Advertisement
Review article|Articles in Press

Minimally-invasive versus open pancreatic enucleation: systematic review and metanalysis of short-term outcomes

  • Author Footnotes
    1 Raffaello Roesel and Lorenzo Bernardi equally contributed to this work.
    Raffaello Roesel
    Correspondence
    Correspondence: Raffaello Roesel, Department of Visceral Surgery, Geneva University Hospital Rue Gabrielle-Perret-Gentil 4 1205 Geneva, Switzerland.
    Footnotes
    1 Raffaello Roesel and Lorenzo Bernardi equally contributed to this work.
    Affiliations
    Department of Visceral Surgery, University Hospital of Geneva (HUG), Rue Gabrielle-Perret Gentil 4, Geneve, Switzerland
    Search for articles by this author
  • Author Footnotes
    1 Raffaello Roesel and Lorenzo Bernardi equally contributed to this work.
    Lorenzo Bernardi
    Footnotes
    1 Raffaello Roesel and Lorenzo Bernardi equally contributed to this work.
    Affiliations
    Department of Visceral Surgery, Hospital of Lugano (EOC), Via Tesserete 46, 6900 Lugano, Switzerland
    Search for articles by this author
  • Marco A. Bonino
    Affiliations
    Department of Visceral Surgery, University Hospital of Geneva (HUG), Rue Gabrielle-Perret Gentil 4, Geneve, Switzerland
    Search for articles by this author
  • Sotirios G. Popeskou
    Affiliations
    Department of Visceral Surgery, Hospital of Lugano (EOC), Via Tesserete 46, 6900 Lugano, Switzerland
    Search for articles by this author
  • Fabio Garofalo
    Affiliations
    Department of Visceral Surgery, Hospital of Lugano (EOC), Via Tesserete 46, 6900 Lugano, Switzerland
    Search for articles by this author
  • Alessandra Cristaudi
    Affiliations
    Department of Visceral Surgery, Hospital of Lugano (EOC), Via Tesserete 46, 6900 Lugano, Switzerland
    Search for articles by this author
  • Author Footnotes
    1 Raffaello Roesel and Lorenzo Bernardi equally contributed to this work.
Published:February 23, 2023DOI:https://doi.org/10.1016/j.hpb.2023.02.014

      Abstract

      Background

      Minimally Invasive Pancreatic Enucleation, either laparoscopic or robot-assisted, is rarely performed. The aim of this study was to offer the current available evidence about the outcomes of minimally invasive pancreatic enucleations and explore the possible advantage of this approach over traditional surgery.

      Methods

      PubMed (MEDLINE), Cochrane Library and Embase (ELSEVIER) medical databases were searched for articles published from January 1990 to March 2022. Studies which included more than 10 cases of minimally-invasive pancreatic enucleation were included. Data on the outcomes were synthetized and meta-analyzed when appropriate.

      Results

      Twenty studies published between 2009 and 2022 with a total of 552 patients were included in the systematic review: three hundred fifty-one patients (63.5%) had a laparoscopic intervention, two hundred and one (36.5%) robot-assisted with a cumulative incidence of conversion rate of 5%.
      Minimally-invasive surgery was performed in 63% of cases on the body/tail of the Pancreas and in 37% of the cases on the head/uncinate process of the Pancreas. The cumulative post-operative 30 days - mortality rate was 0.2% and the major postoperative morbidity (Clavien-Dindo III-IV-V) 35%. Clinically relevant pancreatic fistula was observed in 17% of the patients.
      Compared with the standardized open approach (n: 366 patients), mean length of hospital stay was significantly reduced in patients undergoing minimally invasive pancreatic enucleation (2.45 days, p = 0.003) with a favorable trend for post-operative major morbidity (Clavien-Dindo III-IV) (- 24% RR, p: 0.13). Operative time, blood loss and clinically relevant pancreatic fistula rate were comparable between the two groups. One hundred and fourteen robot-assisted enucleations entered in a subgroup analysis with comparable results to open surgery.

