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Review| Volume 35, ISSUE 4, P435-444, October 2017

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‘Money for nothing’. The role of robotic-assisted laparoscopy for the treatment of endometriosis

  • Nicola Berlanda
    Correspondence
    Corresponding author.
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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  • Maria Pina Frattaruolo
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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  • Giorgio Aimi
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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  • Marilena Farella
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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  • Giussy Barbara
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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  • Laura Buggio
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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  • Paolo Vercellini
    Affiliations
    Unità Operativa Dipartimentale Ginecologia Chirurgica e Endometriosi, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca' Granda Ospedale Maggiore Policlinico, Università degli Studi di Milano, Italy
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      Highlights

      • Robotic treatment of endometriosis does not outweigh standard laparoscopy.
      • Severe endometriosis, peritoneal disease and obesity are not indications for robotic surgery.
      • Robotic surgery for endometriosis should be performed within controlled studies.

      Abstract

      Despite higher costs for robotic-assisted laparoscopy (RAL) than standard laparoscopy (SL), RAL treatment of endometriosis is performed without established indications. PubMed/MEDLINE was searched for ‘robotic surgery’ and ‘endometriosis’ or ‘gynaecological benign disease’ from January 2000 to December 2016. Full-length studies in English reporting original data were considered. Among 178 articles retrieved, 17 were eligible: 11 non-comparative (RAL only) and six comparative (RAL versus SL). Non-comparative studies included 445 patients. Mean operating time, blood loss and hospital stay were 226 min, 168 ml and 4 days. Major complications and laparotomy conversions were 3.1% and 1.3%. Eight studies reported pain improvement at 15-month follow-up. Comparative studies were all retrospective; 749 women underwent RAL and 705 SL. Operating time was longer for RAL in five studies. Major complications and laparotomy conversions for RAL and SL were 1.5% versus 0.3% and 0.3% versus 0.5%. One study reported pain reduction for RAL at 6-month follow-up. RAL treatment of endometriosis did not provide benefits over SL, overall and among subgroups of women with severe endometriosis, peritoneal endometriosis and obesity. Available evidence is low-quality, and data regarding long-term pain relief and pregnancy rates are lacking. RAL treatment of endometriosis should be performed only within controlled studies.

      Graphical Abstract

      Keywords

      Introduction

      During the last decades, laparoscopic surgery has been accepted as the technique of choice for the treatment of endometriosis, because it provides long-term outcomes comparable to those achieved by laparotomy, with the established advantages of a minimally invasive technique, including better visualization, shorter hospital stay, faster recovery and better cosmetic results (
      • Adamson G.D.
      • Subak L.L.
      • Pasta D.J.
      • Hurd S.J.
      • von Franque O.
      • Rodriguez B.D.
      Comparison of CO2 laser laparoscopy with laparotomy for treatment of endometriomata.
      ,
      • Daraï E.
      • Dubernard G.
      • Coutant C.
      • Frey C.
      • Rouzier R.
      • Ballester M.
      Randomized trial of laparoscopically assisted versus open colorectal resection for endometriosis: morbidity, symptoms, quality of life, and fertility.
      ,
      • Luciano A.A.
      • Lowney J.
      • Jacobs S.L.
      Endoscopic treatment of endometriosis-associated infertility. Therapeutic, economic and social benefits.
      ,
      • Vercellini P.
      • Aimi G.
      • Busacca M.
      • Apolone G.
      • Uglietti A.
      • Crosignani P.G.
      Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial.
      ).
      More recently, robotic-assisted laparoscopy (RAL) has become available, which is an implementation of standard laparoscopy (SL). The technical advantages and disadvantages of RAL compared with SL are reported in Table 1. Briefly, the main advantages of RAL over SL include the availability of articulating instruments capable of a range of movements comparable to those of the human wrist, and the possibility of reducing or eliminating the surgeon's tremor, whereas the major disadvantage of RAL is a reduced overall versatility compared with SL.
      Table 1Potential advantages and drawbacks of robotic-assisted laparoscopy for the surgical treatment of endometriosis.
      AdvantagesDrawbacks
      Higher degree of freedom in the robotic instrument and reduction in tremor interferenceCost of implementation and maintenance
      Three-dimensional visionInability to move the surgical table once the robot arms are attached and inability to operate in different quadrants at the same time
      Motion scalingLack of tactile feedback to the surgeon
      Ambidextrous capabilityTime required to dock and separate the robotic cart from the patient
      Better ergonomics (the ability of the surgeon to sit)Large sized ports (8 mm)
      Telesurgery
      When comparing RAL and SL, the issue of costs is also of paramount importance, as the former technique is more expensive than the latter one. Expenses for RAL are related to the cost of around 2 million euros for the robot itself, the annual maintenance fee of around 160,000 euros and the cost of 1200 to 2000 euros of each robotic instrument, which must be mandatorily replaced after 10 surgical procedures (
      • Paul S.
      • McCulloch P.
      • Sedrakyan A.
      Robotic surgery: revisiting ‘no innovation without evaluation’.
      ,
      • Trehan A.
      • Dunn T.J.
      The robotic surgery monopoly is a poor deal.
      ). Consequently, in order to justify a widespread use of a more expensive technique such as RAL, this technique has to prove advantageous over SL in terms of better outcomes for the patients.
      Although several studies have reported the use of RAL for the treatment of endometriosis, the specific clinical indications for RAL rather than SL, and the practical advantages for the patients of the former choice, are not yet established. This study sought to perform a review of the available evidence in order to possibly clarify the issue of whether women with endometriosis, or specific subgroups of patients with the disease, may benefit from RAL compared with SL.

      Materials and methods

      The present review was conducted according to the PRISMA guidelines for systematic reviews (
      • Moher D.
      • Liberati A.
      • Tetzlaff J.
      • Altman D.G.
      PRISMA Group
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      ). The quality of evidence of the selected studies was further assessed using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) criteria (
      • Guyatt G.H.
      • Oxman A.D.
      • Vist G.E.
      • Kunz R.
      • Falck-Ytter Y.
      • Alonso-Coello P.
      • Schünemann H.J.
      GRADE Working Group
      GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.
      ). As only published data were used, the present study was exempt from Institutional Review Board approval.

