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Minimally invasive versus open central pancreatectomy: Systematic review and meta-analysis

Open AccessPublished:August 18, 2022DOI:https://doi.org/10.1016/j.surg.2022.06.024

      Abstract

      Background

      This systematic review and meta-analysis aimed to give an overview on the postoperative outcome after a minimally invasive (ie, laparoscopic and robot-assisted) central pancreatectomy and open central pancreatectomy with a specific emphasis on the postoperative pancreatic fistula. For benign and low-grade malignant lesions in the pancreatic neck and body, central pancreatectomy may be an alternative to distal pancreatectomy. Exocrine and endocrine insufficiency occur less often after central pancreatectomy, but the rate of postoperative pancreatic fistula is higher.

      Methods

      An electronic search was performed for studies on elective minimally invasive central pancreatectomy and open central pancreatectomy, which reported on major morbidity and postoperative pancreatic fistula in PubMed, Cochrane Register, Embase, and Google Scholar until June 1, 2021. A review protocol was developed a priori and registered in PROSPERO as CRD42021259738. A meta-regression was performed by using a random effects model.

      Results

      Overall, 41 studies were included involving 1,004 patients, consisting of 158 laparoscopic minimally invasive central pancreatectomies, 80 robot-assisted minimally invasive central pancreatectomies, and 766 open central pancreatectomies. The overall rate of postoperative pancreatic fistula was 14%, major morbidity 14%, and 30-day mortality 1%. The rates of postoperative pancreatic fistula (17% vs 24%, P = .194), major morbidity (17% vs 14%, P = .672), and new-onset diabetes (3% vs 6%, P = .353) did not differ significantly between minimally invasive central pancreatectomy and open central pancreatectomy, respectively. Minimally invasive central pancreatectomy was associated with significantly fewer blood transfusions, less exocrine pancreatic insufficiency, and fewer readmissions compared with open central pancreatectomy. A meta-regression was performed with a random effects model between minimally invasive central pancreatectomy and open central pancreatectomy and showed no significant difference for postoperative pancreatic fistula (random effects model 0.16 [0.10; 0.24] with P = .789), major morbidity (random effects model 0.20 [0.15; 0.25] with P = .410), and new-onset diabetes mellitus (random effects model 0.04 [0.02; 0.07] with P = .651).

      Conclusion

      In selected patients and in experienced hands, minimally invasive central pancreatectomy is a safe alternative to open central pancreatectomy for benign and low-grade malignant lesions of the neck and body. Ideally, further research should confirm this with the main focus on postoperative pancreatic fistula and endocrine and exocrine insufficiency.

      Introduction

      Central pancreatectomy, also known as middle pancreatectomy, or the Dagradi-Serio-Iacono procedure, was first described in 1984 as a parenchyma-sparing operation that enables the removal of benign and low-grade malignant lesions from the neck and body of the pancreas.
      • Dagradi A S.G.
      Pancreatectomia intermedia.
      The increased use of cross-sectional imaging has contributed to a rising incidence of benign and low-grade malignant lesions found in the pancreas.
      • Farrell J.J.
      Prevalence, diagnosis and management of pancreatic cystic neoplasms: current status and future directions.
      Indications for central pancreatectomy include neuroendocrine neoplasms, noninvasive intraductal papillary mucinous neoplasm, cystadenomas, solid pseudopapillary tumors, and other rare benign lesions located in the neck and body of the pancreas.
      • Santangelo M.
      • Esposito A.
      • Tammaro V.
      • et al.
      What indication, morbidity and mortality for central pancreatectomy in oncological surgery? A systematic review.
      A parenchyma-sparing technique may reduce the rate of exocrine and endocrine pancreatic insufficiency, hereby maintaining quality of life.
      • Jin Y.
      • Feng Y.-Y.
      • Qi X.-G.
      • et al.
      Pancreatogastrostomy vs pancreatojejunostomy after pancreaticoduodenectomy: an updated meta-analysis of RCTs and our experience.
      However, after central pancreatectomy, both a pancreato-enteric anastomosis on the left side of the deducted specimen and a transected surface on the right side leaves the patient with a high risk of developing a postoperative pancreatic fistula (POPF).
      • Chen S.
      • Zhan Q.
      • Jin J.
      • Wu Z.
      • Shi Y.
      Robot-assisted laparoscopic versus open middle pancreatectomy: short-term results of a randomized controlled trial.
      ,
      • Boone B.A.
      • Zenati M.
      • Hogg M.E.
      • et al.
      Assessment of quality outcomes for robotic pancreaticoduodenectomy: identification of the learning curve.
      Several pancreato-enteric reconstructions have been suggested for central pancreatectomy. Whereas pancreatogastrostomy (PG) is easier to perform and does not require Roux-en-Y reconstruction, a pancreatojejunostomy (PJ) may have better long-term outcomes in terms of exocrine function.
      • Jin Y.
      • Feng Y.-Y.
      • Qi X.-G.
      • et al.
      Pancreatogastrostomy vs pancreatojejunostomy after pancreaticoduodenectomy: an updated meta-analysis of RCTs and our experience.
      The currently available literature has emphasized the possibility of a minimally invasive approach to central pancreatectomy (MICP) as an alternative to open central pancreatectomy (OCP).
      • Chen S.
      • Zhan Q.
      • Jin J.
      • Wu Z.
      • Shi Y.
      Robot-assisted laparoscopic versus open middle pancreatectomy: short-term results of a randomized controlled trial.
      However, the postoperative outcome of MICP and OCP have not been compared.
      • Boone B.A.
      • Zenati M.
      • Hogg M.E.
      • et al.
      Assessment of quality outcomes for robotic pancreaticoduodenectomy: identification of the learning curve.
      This systematic review and meta-analysis aimed to provide an overview of the available evidence regarding short- and long-term surgical results of MICP versus OCP.