      Conclusion

      Minimally-Invasive approach for pancreatic enucleation is safe, feasible and offers short-term clinical outcomes comparable with open surgery. The potential benefit of robotic surgery will need to be verified in further studies.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to HPB
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Zhou Y.
        • Zhao M.
        • Wu L.
        • Ye F.
        • Si X.
        Short- and long-term outcomes after enucleation of pancreatic tumors: an evidence-based assessment.
        Pancreatology. 2016; 16: 1092-1098
        • Beane J.D.
        • Borrebach J.D.
        • Billderback A.
        • Onuma A.E.
        • Adam M.A.
        • Zureikat A.H.
        • et al.
        Small pancreatic neuroendocrine tumors: Resect or enucleate?.
        Am J Surg. 2021; 222: 29-34
        • Gratian L.
        • Pura J.
        • Dinan M.
        • Roman S.
        • Reed S.
        • Sosa J.A.
        Impact of extent of surgery on survival in patients with small nonfunctional pancreatic neuroendocrine tumors in the United States.
        Ann Surg Oncol. 2014; 21: 3515-3521
        • Faitot F.
        • Gaujoux S.
        • Barbier L.
        • Novaes M.
        • Dokmak S.
        • Aussilhou B.
        • et al.
        Reappraisal of pancreatic enucleations: a single-center experience of 126 procedures.
        Surgery. 2015; 158: 201-210
        • Heeger K.
        • Falconi M.
        • Partelli S.
        • Waldmann J.
        • Crippa S.
        • Fendrich V.
        • et al.
        Increased rate of clinically relevant pancreatic fistula after deep enucleation of small pancreatic tumors.
        Langenbeck’s Arch Surg. 2014; 399: 315-321
        • Shamseer L.
        • Moher D.
        • Clarke M.
        • Ghersi D.
        • Liberati A.
        • Petticrew M.
        • et al.
        Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation.
        BMJ. 2015; 350: g7647
        • Bassi C.
        • Dervenis C.
        • Butturini G.
        • Fingerhut A.
        • Yeo C.
        • Izbicki J.
        • et al.
        Postoperative pancreatic fistula: an international study group (ISGPF) definition.
        Surgery. 2005; 138: 8-13
        • Bassi C.
        • Marchegiani G.
        • Dervenis C.
        • Sarr M.
        • Abu Hilal M.
        • Adham M.
        • et al.
        The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years after.
        Surgery. 2017; 161: 584-591
        • Higgins J.P.
        • Altman D.G.
        • Gotzsche P.C.
        • Juni P.
        • Moher D.
        • Oxman A.D.
        • et al.
        The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials.
        BMJ. 2011; 343: d5928
        • Hozo S.P.
        • Djulbegovic B.
        • Hozo I.
        Estimating the mean and variance from the median, range, and the size of a sample.
        BMC Med Res Methodol. 2005; 5: 13
        • Higgins J.P.
        Measuring inconsistency in meta-analyses.
        BMJ. 2003; : 327
        • Egger Mathias G.D.S.
        • Martin Schneider
        • Christoph Minder
        Bias in meta-analysis detected by simple, graphical test.
        BMJ. 1997; : 515
        • Luo Y.
        • Liu R.
        • Hu M.G.
        • Mu Y.M.
        • An L.C.
        • Huang Z.Q.
        Laparoscopic surgery for pancreatic insulinomas: a single-institution experience of 29 cases.
        J Gastrointest Surg. 2009; 13: 945-950
        • Dedieu A.
        • Rault A.
        • Collet D.
        • Masson B.
        • Sa Cunha A.
        Laparoscopic enucleation of pancreatic neoplasm.
        Surg Endosc. 2011; 25: 572-576
        • Fernandez-Cruz L.
        • Molina V.
        • Vallejos R.
        • Jimenez Chavarria E.
        • Lopez-Boado M.A.
        • Ferrer J.
        Outcome after laparoscopic enucleation for non-functional neuroendocrine pancreatic tumours.
        HPB. 2012; 14: 171-176
        • Zureikat A.H.
        • Moser A.J.
        • Boone B.A.
        • Bartlett D.L.
        • Zenati M.
        • Zeh 3rd, H.J.
        250 robotic pancreatic resections: safety and feasibility.
        Ann Surg. 2013; 258: 554-559
        • Choi K.S.
        • Chung J.C.
        • Kim H.C.
        Feasibility and outcomes of laparoscopic enucleation for pancreatic neoplasms.
        Ann Surg Treat Res. 2014; 87: 285-289
        • Song K.B.
        • Kim S.C.
        • Hwang D.W.
        • Lee J.H.
        • Lee D.J.
        • Lee J.W.
        • et al.
        Enucleation for benign or low-grade malignant lesions of the pancreas: single-center experience with 65 consecutive patients.