      Sources

      This review was restricted to published research articles that reported the use of RAL for the treatment of endometriosis or specific subgroups of patients with the disease. A PubMed/MEDLINE search was performed of papers published between January 2000 and December 2016, using the terms ‘robotic surgery’ combined with ‘endometriosis’ or ‘gynaecological benign disease’. Only studies published as full-length in English and reporting original data were included. All pertinent articles and review articles were retrieved and their bibliographies were systematically examined to identify any other relevant publication that could be included. Only published data were used and no attempt was made to identify unpublished studies.

      Study selection and data extraction

      Three authors (MPF, MF and LB) conducted an independent screening of all titles and abstracts retrieved from peer-reviewed journals to exclude irrelevant or duplicate citations. Data presented exclusively as abstracts in national and international meetings, or case reports or articles including less than five women or review articles that did not include original data were excluded. When more than one publication based on the same study population and data was found, only the one with most detailed information, or published most recently was included.
      Two authors (MPF and MF) designed a data extraction form that was applied to each paper to independently extract data regarding authors, year of publication, country, study design, number of recruited subjects, age of participants, body mass index (BMI), previous surgery, type of surgical treatment, operating time, blood loss, hospital stay, length of follow-up, major complications, postoperative pain and pregnancy rate. Studies were categorized based on research design as prospective, retrospective, comparative and non-comparative. Correction or resolution of any discrepancies between reviewers was reached by consensus after discussion or arbitration by a third reviewer (NB).

      Results

      The flow diagram of the literature search results is shown in Figure 1. Because almost all studies included in this review are observational studies, the final assessment according to the GRADE criteria (
      • Guyatt G.H.
      • Oxman A.D.
      • Vist G.E.
      • Kunz R.
      • Falck-Ytter Y.
      • Alonso-Coello P.
      • Schünemann H.J.
      GRADE Working Group
      GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.
      ), was a low level of quality. One-hundred and forty-three articles were identified by database search as potentially relevant, and other 35 citations were identified from reference lists. Among the 178 articles, 156 were excluded after evaluation of the abstract and full text because they did not satisfy the inclusion criteria, and 22 articles were assessed for eligibility. Another five publications were excluded from the current review. One study (
      • Vitobello D.
      • Fattizzi N.
      • Santoro G.
      • Rosati R.
      • Baldazzi G.
      • Bulletti C.
      • Palmara V.
      Robotic surgery and standard laparoscopy: a surgical hybrid technique for use in colorectal endometriosis.
      ) was excluded because enrolled patients were most likely included in a larger, more recent study from the same group (
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      ). Two studies were excluded because the number of patients with endometriosis was <5 (
      • Tan S.J.
      • Lin C.K.
      • Fu P.T.
      • Liu Y.L.
      • Sun C.C.
      • Chang C.C.
      • Yu M.H.
      • Lai H.C.
      Robotic surgery in complicated gynecologic diseases: experience of Tri-Service General Hospital in Taiwan.
      ,
      • Williams S.K.
      • Leveillee R.J.
      Expanding the horizons: robot-assisted reconstructive surgery of the distal ureter.
      ). Two studies were excluded because it was not possible to separate surgical data relative specifically to the treatment of endometriosis from those relative to other gynaecological conditions (
      • Scheib S.A.
      • Fader A.N.
      Gynecologic robotic laparoendoscopic single-site surgery: prospective analysis of feasibility, safety, and technique.
      ,
      • Smorgick N.
      • DeLancey J.
      • Patzkowsky K.
      • Advincula A.
      • Song A.
      • As-Sanie S.
      Risk factors for postoperative urinary retention after laparoscopic and robotic hysterectomy for benign indications.
      ). Complete author agreement regarding included and excluded studies was achieved.
      Figure 1
      Figure 1Flowchart of the study selection process.
      Seventeen studies were eventually selected. Among them, 11 studies were non-comparative, i.e. included women operated with RAL only (
      • Abo C.
      • Roman H.
      • Bridoux V.
      • Huet E.
      • Tuech J.J.
      • Resch B.
      • Stochino E.
      • Marpeau L.
      • Darwish B.
      Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience.
      ,
      • Bedaiwy M.A.
      • Rahman M.Y.
      • Chapman M.
      • Frasure H.
      • Mahajan S.
      • von Gruenigen V.E.
      • Hurd W.
      • Zanotti K.
      Robotic-assisted hysterectomy for the management of severe endometriosis: a retrospective review of short-term surgical outcomes.
      ,
      • Brudie L.A.
      • Gaia G.
      • Ahmad S.
      • Finkler N.J.
      • Bigsby 4th., G.E.
      • Ghurani G.B.
      • Kendrick 4th., J.E.
      • Rakowski J.A.
      • Groton J.H.
      • Holloway R.W.
      Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery.
      ,
      • Collinet P.
      • Leguevaque P.
      • Neme R.M.
      • Cela V.
      • Barton-Smith P.
      • Hébert T.
      • Hanssens S.
      • Nishi H.
      • Nisolle M.
      Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study.
      ,
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      ,
      • Lim P.C.
      • Kang E.
      • Park do H.
      Robot-assisted total intracorporeal low anterior resection with primary anastomosis and radical dissection for treatment of stage IV endometriosis with bowel involvement: morbidity and its outcome.
      ,
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      ,
      • Neme R.M.
      • Schraibman V.
      • Okazaki S.
      • Maccapani G.
      • Chen W.J.
      • Domit C.D.
      • Kaufmann O.G.
      • Advincula A.P.
      Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.
      ,
      • Pellegrino A.
      • Damiani G.R.
      • Trio C.
      • Faccioli P.
      • Croce P.
      • Tagliabue F.
      • Dainese E.
      Robotic shaving technique in 25 patients affected by deep infiltrating endometriosis of the rectovaginal space.
      ,
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      ), whereas six studies were comparative, i.e. compared two series of women operated with RAL and SL (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ,
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ,
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ,
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ,
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ,
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ). None of these comparative studies was a randomized trial.