      Methods

      Systematic literature search

      According to the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA)
      • Kamioka H.
      Preferred reporting items for systematic review and meta-analysis protocols (prisma-p) 2015 statement.
      guidelines, a systematic search was performed in PubMed, Embase, and Cochrane Library for relevant articles published from January 1, 2000 up to June 1, 2021. A protocol for this review has been registered on the Prospective Register of Systematic Reviews (PROSPERO) (registration number CRD42021259738). Ethical approval was waived for this study by the institutional review board of the Amsterdam UMC. A description of the systematic literature search, study selection, and data collection process is shown in Appendix S1 in Supplementary Materials.

      Eligibility criteria

      Randomized as well as nonrandomized studies, prospective and retrospective studies that involve elective MICP and OCP, which reported on major morbidity or POPF specific per approach (MICP or OCP), are included. The studies reporting data of <5 procedures were excluded due to a risk of selection bias.

      Outcome measures

      The primary outcomes of this study were clinically relevant POPF (grade B and C), defined by the International Study Group of Pancreatic Surgery (ISGPS) definition. Both the ISGPS 2005 and 2016 were used for POPF grade B/C combined.
      • Bassi C.
      • Marchegiani G.
      • Dervenis C.
      • et al.
      The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after.
      Major morbidity was defined as a Clavien-Dindo grade ≥3. The ISGPS 2005 and 2016 definitions are both taken into the analysis, because only clinically relevant POPF is reported in current study. In this scenario of combined B/C the rate of clinically relevant POPF is similar between the 2 definitions.
      • Bassi C.
      • Marchegiani G.
      • Dervenis C.
      • et al.
      The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after.
      Secondary outcomes were overall morbidity, reinterventions, readmissions, intensive care unit admissions, reoperations, new-onset diabetes mellitus (DM), and exocrine pancreatic insufficiency (EPI).

      Data extraction

      Initial data included baseline characteristics: first author, year of publication, country, and number of centers, patients age, sex, body mass index (BMI), comorbidities, American Society of Anesthesiologists status; type of surgical treatment (laparoscopic, robot-assisted-assisted, open), CR-POPF (defined as POPF grade B or C), Clavien-Dindo grade 3 morbidity, new-onset DM, worsening DM, new-onset EPI, EPI, 90-day postoperative mortality, and length of hospital stay.

      Risk of bias

      Risk of bias in the individual studies was assessed independently by 2 reviewers (S.S.F. and W.V.B.) using the Newcastle-Ottawa Scale tool
      • Stang A.
      Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses.
      (Table 1A, 1B, 1C). It was developed to assess the quality of nonrandomized studies with its design, content, and ease of use directed to the task of incorporating the quality assessments in the interpretation of meta-analytic results. Disagreements regarding the risk of bias assessment were resolved by consulting a third party (M.B.). Heterogeneity was investigated with the χ2 analysis and I2 test and interpreted as follows: 0% to 40% low, 30% to 60% moderate, 50% to 90% high, and 75% to 100% considerable. A fixed effects model was used with a I2 index of <50%. A random effects model was used with an I2 >50%.