        Surgery. 2015; 158: 1203-1210
        • Jin J.B.
        • Qin K.
        • Li H.
        • Wu Z.C.
        • Zhan Q.
        • Deng X.X.
        • et al.
        Robotic enucleation for benign or borderline tumours of the pancreas: a retrospective analysis and comparison from a high-volume Centre in Asia.
        World J Surg. 2016; 40: 3009-3020
        • Shi Y.
        • Peng C.
        • Shen B.
        • Deng X.
        • Jin J.
        • Wu Z.
        • et al.
        Pancreatic enucleation using the da Vinci robotic surgical system: a report of 26 cases.
        Int J Med Robot. 2016; 12: 751-757
        • Tian F.
        • Hong X.F.
        • Wu W.M.
        • Han X.L.
        • Wang M.Y.
        • Cong L.
        • et al.
        Propensity score-matched analysis of robotic versus open surgical enucleation for small pancreatic neuroendocrine tumours.
        Br J Surg. 2016; 103: 1358-1364
        • Zhang R.C.
        • Zhou Y.C.
        • Mou Y.P.
        • Huang C.J.
        • Jin W.W.
        • Yan J.F.
        • et al.
        Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis.
        Surg Endosc. 2016; 30: 2657-2665
        • Dokmak S.
        • Fteriche F.S.
        • Aussilhou B.
        • Levy P.
        • Ruszniewski P.
        • Cros J.
        • et al.
        The largest European single-center experience: 300 laparoscopic pancreatic resections.
        J Am Coll Surg. 2017; 225: 226-234 e2
        • Siech M.
        • Strauss P.
        • Huschitt S.
        • Bartsch D.K.
        • Wittel U.
        • Keck T.
        The indications for laparoscopic pancreatectomy.
        Dtsch Arztebl Int. 2017; 114: 263-268
        • Belfiori G.
        • Wiese D.
        • Partelli S.
        • Wachter S.
        • Maurer E.
        • Crippa S.
        • et al.
        Minimally invasive versus open treatment for benign Sporadic insulinoma comparison of short-term and long-term outcomes.
        World J Surg. 2018; 42: 3223-3230
        • Di Benedetto F.
        Ultrasound-guided robotic enucleation of pancreatic neuroendocrine tumors.
        Surgical Innovation, 2018
        • Chen K.
        • Pan Y.
        • Mou Y.P.
        • Wang G.Y.
        • Zhang R.C.
        • Yan J.F.
        • et al.
        Evolution of laparoscopic pancreatic resections for pancreatic and periampullary Diseases: perioperative outcomes of 605 patients at a high-volume center.
        J Laparoendosc Adv Surg Tech. 2019; 29: 1085-1092
        • Ore A.S.
        • Klompmaker S.
        • Stackhouse K.
        • Solis-Velasco M.
        • Francken M.
        • Callery M.P.
        • et al.
        Does surgical approach affect outcomes of enucleation for benign and low-grade pancreatic tumors? An ACS-NSQIP evaluation.
        HPB. 2019; 21: 1585-1591
        • Najafi N.
        • Mintziras I.
        • Wiese D.
        • Albers M.B.
        • Maurer E.
        • Bartsch D.K.
        A retrospective comparison of robotic versus laparoscopic distal resection and enucleation for potentially benign pancreatic neoplasms.
        Surg Today. 2020; 50: 872-880
        • Ei S.
        • Mihaljevic A.L.
        • Kulu Y.
        • Kaiser J.
        • Hinz U.
        • Buchler M.W.
        • et al.
        Enucleation for benign or borderline tumors of the pancreas: comparing open and minimally invasive surgery.
        HPB. 2021; 23: 921-926
        • Lapo Bencini I.U.
        • Trafeli Martina
        • Paolini Claudia
        • Moraldi Luca
        • Tribuzi Angela
        • Pacciani Sabrina
        • et al.
        Robotic pancreatic surgery: minimally invasive approach to challenging operations.
        Minerva Surgery. 2021; 76: 138-145
        • Xu J.
        • Li F.
        • Zhan H.
        • Liu H.
        • Wu D.
        • Hu S.
        • et al.
        Laparoscopic enucleation of pancreatic tumours: a single-institution experience of 66 cases.
        ANZ J Surg. 2021; 91: 106-110
        • Sterne J.A.
        • Hernán M.A.
        • Reeves B.C.
        • Savović J.
        • Berkman N.D.
        • Viswanathan M.
        • et al.
        ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions.
        BMJ. 2016; 355: i4919
        • Tsuchikawa T.
        • Tanaka K.
        • Nakanishi Y.
        • Asano T.
        • Noji T.
        • Nakamura T.
        • et al.
        Clinical impact of organ-preserving surgery for pancreatic neuroendocrine neoplasms: a single-center experience.
        Pancreas. 2021; 50: 196-200