      Non-comparative studies

      The characteristics of the patients and the perioperative data of the non-comparative studies are reported in Table 2. Four studies were prospective (
      • Abo C.
      • Roman H.
      • Bridoux V.
      • Huet E.
      • Tuech J.J.
      • Resch B.
      • Stochino E.
      • Marpeau L.
      • Darwish B.
      Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience.
      ,
      • Lim P.C.
      • Kang E.
      • Park do H.
      Robot-assisted total intracorporeal low anterior resection with primary anastomosis and radical dissection for treatment of stage IV endometriosis with bowel involvement: morbidity and its outcome.
      ,
      • Neme R.M.
      • Schraibman V.
      • Okazaki S.
      • Maccapani G.
      • Chen W.J.
      • Domit C.D.
      • Kaufmann O.G.
      • Advincula A.P.
      Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy.
      ,
      • Pellegrino A.
      • Damiani G.R.
      • Trio C.
      • Faccioli P.
      • Croce P.
      • Tagliabue F.
      • Dainese E.
      Robotic shaving technique in 25 patients affected by deep infiltrating endometriosis of the rectovaginal space.
      ) and seven were retrospective (
      • Bedaiwy M.A.
      • Rahman M.Y.
      • Chapman M.
      • Frasure H.
      • Mahajan S.
      • von Gruenigen V.E.
      • Hurd W.
      • Zanotti K.
      Robotic-assisted hysterectomy for the management of severe endometriosis: a retrospective review of short-term surgical outcomes.
      ,
      • Brudie L.A.
      • Gaia G.
      • Ahmad S.
      • Finkler N.J.
      • Bigsby 4th., G.E.
      • Ghurani G.B.
      • Kendrick 4th., J.E.
      • Rakowski J.A.
      • Groton J.H.
      • Holloway R.W.
      Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery.
      ,
      • Collinet P.
      • Leguevaque P.
      • Neme R.M.
      • Cela V.
      • Barton-Smith P.
      • Hébert T.
      • Hanssens S.
      • Nishi H.
      • Nisolle M.
      Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study.
      ,
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      ,
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.
      ,
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      ). In total, 445 patients were evaluated, with a mean age of 39 years. The most frequent indication for RAL was deep infiltrating endometriosis: 55% of women underwent excision of bowel endometriosis, 27% ureterolysis and 8% excision of urinary tract endometriosis. Thirty-six percent of women underwent hysterectomy in addition to excision of endometriotic lesions. Mean operating time was 226 min, mean blood loss was 168 ml and mean hospital stay was 4 days. The outcome of the surgical procedures performed in non-comparative studies are reported in Table 3. The rate of major complications was 3.1%, with a 1.3% rate of conversion to laparotomy. All the eight studies that evaluated the effect of surgery on symptoms (
      • Abo C.
      • Roman H.
      • Bridoux V.
      • Huet E.
      • Tuech J.J.
      • Resch B.
      • Stochino E.
      • Marpeau L.
      • Darwish B.
      Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience.
      ,
      • Brudie L.A.
      • Gaia G.
      • Ahmad S.
      • Finkler N.J.
      • Bigsby 4th., G.E.
      • Ghurani G.B.
      • Kendrick 4th., J.E.
      • Rakowski J.A.
      • Groton J.H.
      • Holloway R.W.
      Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery.
      ,
      • Collinet P.
      • Leguevaque P.
      • Neme R.M.
      • Cela V.
      • Barton-Smith P.
      • Hébert T.
      • Hanssens S.
      • Nishi H.
      • Nisolle M.
      Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study.
      ,
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      ,
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      ,
      • Neme R.M.
      • Schraibman V.
      • Okazaki S.
      • Maccapani G.
      • Chen W.J.
      • Domit C.D.
      • Kaufmann O.G.
      • Advincula A.P.
      Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.
      ,
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      ), with a mean follow-up time of 15 months (range 2–28 months), reported either complete remission or a significant reduction of pain. The mean pregnancy rate among 73 women wishing to conceive in five studies was 38% at a mean follow-up of 16 months (range 10–24 months). One study reported that sexual wellbeing, urinary function and impact of symptoms on quality of life were slightly worsened 1 month after surgery, and became comparable to the preoperative period 1 year after surgery. Dyspareunia was the only exception, as it was significantly improved 12 months after surgery (
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      ).
      Table 2Characteristics of 11 non-comparative studies evaluating robotic-assisted laparoscopy for the treatment of moderate/severe and deeply infiltrating endometriosis. Literature data, 2011–2016.
      Author, yearNumber of patientsStudy designAge of patientsBMI of patientsPrevious surgeryBowel shaving/disc excisionBowel resectionBladder resectionUretero-lysisUNCHysterectomyOperating time (min)Blood loss (ml)LOS (days)
      (number)(mean or bmedian (years))(number (%))(mean or bmedian (range))
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.
      5R38NR4 (80)1 (20)1 (20)1 (20)1 (20)1 (20)2 (40)328 (245–475)195 (100–350)2
      • Lim P.C.
      • Kang E.
      • Park do H.
      Robot-assisted total intracorporeal low anterior resection with primary anastomosis and radical dissection for treatment of stage IV endometriosis with bowel involvement: morbidity and its outcome.
      8P47308 (100)8 (100)8 (100)8 (100)238 (157–321)425 (50–1500)6
      • Brudie L.A.
      • Gaia G.
      • Ahmad S.
      • Finkler N.J.
      • Bigsby 4th., G.E.
      • Ghurani G.B.
      • Kendrick 4th., J.E.
      • Rakowski J.A.
      • Groton J.H.
      • Holloway R.W.
      Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery.
      80R4427,523 (29)29 (36)62 (78)115 (69–161)88 (21–155)1
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      10R38b21b12/22 (55)
      In Ercoli et al. 2012, the number of patients who underwent previous surgery is not reported separately for the two subgroups.
      10 (100)280b (220–365)200b (100–350)5
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      12R38b21b12/22 (55)