      Summary measures and synthesis of data

      Robot-assisted and laparoscopic approaches were pooled as “minimally invasive.” Baseline characteristics, operative parameters, and outcome measures were given per approach (minimally invasive versus open), in percentages, and only the studies reporting on this parameter are given in this percentage. The P values were given to assess the differences in outcomes between approaches. The POPF were reported per anastomosis (PJ/PG). A meta-regression was performed by using a random effects model with R statistics (R Foundation for Statistical Computing, Vienna, Austria). The events were pooled for minimally invasive and for open approach, which were compared for the postoperative outcomes (POPF, major morbidity, overall morbidity, EPI, and new-onset DM). Type of anastomosis was compared for the outcome POPF by pooling all of the PJs and PGs and performing random effects model.

      Results

      Search results

      The search identified 1,966 studies based on title and abstract against the predetermined eligibility criteria. Overall, 1,925 studies were excluded: 302 duplicates, 1,402 wherein central pancreatectomy was not the subject of analysis, 190 wherein the outcomes of interest were not reported, and 4 because no full text was available. Of the remaining 68 studies, full-text papers were obtained and a further 11 excluded because outcomes of interest were not reported per type of approach, 7 because the minimum number of patients included was not met, 5 studies were excluded because they were published before 2000, and 4 studies because there was an overlap in the period of analysis with a study from the same center. No studies were added after a crosscheck. Finally, 41 studies remained. Of the 41 studies, 26 described OCP,
      • Lv A.
      • Qian H.G.
      • Qiu H.
      • Wu J.H.
      • Hao C.Y.
      Is central pancreatectomy truly recommendable? A 9-year single-center experience.
      • Roggin K.K.
      • Rudloff U.
      • Blumgart L.H.
      • Brennan M.F.
      Central pancreatectomy revisited.
      • Balzano G.
      • Zerbi A.
      • Veronesi P.
      • Cristallo M.
      • Di Carlo V.
      Surgical treatment of benign and borderline neoplasms of the pancreatic body.
      • Wayne M.
      • Neragi-miandoab S.
      • Kasmin F.
      • Brown W.
      • Pahuja A.
      • Cooperman A.M.
      Central pancreatectomy without anastomosis.
      • Adham M.
      • Guinippero A.
      • Hervieu V.
      • et al.
      Central pancreatectomy.
      • Shikano T.
      • Nakao A.
      • Kodera Y.
      Middle pancreatectomy: safety and long-term results.
      • Allendorf J.D.
      • Schrope B.A.
      • Lauerman M.H.
      • Inabnet W.B.
      • Chabot J.A.
      Postoperative glycemic control after central pancreatectomy for mid-gland lesions.
      • Brown K.M.
      • Shoup M.
      • Abodeely A.
      • Hodul P.A.M.
      • Brems J.J.
      • Aranha G.V.
      Central pancreatectomy for benign pancreatic lesions.
      • Du Z.
      • Chen S.
      • Han B.
      • Shen B.
      • Liu Y.
      • Peng C.
      Middle segmental pancreatectomy: a safe and organ-preserving option for benign and low-grade malignant lesions.
      • Crippa B.
      • Bassi C.
      • Warshaw A.L.
      • et al.
      Middle pancreatectomy: indications, short- and long-term operative outcomes.
      • Dinorcia J.
      • Ahmed L.
      • Lee M.K.
      • et al.
      Better preservation of endocrine function after central versus distal pancreatectomy for mid-gland lesions.
      • Goudard Y.
      • Gaujoux S.
      • Dokmak S.
      • et al.
      Reappraisal of central pancreatectomy: a 12-year single-center experience.
      • Hirono S.
      • Yamaue H.
      Middle pancreatectomy for pancreatic neoplasms.
      • Yeo C.J.
      Central pancreatectomy with pancreaticogastrostomy for benign pancreatic pathology.
      • Goldstein M.J.
      • Toman J.
      • Chabot J.A.
      Pancreaticogastrostomy: a novel application after central pancreatectomy.
      • Lafemina J.
      • Vagefi P.A.
      • Warshaw A.L.
      • Ferna C.
      Transgastric pancreaticogastric anastomosis.
      • Iacono C.
      • Bortolasi L.
      • Serio G.
      Indications and technique of central pancreatectomy: early and late results.
