large sample sizes and clear definitions of DIE recurrence to compare the recurrence rate of different surgical approaches.
      Concerning the recurrence of urinary tract endometriosis, in particular for ureteral endometriosis, the more significant risk factor seems to be the extent of disease excision from the ureter [
      • Cavaco-Gomes J.
      • Martinho M.
      • Gilabert-Aguilar J.
      • Gilabert-Estelles J.
      Laparoscopic management of ureteral endometriosis: a systematic review.
      ]. Despite the approach to spare the ureter whenever possible, ureteral endometriosis might be an intrinsic lesion [
      • Chapron C.
      • Chiodo I.
      • Leconte M.
      • et al.
      Severe ureteral endometriosis: the intrinsic type is not so rare after complete surgical exeresis of deep endometriotic lesions.
      ] that cannot be treated with ureterolysis [
      • Mereu L.
      • Gagliardi M.L.
      • Clarizia R.
      • Mainardi P.
      • Landi S.
      • Minelli L.
      Laparoscopic management of ureteral endometriosis in case of moderate-severe hydroureteronephrosis.
      ]. Because it is impossible to differentiate intrinsic and extrinsic ureteral endometriosis preoperatively, several studies note that the indication for ureterocystoneostomy should be moderate/severe hydronephrosis because of ureteral stenosis [
      • Mereu L.
      • Gagliardi M.L.
      • Clarizia R.
      • Mainardi P.
      • Landi S.
      • Minelli L.
      Laparoscopic management of ureteral endometriosis in case of moderate-severe hydroureteronephrosis.
      ,
      • Miranda-Mendoza I.
      • Kovoor E.
      • Nassif J.
      • Ferreira H.
      • Wattiez A.
      Laparoscopic surgery for severe ureteric endometriosis.
      ]. The conservative approach may be used as the initial treatment option in most patients with ureteral endometriosis, but for some patients with a suspected ureteral intrinsic lesion and in case of failure of ureterolysis, ureteral resection and reanastomosis/reimplantation may be best.
      The relation between the recurrence rate of bladder endometriosis and the depth of surgical resection of the adjacent myometrium was postulated by Donnez et al [
      • Donnez J.
      • Spada F.
      • Squifflet J.
      • Nisolle M.
      Bladder endometriosis must be considered as bladder adenomyosis.
      ] in 2000 because of the hypothesis that bladder endometriosis is an adenomyotic nodule arising from the myometrium and spreading to the bladder. In the case of bladder endometriosis, the option of radical surgery to reduce DIE recurrence should be balanced with the risk of myometrial lesions, especially for women who wish to preserve fertility. The varying data concerning recurrence of diaphragmatic endometriosis may stem from the small sample size, the follow-up period varying between 3 and 52 months [
      • Ciriaco P.
      • Negri G.
      • Libretti L.
      • et al.
      Surgical treatment of catamenial pneumothorax: a single centre experience.
      ,
      • Ceccaroni M.
      • Roviglione G.
      • Giampaolino P.
      • et al.
      Laparoscopic surgical treatment of diaphragmatic endometriosis: a 7-year single-institution retrospective review.
      ], the surgical techniques (pleurodesis or surgical resection), and the postoperative hormonal treatment.
      Standardized reporting of surgical treatment for deep endometriosis, as suggested in the Consensus On Recording Deep Endometriosis Surgery (CORDES) statement [
      • Vanhie A.
      • Meuleman C.
      • Tomassetti C.
      • et al.
      Consensus on recording deep endometriosis surgery: the CORDES statement.
      ], may prevent bias in data collection as much possible. The deep endometriosis surgical sheet proposed by Vanhie et al [
      • Vanhie A.
      • Meuleman C.
      • Tomassetti C.
      • et al.
      Consensus on recording deep endometriosis surgery: the CORDES statement.
      ] could be a useful tool for physicians to use the same surgical language and similar rigorous protocols to compare the results of different studies of DIE.

      Conclusion

      Younger age and increased BMI appear to be risk factors for DIE recurrence. Prospective, large studies are warranted to establish the definitions of DIE and recurrence, attempt various surgical approaches, and determine the most effective medical and surgical treatment of DIE with long-term follow-up. Considering that DIE is a benign disease that is very often responsive to medical treatment, correct timing for the first surgery and the radical nature of that surgery implies a progression of standardized essential key steps in the management of the disease to reduce recurrence and reoperations as well as anatomic damage while preserving fertility.

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