      In Ercoli et al. 2012, the number of patients who underwent previous surgery is not reported separately for the two subgroups.
      12 (100)1 (8)370b (260–720)100b (50–250)8
      • Bedaiwy M.A.
      • Rahman M.Y.
      • Chapman M.
      • Frasure H.
      • Mahajan S.
      • von Gruenigen V.E.
      • Hurd W.
      • Zanotti K.
      Robotic-assisted hysterectomy for the management of severe endometriosis: a retrospective review of short-term surgical outcomes.
      43R46b289 (21)43 (100)190b (97–368)100b (20–400)1
      • Neme R.M.
      • Schraibman V.
      • Okazaki S.
      • Maccapani G.
      • Chen W.J.
      • Domit C.D.
      • Kaufmann O.G.
      • Advincula A.P.
      Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy.
      10P37235 (50)10 (100)8 (80)157 (90–190)NR3
      • Collinet P.
      • Leguevaque P.
      • Neme R.M.
      • Cela V.
      • Barton-Smith P.
      • Hébert T.
      • Hanssens S.
      • Nishi H.
      • Nisolle M.
      Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study.
      164R342439 (24)68 (41)24 (15)22 13)62 (38)1 (1)28 (17)180 (103–257)85 (5–2300)4
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      43R34b22b21 (49)23 (53)19 (44)5 (12)3 (7)200b (57–366)120b (100–1000)3
      • Pellegrino A.
      • Damiani G.R.
      • Trio C.
      • Faccioli P.
      • Croce P.
      • Tagliabue F.
      • Dainese E.
      Robotic shaving technique in 25 patients affected by deep infiltrating endometriosis of the rectovaginal space.
      25P342118 (72)25 (100)2 (8)174b (75–300)NR (0–100)3
      • Abo C.
      • Roman H.
      • Bridoux V.
      • Huet E.
      • Tuech J.J.
      • Resch B.
      • Stochino E.
      • Marpeau L.
      • Darwish B.
      Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience.
      35P3624,520 (57)28 (80)4 (11)3 (9)11 (31)2 (6)11 (31)207 (NR)NRNR
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      10R36b22b7 (70)10 (100)3 (30)280b (180–420)200 (100–400)6
      Total4453924179 (40)155 (35)88 (20)31 (7)122 (27)5 (1)159 (36)226 (57–720)168 (0–2300)4
      Data from
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      were reported separately for women who underwent bowel shaving (n = 10) and women who underwent bowel resection (n = 12).
      Values are mean or bmedian (range), or number (%).
      BMI = body mass index; LOS = length of hospital stay; NR = not reported; P = prospective; R = retrospective; UNC = uretero-neocystostomy.
      a In
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      , the number of patients who underwent previous surgery is not reported separately for the two subgroups.
      Table 3Complications and outcome of women undergoing robotic-assisted laparoscopy for advanced endometriosis in 11 non-comparative studies. Literature data, 2011–2016.
      StudyFollow up (months)Major complicationsConversion to laparotomyPostoperative pain (%)Pregnancy rate
      Percentage among women seeking pregnancy.
      (mean)number (%)(number pregnant women/women seeking pregnancy (%))
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.
      2300Pain free (100)NR
      • Lim P.C.
      • Kang E.
      • Park do H.
      Robot-assisted total intracorporeal low anterior resection with primary anastomosis and radical dissection for treatment of stage IV endometriosis with bowel involvement: morbidity and its outcome.
      NR00NRNR
      • Brudie L.A.
      • Gaia G.
      • Ahmad S.
      • Finkler N.J.
      • Bigsby 4th., G.E.
      • Ghurani G.B.
      • Kendrick 4th., J.E.
      • Rakowski J.A.
      • Groton J.H.
      • Holloway R.W.
      Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery.
      22 (2.5)
      Ureteral injury, vaginal cuff abscess requiring reoperation.
      4Significant reduction (99)NR
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      61 (4.5)
      Small bowel occlusion.
      0Significant reductionNR
      • Bedaiwy M.A.
      • Rahman M.Y.
      • Chapman M.
      • Frasure H.
      • Mahajan S.
      • von Gruenigen V.E.
      • Hurd W.
      • Zanotti K.
      Robotic-assisted hysterectomy for the management of severe endometriosis: a retrospective review of short-term surgical outcomes.
      NR1 (2.3)
      Vaginal cuff abscess.
      1NRNR
      • Neme R.M.
      • Schraibman V.
      • Okazaki S.
      • Maccapani G.
      • Chen W.J.
      • Domit C.D.
      • Kaufmann O.G.
      • Advincula A.P.
      Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy.
      1200Pain free (100)4/6 (67)
      • Collinet P.
      • Leguevaque P.
      • Neme R.M.
      • Cela V.
      • Barton-Smith P.
      • Hébert T.
      • Hanssens S.
      • Nishi H.
      • Nisolle M.
      Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study.
      106 (3.7)
      Two ureteral fistula, 2 bowel injury, 1 ureter bladder anastomotic leak, 1 prolonged urinary catheterization.
      1Pain free (88)11/39 (28)
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      282 (4.7%)
      Anastomotic leakage, hemoperitoneum requiring reoperation.
      0NRNR
      • Pellegrino A.
      • Damiani G.R.
      • Trio C.
      • Faccioli P.
      • Croce P.
      • Tagliabue F.
      • Dainese E.
      Robotic shaving technique in 25 patients affected by deep infiltrating endometriosis of the rectovaginal space.
      221 (4%)
      Opening of rectal wall during shaving.
      0Significant reduction (75 −100)4/15 (27)
      • Abo C.
      • Roman H.
      • Bridoux V.
      • Huet E.
      • Tuech J.J.
      • Resch B.
      • Stochino E.
      • Marpeau L.
      • Darwish B.
      Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience.
      241 (2.9)
      Ureteral necrosis and fistula.
      0Significant reduction8/9 (89)
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      1200Significant reduction1/4 (25)
      Total15 (2 −28)14 (3.1)6 (1.3)28/73 (38)
      NR = not reported; Values are mean (range), or number (%).
      a Percentage among women seeking pregnancy.
      b Ureteral injury, vaginal cuff abscess requiring reoperation.
      c Small bowel occlusion.
      d Vaginal cuff abscess.
      e Two ureteral fistula, 2 bowel injury, 1 ureter bladder anastomotic leak, 1 prolonged urinary catheterization.
      f Anastomotic leakage, hemoperitoneum requiring reoperation.
      g Opening of rectal wall during shaving.
      h Ureteral necrosis and fistula.