      • Müller M.W.
      • Friess H.
      • Kleeff J.
      • et al.
      An option to treat benign pancreatic body lesions.
      • Ocuin L.M.
      • Sarmiento J.M.
      • Staley C.A.
      • et al.
      Comparison of central and extended left pancreatectomy for lesions of the pancreatic neck.
      • Lee S.E.
      • Jang J.
      • Hwang D.W.
      • Lee K.U.
      • Kim S.
      Clinical efficacy of organ-preserving pancreatectomy for benign or low-grade malignant potential lesion.
      • Lavu H.
      • Knuth J.L.
      • Baker M.S.
      • et al.
      Middle segment pancreatectomy can be safely incorporated into a pancreatic surgeon’s clinical practice.
      • Sauvanet A.
      • Partensky C.
      • Sastre B.
      • et al.
      Medial pancreatectomy: a multi- institutional retrospective study of 53 patients by the French Pancreas Club.
      • Shibata S.
      • Sato T.
      • Andoh H.
      • et al.
      Outcomes and indications of segmental pancreatectomy.
      • Sudo T.
      • Murakami Y.
      • Uemura K.
      • et al.
      Middle pancreatectomy with pancreaticogastrostomy: a technique, operative outcomes, and long-term pancreatic function.
      • Shimada K.
      • Sakamoto Y.
      • Esaki M.
      • et al.
      Role of medial pancreatectomy in the management of intraductal papillary mucinous neoplasms and islet cell tumors of the pancreatic neck and body.
      • Sperti C.
      • Pasquali C.
      • Ferronato A.
      • Pedrazzoli S.
      Median pancreatectomy for tumors of the neck and body of the pancreas.
      10 laparoscopic MICP
      • Dokmak S.
      • Ftériche F.S.
      • Aussilhou B.
      • et al.
      The largest European single-center experience: 300 laparoscopic pancreatic resections.
      • Cienfuegos J.A.
      • Salguero J.
      • Núñez-Córdoba J.M.
      • et al.
      Short- and long-term outcomes of laparoscopic organ-sparing resection in pancreatic neuroendocrine tumors: a single-center experience.
      • Senthilnathan P.
      • Gul S.I.
      • Gurumurthy S.S.
      • et al.
      Laparoscopic central pancreatectomy: our technique and long-term results in 14 patients.
      • Hong D.
      • Liu Y.
      • Peng S.
      • et al.
      Binding pancreaticogastrostomy in laparoscopic central pancreatectomy: a novel technique in laparoscopic pancreatic surgery.
      • Chen X.M.
      • Zhang Y.
      • Sun D.L.
      Laparoscopic central pancreatectomy for solid pseudopapillary tumors of the pancreas: our experience with ten cases.
      • Cunha A.S.
      • Rault A.
      • Beau C.
      • Collet D.
      • Masson B.
      Laparoscopic central pancreatectomy: single institution experience of 6 patients.
      • Rotellar F.
      • Pardo F.
      • Montiel C.
      • et al.
      Totally laparoscopic Roux-en-Y duct-to-mucosa.
      • Byung K.
      • Song S.
      • Kim C.
      • et al.
      Laparoscopic central pancreatectomy for benign or low-grade malignant lesions in the pancreatic neck and proximal body.
      • Bin R.Z.
      • Mou Z.Y.
      • Zhou X.X.Y.
      Comparison of clinical outcomes and quality of life between laparoscopic and open central pancreatectomy with pancreaticojejunostomy.
      • Zhang H.
      • Xu Q.
      • Tan C.
      • et al.
      Laparoscopic spleen-preserving distal versus central pancreatectomy for tumors in the pancreatic neck and proximal body.
      and 5 robot-assisted MICP.
      • Abood G.J.
      • Can M.F.
      • Daouadi M.
      • et al.
      Robotic-assisted minimally invasive central pancreatectomy: technique and outcomes.
      • Cheng K.
      • Shen B.
      • Peng C.
      • Deng X.
      • Hu S.
      Initial experiences in robot-assisted middle pancreatectomy..
      • Boggi U.
      • Napoli N.
      • Costa F.
      • et al.
      Robotic-assisted pancreatic resections.
      • Kang C.
      • Dong K.
      • Woo J
      Initial experiences using robot-assisted central pancreatectomy with pancreaticogastrostomy: a potential way to advanced laparoscopic pancreatectomy.
      • Wang Z.
      • Zhao G.
      • Zhao Z.
      • Gao Y.
      • Xu Y.
      • Yin Z.
      • et al.
      An end-to-end pancreatic anastomosis in robotic central pancreatectomy.
      A flowchart of the literature search is shown in Figure 1.