        • Heidsma C.M.
        • Tsilimigras D.I.
        • van Dieren S.
        • Rocha F.
        • Abbott D.E.
        • Fields R.
        • et al.
        Indications and outcomes of enucleation versus formal pancreatectomy for pancreatic neuroendocrine tumors.
        HPB. 2021; 23: 413-421
        • Wang P.
        • Wei J.
        • Wu J.
        • Xu W.
        • Chen Q.
        • Gao W.
        • et al.
        Diagnosis and treatment of solid-pseudopapillary tumors of the pancreas: a single institution experience with 97 cases.
        Pancreatology. 2018; 18: 415-419
        • Kaiser J.
        • Fritz S.
        • Klauss M.
        • Bergmann F.
        • Hinz U.
        • Strobel O.
        • et al.
        Enucleation: a treatment alternative for branch duct intraductal papillary mucinous neoplasms.
        Surgery. 2017; 161: 602-610
        • Riviere D.
        • Gurusamy K.S.
        • Kooby D.A.
        • Vollmer C.M.
        • Besselink M.G.
        • Davidson B.R.
        • et al.
        Laparoscopic versus open distal pancreatectomy for pancreatic cancer.
        Cochrane Database Syst Rev. 2016; 4Cd011391
        • Asbun H.J.
        • Stauffer J.A.
        Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System.
        J Am Coll Surg. 2012; 215: 810-819
        • Guerra F.
        • Giuliani G.
        • Bencini L.
        • Bianchi P.P.
        • Coratti A.
        Minimally invasive versus open pancreatic enucleation. Systematic review and meta-analysis of surgical outcomes.
        J Surg Oncol. 2018; 117: 1509-1516
        • Huttner F.J.
        • Koessler-Ebs J.
        • Hackert T.
        • Ulrich A.
        • Buchler M.W.
        • Diener M.K.
        Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms.
        Br J Surg. 2015; 102: 1026-1036
        • Dalla Valle R.
        • Cremaschi E.
        • Lamecchi L.
        • Guerini F.
        • Rosso E.
        • Iaria M.
        Open and minimally invasive pancreatic neoplasms enucleation: a systematic review.
        Surg Endosc. 2019; 33: 3192-3199
        • Dokmak S.
        • Aussilhou B.
        • Fteriche F.S.
        • Belghiti J.
        • Sauvanet A.
        Hanging Maneuver for Stomach traction in laparoscopic distal pancreatic resections: an original technique Applied in 218 patients.
        Dig Surg. 2017; 34: 89-94
        • Jilesen A.P.
        • van Eijck C.H.
        • Busch O.R.
        • van Gulik T.M.
        • Gouma D.J.
        • van Dijkum E.J.
        Postoperative outcomes of enucleation and standard resections in patients with a pancreatic neuroendocrine tumor.
        World J Surg. 2016; 40: 715-728
        • Giuliani T.
        • De Pastena M.
        • Paiella S.
        • Marchegiani G.
        • Landoni L.
        • Festini M.
        • et al.
        Pancreatic Enucleation Patients Share the Same Quality of Life as the General Population at Long-Term Follow-Up: A Propensity-Score Matched Analysis.
        Ann Surg. 2021; (Epub 2021/04/16)https://doi.org/10.1097/SLA.0000000000004911
        • Kabir T.
        • Tan Z.Z.X.
        • Syn N.
        • Chung A.Y.F.
        • Ooi L.
        • Goh B.K.P.
        Minimally-invasive versus open enucleation for pancreatic tumours: a propensity-score adjusted analysis.
        Ann Hepatobiliary Pancreat Surg. 2019; 23: 258-264
        • Duconseil P.
        • Marchese U.
        • Ewald J.
        • Giovannini M.
        • Mokart D.
        • Delpero J.R.
        • et al.
        A pancreatic zone at higher risk of fistula after enucleation.
        World J Surg Oncol. 2018; 16: 177
        • Wang X.
        • Tan C.L.
        • Zhang H.
        • Chen Y.H.
        • Yang M.
        • Ke N.W.
        • et al.
        Short-term outcomes and risk factors for pancreatic fistula after pancreatic enucleation: a single-center experience of 142 patients.
        J Surg Oncol. 2018; 117: 182-190
        • Marchegiani G.
        • Landoni L.
        • Andrianello S.
        • Masini G.
        • Cingarlini S.
        • D’Onofrio M.
        • et al.
        Patterns of recurrence after resection for pancreatic neuroendocrine tumors: who, when, and where?.
        Neuroendocrinology. 2019; 108: 161-171
        • Giuliani T.
        • Marchegiani G.
        • Girgis M.D.
        • Crino S.F.
        • Muthusamy V.R.
        • Bernardoni L.
        • et al.
        Endoscopic placement of pancreatic stent for “Deep” pancreatic enucleations operative technique and preliminary experience at two high-volume centers.
        Surg Endosc. 2020; 34: 2796-2802