      Comparative studies

      All studies were retrospective and included a total of 1454 women, 749 undergoing RAL and 705 SL. One study (
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ), included women who presented with pelvic pain suggestive of endometriosis; among them, endometriosis was eventually diagnosed in 78% of women in the RAL group and 71% of women in the SL group. The prevalence of advanced endometriosis, i.e. stage III or IV according to the revised American Society for Reproductive Medicine classification (
      • American Society for Reproductive Medicine (ASRM)
      Revised American Society for Reproductive Medicine classification of endometriosis: 1996.
      ), was 23% in one study (
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ), 48% in another study (
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ) and 100% in the remaining 4 studies. In all studies, the decision of performing RAL or SL was made upon preference of the surgeon and availability of the robot. A preoperative diagnosis of high-complexity cases favoured a RAL approach in two studies (
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ,
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), and obesity favoured a RAL approach in one study (
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ).
      In one study, patients in the two groups were not comparable because of the higher number of procedures and more radical operations in the robotic group (
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ). In this study, women undergoing hysterectomy, colorectal shaving or disk excision, small bowel resection or ureteral surgery in the RAL group versus the SL group were 50% versus 27%, 2.7% versus 0.6%, 1.2% versus 1.2% and 5.4% versus 35%, respectively (
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ). In each of the remaining five studies, the rate of hysterectomy in the RAL versus the SL group was 25% versus 21% (
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), 0% versus 0% (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ,
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ,
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ) and not reported (
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ), respectively. In one study (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ), all patients underwent colorectal resection.
      The characteristics of the patients and the perioperative data of the six comparative studies are reported in Table 4. In one study (
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), the median BMI in the RAL group was significantly higher than SL group.
      Table 4Characteristics of retrospective cohort studies comparing robotic-assisted and standard laparoscopic surgery for the treatment of endometriosis. Literature data, 2010–2015.
      Author, yearPatientsAgeBMIPrevious surgeryOperating time (minutes)Blood loss (ml)Hospital stay (days)
      (number)(mean or bmedian (years))(mean or bmedian)number (%)(mean or bmedian (range))
      RALSLRALSLRALSLRALSLRALSLRALSLRALSL
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      40383533242318 (45)15 (39)191 (135–295)159 (85–320)
      P < 0.05.
      60 (0–350)65 (0–500)NRNR
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      18010033292827124 (69)65 (65)77722925NRNR
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      194637NR21NRNRNR370b (250–720)180b (80–220)
      P < 0.05.
      150 (50–350)320 (100–650)5 (3–8)NR
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      328639b38b27b24
      P < 0.05.
      22 (69)53 (62)250b (176–328)173b (123–237)
      P < 0.05.
      100b (50–200)100b (50–200)11
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      33116240382626NRNR139 (40–531)113 (28–347)
      P < 0.05.
      92 (10–2500)82 (10–700)1.10.7
      P < 0.05.
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      14727330b31b232335 (24)107 (39)196135
      P < 0.05.
      4025>11
      P < 0.05.
      Total74970536342525199 (50)240 (48)204 (40–720)139 (28–347)79103
      Data are mean or bmedian (range) or number (%).
      BMI = body mass index; NR = not reported; RAL = robotic-assisted laparoscopy; SL = standard laparoscopy.
      a P < 0.05.
      Operating time was significantly longer in the RAL group compared with the SL group in five studies (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ,
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ,
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ,
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ,
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), and comparable between RAL and SL groups in one study (
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ). However, in one study, the longer operating time was explained by the higher number of procedures and more radical operations in the RAL group. In this study, multivariate analysis showed that RAL was actually associated with a 16% reduction in operating time compared with SL (
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ). In another study (
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), when operating times were correlated to patients' BMI, a longer operating time for RAL compared with SL was observed only for obese patients with a BMI ≥30 kg/m2, whereas operating time was comparable between the two groups among normal weight and overweight patients.
      Hospital stay was significantly longer in the RAL group in one study (
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ). In another study, hospital stay was longer in the RAL group at univariate analysis, but comparable between RAL and SL at multivariate analysis (
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ). Hospital stay was comparable between RAL and SL groups in two studies (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ,
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), although in one of these studies (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ) the data for the SL group were not reported.
      No study has reported a significant difference in blood loss between RAL and SL.
      Intra- and post-operative complications and post-operative follow-up of the comparative studies are reported in Table 5. The rate of major complications was 1.5% in the RAL group and 0.3% in the SL group and the rate of conversion to laparotomy was 0.3% in the RAL group and 0.5% in the SL group. In four studies, follow-up time was 42 days or less (
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ,
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      ,
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ,
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ), in one study follow up was not reported (
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ). In one study, a 6-month follow up evaluation was reported only for the RAL group, with a significant reduction of pain symptoms compared with pre-operative assessment and a pregnancy rate of 2/19 (10%) (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ).
      Table 5Operative and postoperative findings of retrospective cohort studies comparing robotic-assisted and standard laparoscopic surgery for the treatment of endometriosis. Literature data, 2010–2015.
      Author, yearPatientsFollow up (days)Major complicationsConversion to laparotomy
      (number)(mean or range)(number (%))
      RALSLRALSLRALSLRALSL
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      403828–4228 − 420000
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      18010014141 (1)
      Intraoperative inadvertent cystotomy.
      000
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      1946180NR2 (11)
      Two rectovaginal fistulas.
      NR01 (2)
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      328630302 (6)
      Bowel perforation, gastrointestinal fistula.
      1 (1)
      Gastrointestinal fistula.
      00
      • Magrina J.F.
      • Espada M.
      • Kho R.M.
      • Cetta R.
      • Chang Y.H.
      • Magtibay P.M.
      Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors.
      33116242426 (2)
      One ureteral peritoneal leak, two pelvic abscesses, two partial small bowel obstructions, two intraoperative (one inadvertent sigmoid enterotomy and one inadvertent cystotomy).
      1 (1)
      One ureteral peritoneal leak, two pelvic abscesses, two partial small bowel obstructions, two intraoperative (one inadvertent sigmoid enterotomy and one inadvertent cystotomy).
      2 (1)1 (1)
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      147273NRNR00NRNR
      Total749705603111 (1.5)2 (0.3)2 (0.3)2 (0.5)
      Data are number (%).
      NR = not reported; RAL = robotic-assisted laparoscopy; SL = standard laparoscopy.
      a Intraoperative inadvertent cystotomy.
      b Two rectovaginal fistulas.
      c Bowel perforation, gastrointestinal fistula.
      d Gastrointestinal fistula.
      e One ureteral peritoneal leak, two pelvic abscesses, two partial small bowel obstructions, two intraoperative (one inadvertent sigmoid enterotomy and one inadvertent cystotomy).