      Included studies

      The 41 studies including 1,004 patients, consisting of 766 OCP, 158 laparoscopic central pancreatectomies (LCP), and 80 robot-assisted central pancreatectomies. The study characteristics from the included studies are shown in Table I. The operative parameters are shown in Table II, and PJ was performed in 45% and PG in 53%. As shown in Table III, 22 studies with 609 patients reported on POPF B/C, and this was present in 141 (23%) patients. Forty studies with 968 patients reported on morbidity, and this was present in 501 (52%) patients, 32 studies with 760 patients reported on major morbidity, and this was present in 162 (21%) patients, 33 studies with 866 patients reported on reinterventions, and this was present in 80 (9%) patients. Thirty-five studies with 856 patients reported on new-onset DM, and this was present in 47 (5%) patients; and 29 studies with 669 patients reported on EPI, and this was present in 32 (5%) patients.
      Table IStudy characteristics from the included studies on centra
      AuthorStudy periodStudy designCountryN patientsAge, yrFemale n (%)
      OCP
      Sperti 20001985–1998RMItaly1045.7 (14–71)5 (50)
      Sauvanet 20021990–1998RMFrance5349 (16–73)42 (79)
      Balzano 20031990–2000RMItaly3251 (24–68)21 (66)
      Goldstein 20041999–2002RMUSA1257 ± 159 (75)
      Effron 20041999–2002RMUSA1461 (37–84)7 (50)
      Shibata 20041989–2002RMJapan1058 (47–73)7 (70)
      Iacono 2005RMItaly20
      Roggin 20061993–2005RMUSA10
      Müller 20062001–2005RMGermany4050 ± 1720 (50)
      Brown 20061999–2004RMUSA1059 (21–75)8 (80)
      Crippa 20071990–2005RMUSA10052 ± 14.483 (83)
      Allendorf 20071990–2005RMUSA2656 (15–79)19 (73)
      Adham 20081987–2005RMFrance5049 (13–79)38 (76)
      Lavu 20081998–2008RMUSA3449 (19–75)22 (65)
      Ocuin 20082000–2007RMUSA1355 ± 149 (69)
      Shimada 20082000–2007RMJapan1461 ± 155 (36)
      Hirono 20091999–2008RMJapan2469 (26–81)14 (58)
      Wayne 20092005–2009RMUSA1054 ± 155 (50)
      Sudo 20121996–2008RMJapan1960 (34–80)10 (53)
      Shikano 20101991–2006RMJapan2658 ± 912 (46)
      Dinorcia 20101997–2009RMUSA5065 (49–73)37 (74)
      Lafemina 20102005–2009RM, PSMUSA2355 (15)15 (65)
      Lee 20101995–2007RMKorea1446 ± 712 (86)
      Du 20132003–2009RMChina3649 ± 1527 (75)
      Goudard 20142000–2012RMFrance10056 (42–65)67 (67)
      Lv 20172007–2014RMChina1637 ± 1212 (75)
      Subtotal1985–201476654 (14–80)415 (54)
      Laparoscopic MICP
      Sa chuna 20071999–2006PMFrance655 (30–67)5 (83)
      Rotellar 20082005–2007PMSpain953 (28–60)8 (89)
      Chen 20142009–2013RMChina1045 (35–57)8 (80)
      Song20142007–2010RMKorea2647 (37–56)19 (73)
      Hong 20152011–2014RMChina1054 (33–67)6 (60)
      Senthilnathan 2015RMIndia14498 (57)
      Zhang 20171997–2015RMChina1752 (39–65)10 (59)
      Cienfuegos 20172003–2015RMSpain855 (43– 67)
      Dokmak 20172008–2015RMFrance3551 (37–65)24 (68)
      Zhang 20192013–2017RMChina2346 (35–57)15 (65)
      Subtotal15850 (30–67)103 (65)
      Robot-assisted MICP
      Kang 20112007–2009RMKorea550.0 ± 12.30 (0)
      Abood 20132009–2010RMUSA964 (18–75)6 (67)
      Chen 20132010–2011RMChina5050 ± 1234 (68)
      Boggi 20162008–2014RMItaly5
      Wang 20192017–2017RMChina1142 ± 145 (45)
      Subtotal8050 (18–75)46 (60)
      Total100453 (13–84)654 (65)
      MICP, minimally invasive central pancreatectomy; OCP, open central pancreatectomy; PM, prospectively monocenter; PSM, propensity score–matched; RM, retrospectively monocenter.
      Table IIOperative parameters
      AuthorNOperative time in minEstimated blood loss in mLBlood transfusion (%)PJ n (%)PG n (%)SCM Sutured n (%)SCM Stapling n (%)
      OCP
      Sperti 200010273 (180–330)440 (150–1500)4 (40)10 (100)(0)
      Sauvanet 20025326 (49)25 (47)53 (100)32 (55)
      Balzano 200332207 ± 57443 ± 3776 (19)10 (31)0 (0)
      Goldstein 200412226 ± 70700 ± 5200 (0)0 (0)12 (100)12 (100)0 (0)
      Effron 200414229 ± 49412 ± 3264 (29)0 (0)14 (100)14 (100)0 (0)
      Shibata 200410331 (207–471)359 ± 7110 (100)0 (0)
      Iacono 20052020 (100)0 (0)20 (100)0 (0)
      Roggin 2006109 (90)1 (10)10 (100)0 (0)
      Müller 200640304 ± 73564 ± 4333 (8)40 (100)0 (0)0 (0)40 (100)
      Brown 200610255 (160–380)650 (200–2000)6 (60)4 (40)5 (50)5 (50)
      Crippa 2007100248 ± 60311 ± 3358 (8)95 (95)5 (5)100 (100)0 (0)
      Allendorf 200726226 ± 70.7650 ± 4460 (0)26 (100)
      Adham 200850201 (110–360)6 (12)44 (88)50 (100)0 (0)
      Lavu 200834244.7 ± 58720.9 ± 1143.731 (91)3 (89)34 (100)0 (0)
      Ocuin 200813232 ± 93308 ± 2844 (30)6 (46)7 (54)
      Shimada 200814320 (195–390)262 (55–510)0 (0)10 (71)3 (21)14 (100)0 (0)
      Hirono 200924279 (205–399)355 (20–4070)3 (13)21 (87)3 (12)
      Wayne 20091074 ± 10164 ± 890 (0)0 (0)10 (100)0 (0)
      Sudo 201219215 (160–375)228 (60–1780)2 (11)3 (15)16 (84)19 (100)0 (0)
      Shikano 201026295 ± 61312 ± 2362 (8)2 (7)24 (92)26 (100)0 (0)
      Dinorcia 201050257 (222–315)400 (275–675)0 (0)2 (4)48 (96)
      Lafemina 201023191 (39)0 (0)0 (0)23 (100)
      Lee 201014228 ± 67292 ± 5301 (7)14 (100)0 (0)
      Du 201336222.1 ± 62316 ± 31022 (61)14 (39)36 (100)0 (0)
      Goudard 2014100250 (100–300)2 (2)0 (0)98 (98)88 (88)12 (12)
      Lv 201716265 ± 69212 ± 1130 (0)7 (44)9 (56)9 (56)7 (44)
      Subtotal766245 (110–471)377 (20–4070)39(8)336 (44)379 (52)514 (86)119 (20)
      Laparoscopic MICP
      Sa chuna 20076225 (180–365)125 (50–300)0 (0)0 (0)6 (100)0 (0)6 (100)
      Rotellar 20089435 (357–509)0 (0)9 (100)0 (0)0 (0)9 (100)
      Chen 201410271 (250–310)104 (80–150)0 (0)10 (100)0 (0)0 (0)10 (100)
      Song 201426350 (287 –413)477 (89–865)0 (0)26 (100)0 (0)0 (0)26 (100)
      Hong 201510198 (170–250)125 (20–300)0 (0)0 (0)10 (100)0 (0)10 (100)
      Senthilnathan 201514240 (162–342)153 (60–320)0 (0)14 (100)0 (0)0 (0)14 (100)
      Zhang 201717280 (247–314)76 (6–146)0 (0)17 (100)0 (0)0 (0)17 (100)
      Cienfuegos 20178288 (189–387)0 (0)8 (100)
      Dokmak 201735191 (120–285)111 (0–800)1 (3)0 (0)350 (0)35 (100)
      Zhang 2019230 (0)23 (100)
      Subtotal158268 (120–509)193 (0–865)1 (1)76 (60)51 (40)0 (0)158 (100)
      Robot-assisted MICP
      Kang5432.0 ± 65.7275.0 ± 221.70 (0)5 (100)0 (0)
      Abood9425 (305–506)190 (50–350)0 (0)2 (22)7 (77)
      Chen50160 (120–210)50 (50–100)0 (0)0 (0)50 (100)
      Boggi5
      Wang11121 (105–199)50 (20–100)0 (0)
      Subtotal80204 (105–506)81 (20–350)0 (0)2 (3)57 (97)5 (100)0 (0)
      1004244 (74–506)202 (0–4070)40 (5)414 (45)487 (53)519 (68)277 (36)
      The percentages are based on the studies that reported on the outcome.
      MICP, minimally invasive central pancreatectomy; PG, pancreatogastrostomy; PJ, pancreaticojejunostomy; SCM, stump closing method.
      Table IIIOutcomes from the included studies
      AuthorNGlobal morbidity n (%)Severe morbidity