      Discussion

      Available data from non-comparative series of women that were operated using RAL, show that this treatment of endometriosis is feasible and safe. These non-comparative studies reported a low rate of complications and a significant reduction of pain at a mean follow-up of 15 months (
      • Abo C.
      • Roman H.
      • Bridoux V.
      • Huet E.
      • Tuech J.J.
      • Resch B.
      • Stochino E.
      • Marpeau L.
      • Darwish B.
      Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience.
      ,
      • Brudie L.A.
      • Gaia G.
      • Ahmad S.
      • Finkler N.J.
      • Bigsby 4th., G.E.
      • Ghurani G.B.
      • Kendrick 4th., J.E.
      • Rakowski J.A.
      • Groton J.H.
      • Holloway R.W.
      Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery.
      ,
      • Collinet P.
      • Leguevaque P.
      • Neme R.M.
      • Cela V.
      • Barton-Smith P.
      • Hébert T.
      • Hanssens S.
      • Nishi H.
      • Nisolle M.
      Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study.
      ,
      • Ercoli A.
      • D'Asta M.
      • Fagotti A.
      • Fanfani F.
      • Romano F.
      • Baldazzi G.
      • Salerno M.G.
      • Scambia G.
      Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results.
      ,
      • Morelli L.
      • Perutelli A.
      • Palmeri M.
      • Guadagni S.
      • Mariniello M.D.
      • Di Franco G.
      • Cela V.
      • Brundu B.
      • Salerno M.G.
      • Di Candio G.
      • Mosca F.
      Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes.
      ,
      • Neme R.M.
      • Schraibman V.
      • Okazaki S.
      • Maccapani G.
      • Chen W.J.
      • Domit C.D.
      • Kaufmann O.G.
      • Advincula A.P.
      Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy.
      ,
      • Nezhat C.
      • Hajhosseini B.
      • King L.P.
      Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.
      ,
      • Siesto G.
      • Ieda N.
      • Rosati R.
      • Vitobello D.
      Robotic surgery for deep endometriosis: a paradigm shift.
      ). The surgical procedures successfully performed by RAL include radical treatment of the most severe, surgically demanding and painful (
      • Vercellini P.
      Endometriosis: what a pain it is.
      ) form of the disease, which is deeply infiltrating endometriosis involving the bowel or the urinary tract. Although these results appear encouraging, comparative studies, including women operated using RAL and women operated using SL by the same surgical team, did not show any substantial advantage of the former over the latter technique. In particular, the only statistically significant differences were in favour of SL, with a reduced operating time in three studies (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ,
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ,
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ) and a reduced hospital stay in one study (
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ). However, comparative studies were all retrospective and they lack an adequate follow-up. Because in these studies the comparison between RAL and SL has been limited to perioperative outcomes, by no means has it been possible to draw any conclusion about the most important outcomes such as long-term relief of pain, pregnancy rates in infertile women and variation in health-related quality of life. Only adequately designed randomized trials comparing RAL and SL for the treatment of endometriosis would disentangle these issues.
      Recently, a review and meta-analysis on the robotic treatment of advanced endometriosis has been published, which concluded that RAL required a higher mean operating time than SL, with no significant differences between the two groups in blood loss, complications and hospital stay (
      • Chen S.H.
      • Li Z.A.
      • Du X.P.
      Robot-assisted versus conventional laparoscopic surgery in the treatment of advanced stage endometriosis: a meta-analysis.
      ). However, the present review was performed because it was found that a few more papers could be included. In fact, among the four studies considered in the review by
      • Chen S.H.
      • Li Z.A.
      • Du X.P.
      Robot-assisted versus conventional laparoscopic surgery in the treatment of advanced stage endometriosis: a meta-analysis.
      , one is a retrospective study that has also been included (
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ), and the remaining studies are three abstracts, all from the same principal investigator (
      • Chu C.M.
      • Chang-Jackson S.C.
      • Nezhat F.R.
      Retrospective study assessing laparoscopic versus robotic assisted laparoscopic treatment of severe endometriosis.
      ,
      • Sirota I.
      • Nezhat F.R.
      Comparison of outcomes for patients undergoing robot-assisted vs conventional laparoscopic surgery for advanced-stage endometriosis. Does weight make a difference?.
      ,
      • Sirota I.
      • Nezhat F.
      Robotic compared with conventional laparoscopy for treatment of severe endometriosis: comparison of outcomes.
      ), of whom a full paper has been included, which is most likely based on the same series of women included in the three abstracts (
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ). We believe that the strength of the present review is the rigorous methodology adopted. A thorough literature review was performed using an accepted modality for article search. To avoid major bias in data gathering, these were extracted from the reports by two independent observers who were not blinded. Rejected studies have been described and the reason for their exclusion and a formal evaluation of the quality of the selected studies has been performed. The limit of the present review is that the overall quality of the studies included is low. Despite this limitation, the data included in this analysis constitute the only available evidence on which to base clinical decision-making.
      With regard to the treatment of benign gynaecological conditions in general, a recent American Association of Gynecologic Laparoscopists position statement (
      • AAGL Advancing Minimally Invasive Gynecology Worldwide
      AAGL position statement: robotic-assisted laparoscopic surgery in benign gynecology.
      ) as well as a Cochrane review (
      • Liu H.
      • Lu D.
      • Wang L.
      • Shi G.
      • Song H.
      • Clarke J.
      Robotic surgery for benign gynaecological disease.
      ) suggest that robotic surgery offers no patient benefits compared with SL. Along the same line, the American College of Obstetrician and Gynecologists, as part of the Choosing Wisely® campaign, has issued the general evidence-based recommendation to ‘avoid using robotic-assisted laparoscopic surgery for benign gynecologic disease when it is feasible to use a conventional laparoscopic or vaginal approach’ (). However, such statements have been mainly based on data related to benign gynaecologic conditions other than endometriosis, without a specific focus on the endometriotic disease.
      In a recent commentary, the main argument in favour of RAL versus SL was that the use of the former technique lowers the proportion of patients having open surgery for endometrial cancer, with conversion rates that are probably halved compared with SL (
      • Ind T.
      AGAINST: robotic surgery has no advantages over conventional laparoscopic surgery.
      ). However, it has to be underscored that gynaecologists that deal with endometriosis, compared with gynaecologic oncologists, are used to being trained in standard laparoscopic surgery from the very beginning of their practice, by treating less advanced cases such as ovarian endometriotic cysts and infertility. This is confirmed by the extremely low rate of conversions to laparotomy documented in the present review. For this reason, the development of a sophisticated and expensive technique with the aim of reducing laparotomies and increasing minimally invasive procedures seems unfounded.
      Nevertheless, even among experienced laparoscopic surgeons that deal with endometriosis, the use of RAL has been advocated, especially in the subgroup of women with severe endometriosis requiring difficult surgical procedures. In these women, the benefit of RAL may be in reducing the number of procedures performed at laparotomy. Such improvement would be the logical consequence of the high degree of movements allowed by the robotic instruments, making the robotic procedure more intuitive and more similar to the open abdomen technique compared with SL. However, such argument does not seem to be substantiated by the findings of the present review, because the rate of severe endometriosis cases that are managed by SL in referral centres for the treatment of endometriosis is very high already, approaching 100%, with rates of conversion to laparotomy that are not different between RAL and SL. Of relevance here, is that the clinical characteristics of advanced endometriosis involving the bowel or the urinary tract, namely the availability of an accurate preoperative diagnosis by means of transvaginal ultrasound and magnetic resonance imaging and a limited prevalence in the overall female population, allows the optimizing of surgical treatment of the disease in referral centres by high-volume surgeons. In this scenario, standard laparoscopic surgery offers safe and cost-effective outcomes.
      Furthermore, when evaluating the perioperative performances of RAL and SL among women requiring difficult surgical procedures, there seems to be a strong argument against robotic surgery in cases when the operating field is not limited to the pelvis. In fact, in the opinion of surgeons that master both SL and RAL, in these cases ‘because the robotic camera is not interchangeable between ports and the arms are not so easily manoeuvrable in extrapelvic sites, use of the robotic platform would have been time consuming and intricate’ (
      • Nezhat C.R.
      • Stevens A.
      • Balassiano E.
      • Soliemannjad R.
      Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis.
      ). The surgical procedures in which at least one step of the operation must be performed outside of the pelvis, are typically rectosigmoid resections, which require the mobilization of the descending colon from the splenic flexure. Accordingly, most surgeons advocate in these cases a ‘hybrid’ technique, meaning that during RAL operations the robot is temporarily undocked and one or more surgical steps are performed via SL. However, a study that included only women undergoing colorectal resection for endometriosis has reported a median operating time twice as long for the RAL-hybrid technique (370 min) than for SL (180 min) (
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      ). According to available clinical data, therefore, the use of RAL instead of SL does not seem justified in women with advanced disease and requiring difficult surgical operations, especially in cases when lesions are located also outside the pelvis or colorectal resection is required.
      Another specific subgroup of women who may benefit from RAL instead of SL may be that of women suffering from pelvic pain suggestive of endometriosis. In these women, the improved three-dimensional visualization associated with robotic technology could increase the capacity of visually diagnosing peritoneal endometriosis. As a demonstration, a significantly higher rate of biopsies confirming endometriosis was found in the RAL group than in the SL group (80% versus 57%, respectively) (
      • Dulemba J.F.
      • Pelzel C.
      • Hubert H.B.
      Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis.
      ). However, we believe that this observation is of limited clinical importance. Firstly, these findings have not been confirmed by independent investigators. Moreover, 3D visualization is available for standard laparoscopy too, which may narrow the gap of visualization quality between the two techniques. Finally, there is no proof that detecting endometriosis in a higher number of peritoneal biopsies translates into practical benefits for the patient.
      Another subgroup of women with endometriosis who may benefit from RAL rather than SL is represented by obese women, as proposed by
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      . However, such a proposal does not seem to be supported by the data presented by these same authors, since they reported higher operating time for RAL compared with SL specifically and only among obese women (
      • Nezhat F.R.
      • Sirota I.
      Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis.
      ). On the contrary,
      • Cassini D.
      • Cerullo G.
      • Miccini M.
      • Manoochehri F.
      • Ercoli A.
      • Baldazzi G.
      Robotic hybrid technique in rectal surgery for deep pelvic endometriosis.
      strongly recommend a robotic hybrid procedure especially in obese patients or those with abundant visceral fat in order to avoid multiple changing in table position. Therefore, according to available evidence, there are no subgroups of women with endometriosis for whom RAL has proven advantageous over SL.
      On the basis of the limited data available we conclude that, similarly to what has been reported for benign gynaecologic diseases in general, the indications for robotic surgery for the treatment of endometriosis still need to be defined. Indeed, the hypothetical role of robotic assistance in reducing laparotomic in favour of minimally invasive surgery, seems to apply only to those surgeons that are not skilled and experienced enough to using standard laparoscopy for difficult procedures. From this standpoint, the implementation of RAL, due to the lack of evidence of any clinical advantage over SL, would be mostly a benefit for the surgeon rather than for the patient. A possible exception, although evidence is limited due to the rarity of the condition and although data were not presented in this review, is represented by large diaphragmatic endometriotic lesions. In the removal of these lesions, the superiority of robotic assistance has been advocated by skilled laparoscopic surgeons, because they found that robotic suture of the diaphragm becomes particularly easier (
      • Roman H.
      • Darwish B.
      • Provost D.
      • Baste J.M.
      Laparoscopic management of diaphragmatic endometriosis by three different approaches.
      ). Further studies are necessary to validate this recent preliminary observation.
      Another argument in favour of the implementation of robotic surgery is the supposedly shorter learning curve associated with this technique compared with SL. However, no studies have demonstrated this hypothesis in a clinical setting for any specific surgical procedure (
      • AAGL Advancing Minimally Invasive Gynecology Worldwide
      AAGL position statement: robotic-assisted laparoscopic surgery in benign gynecology.
      ). Previous studies that have investigated this issue suggest that robotic assistance for laparoscopy may reduce or eliminate the early learning curve for novices but does not provide advantages for experienced laparoscopic surgeons (
      • Chandra V.
      • Nehra D.
      • Parent R.
      • Woo R.
      • Reyes R.
      • Hernandez-Boussard T.
      • Dutta S.A.
      Comparison of laparoscopic and robotic assisted suturing performance by experts and novices.
      ,
      • Yohannes P.
      • Rotariu P.
      • Pinto P.
      • Smith A.D.
      • Lee B.R.
      Comparison of robotic versus laparoscopic skills: is there a difference in the learning curve?.
      ). A study evaluating specifically the impact of 3D vision in completing a suturing task among surgeons with different levels of expertise in laparoscopic surgery concluded that the previous observation, that tasks were completed faster with a robot system (
      • Wagner O.J.
      • Hagen M.
      • Kurmann A.
      • Horgan S.
      • Candinas D.
      • Vorburger S.A.
      Three-dimensional vision enhances task performance independently of the surgical method.
      ), may be true for novices only (
      • Park Y.S.
      • Oo A.M.
      • Son S.Y.
      • Shin D.J.
      • Jung D.H.
      • Ahn S.H.
      • Park D.J.
      • Kim H.H.
      Is a robotic system really better than the three-dimensional laparoscopic system in terms of suturing performance?: comparison among operators with different levels of experience.
      ). Again, it has to be noted that, because laparoscopic surgery is recognized as the technique of choice for the treatment of endometriosis, the laparoscopic training of young surgeons approaching the disease begins very soon in their professional life. Consequently, the additional costs associated with RAL seems currently unjustified by a possible, undefined shortening of the learning curve for the minimally invasive treatment of endometriosis.
      In the first report on the comparison between RAL and SL for endometriosis, published in 2010 (
      • Nezhat C.
      • Lewis M.
      • Kotikela S.
      • Veeraswamy A.
      • Saadat L.
      • Hajhosseini B.
      • Nezhat C.
      Robotic versus standard laparoscopy for the treatment of endometriosis.
      ), the authors recognized the limitations of RAL and advocated a future technological development in which ‘smaller, cheaper and easier to use robots are going to make this alternative form of surgery faster and more cost-effective’. Unfortunately, after more than 6 years, such expectations of technological improvement have not been realized. This may partly be explained by the fact that there is only one robotic system on the market, the da Vinci robot produced by Intuitive Surgical, Inc (Sunnyvale, California, USA). When the only past competitor Computer Motion, which developed the ZEUS robotic system, merged with Intuitive Surgical in 2003, a monopoly of Intuitive Surgical was created for the market of robotic surgery. In this monopoly condition, the financial investments undertaken by Intuitive Surgical to developing more effective and more affordable robotic systems might remain substantially lower than they would be in presence of the competitive pressure of another company.
      The da Vinci robotic system was approved by the United States Food and Drug Administration with limited clinical evidence of safety or effectiveness (
      • Paul S.
      • McCulloch P.
      • Sedrakyan A.
      Robotic surgery: revisiting ‘no innovation without evaluation’.
      ). In the absence of proof that RAL is superior to SL, many investigators simply skip this issue and try to move on to the question of how we should better adopt this new technology (
      • Steege J.F.
      • Einarsson J.I.
      Robotics in benign gynecologic surgery: where should we go?.
      ). Of relevance here, in 2014 Intuitive Surgical, Inc. has been the second leading payer to US obstetricians and gynaecologists and the leading payer to US gynaecologic oncologists, in terms of money transferred for non-research purposes, such as participation at conferences and courses, travel and lodge, meals, speaker fees and consultancies (
      • Shalowitz D.I.
      • Spillman M.A.
      • Morgan M.A.
      Interactions with industry under the Sunshine Act: an example from gynecologic oncology.
      ,
      • Tierney N.M.
      • Saenz C.
      • McHale M.
      • Ward K.
      • Plaxe S.
      Industry payments to obstetrician-gynecologists: an analysis of 2014 open payments data.
      ). Therefore, when evaluating the studies reporting the outcomes of robotic surgery, sponsorship of industry and possible conflicts of interests of authors should be taken into account. In fact, it is known that studies sponsored by industry almost always report more favourable outcomes for the experimental technique compared with independent studies (
      • Flacco M.E.
      • Manzoli L.
      • Boccia S.
      • Capasso L.
      • Aleksovska K.
      • Rosso A.
      • Scaioli G.
      • De Vito C.
      • Siliquini R.
      • Villari P.
      • Ioannidis J.P.
      Head-to-head randomized trials are mostly industry sponsored and almost always favor the industry sponsor.
      ,
      • Lundh A.
      • Sismondo S.
      • Lexchin J.
      • Busuioc O.A.
      • Bero L.
      Industry sponsorship and research outcome.
      ).
      The diffusion of the da Vinci robot, rather than being based on evidence derived from independent, randomized trials, seems to be mainly the result of well-designed marketing campaigns. Robotic surgery, in fact, is presented on the market as the ultimate technology and it has become a symbol of providing advanced care. Consequently, women may seek for robotic surgery and the number of da Vinci robots and robotic surgeons may increase to provide this cutting-edge, ultimate surgical technology to them. However, marketing the robot to patients as something that permits better surgery than regular laparoscopy, in the absence of robust evidence showing definite clinical advantages of RAL over SL, seems unethical. Moreover, the combination of these aggressive marketing strategies with a market monopoly, is potentially dangerous. In fact, if a self-propagating cycle takes place and the presence of the da Vinci robot expands from a limited number of teaching hospitals to virtually all hospitals, the costs for healthcare providers would become unacceptably high. Accordingly, it has been calculated that, if robotic surgery were to replace conventional surgery for all surgical procedures, the additional cost would be more than $2.5 billion every year (
      • Barbash G.I.
      • Glied S.A.
      New technology and health care costs-the case of robot-assisted surgery.
      ).
      Because an uncontrolled growth of robotic surgery would not be sustainable in the current medico-economic environment, it is of paramount importance that its implementation take place in research hospitals in order to evaluate the possible benefits of this technique for the patients. On the contrary, in the absence of robust evidence showing definite clinical advantages of RAL, limited healthcare resources should be employed in implementing surgical training in SL, in order to avoid the development of an irreversible dependence from the da Vinci robot. The ultimate goal of healthcare policies should be that of directing women requiring surgical treatment for advanced endometriosis towards high volume providers who are able to provide safe and cost-effective surgical care.
      In conclusion, RAL for the treatment of endometriosis did not show any perioperative advantage compared with SL, whereas it was associated with a longer operating time in some studies. The absence of advantages of RAL over SL was confirmed also among subgroups of women who were supposedly more likely to benefit from the former technique such as women with severe endometriosis, women with pelvic pain suggestive of endometriosis and obese women. Since the quality of available studies comparing RAL and SL for the treatment of endometriosis is low and, moreover, data regarding long-term pain relief and pregnancy rates are lacking, adequately designed randomized trials are needed to investigate the role of RAL for the treatment of endometriosis. Due to the higher costs, RAL treatment of endometriosis should be performed only within controlled studies.

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      Biography

      Nicola Berlanda graduated in Medicine and Surgery in 1994 and completed his residency in Gynaecology and Obstetrics in 1999, at the University of Milan. He was given the title Associate Professor of Gynaecology and Obstetrics by the Italian Scientific Commission in 2014. His major scientific interests are endometriosis and laparoscopic surgery.
      Key message
      Robotic-assisted laparoscopic treatment of endometriosis does not provide benefits over standard laparoscopy. Because the quality of published studies is low, randomized studies comparing robotic and standard laparoscopy for endometriosis are needed. At present, due to the increased costs, robotic surgery may not be justified outside of research settings.