      N (%)
      POPF b/c

      N (%)
      PPH

      N (%)
      DGE n (%)Reintervention

      N (%)
      NODM

      N (%)
      EPI

      N (%)
      Readmission

      N (%)
      LOS30-d mortality

      N (%)
      OCP
      Sperti 2000104 (40)3 (30)0 (0)0 (0)0 (0)0 (0)26 (11–48)0 (0)
      Sauvanet 20025340 (75)1 (2)1 (2)6 (11)3 (5)4 (7)1 (2)
      Balzano 20033220 (62)1 (3)3 (9)14 ± 60 (0)
      Goldstein 2004123 (25)1 (8)0 (0)0 (0)0 (0)0 (0)2 (16)0 (0)1 (8)7 (5–15)0 (0)
      Effron 2004147 (50)2 (14)2 (14)0 (0)2 (14)111 (7)
      Shibata 2004105 (50)1 (10)0 (0)0 (0)0 (0)1 (10)0 (0)37 (19–49)0 (0)
      Iacono 2005207 (35)0 (0)0 (0)0 (0)0 (0)
      Roggin 2006106 (60)5 (50)1 (10)1 (10)0 (0)0 (0)
      Müller 20064011 (27)13 (32)5 (12)0 (0)2 (5)6 (15)7 (17)4 (10)11 (6–62)1 (3)
      Brown 2006106 (60)4 (40)1 (10)0 (0)0 (0)0 (0)0 (0)0 (0)9 (7–25)0 (0)
      Crippa 200710058 (58)17 (17)17 (17)1 (1)2 (2)0 (0)4 (4)5 (5)16 (16)13 ± 100 (0)
      Allendorf 2007268 (31)4 (15)0 (0)0 (0)0 (0)2 (4)0 (0)3 (11)7 ± 30 (0)
      Adham 20085018 (36)13 (26)3 (6)0 (0)6 (12)0 (0)19 (12–71)0 (0)
      Lavu 20083416 (47)2 (6)4 (12)0 (0)4 (12)9 ± 50 (0)
      Ocuin 20081312 (92)5 (38)5 (38)0 (0)1 (7)1 (7)9 ± 31 (8)
      Shimada 2008146 (43)4 (28)1 (7)1 (7)0 (0)0 (0)30 (18–68)0 (0)
      Hirono 2009247 (29)3 (12)1 (4)0 (0)1 (4)1 (4)0 (0)22 (11–58)1 (4)
      Wayne 2009104 (40)0 (0)0 (0)0 (0)0 (0)5 ± 10 (0)
      Sudo 20121910 (53)9 (47)9 (47)1 (5)7 (37)5 (26)6 (32)0 (0)
      Shikano 20102610 (38)3 (11)3 (11)0 (0)1 (4)0 (0)
      Dinorcia 20105021 (42)6 (12)9 (18)2 (4)7 (14)7 (14)6 (12)7 (5–8)0 (0)
      Lafemina 20102316 (69)7 (30)1 (4)7 (30)0 (0)0 (0)7 (30)50 (0)
      Lee 2010144 (28)0 (0)1 (7)0 (0)0 (0)0 (0)0 (0)17 ± 70 (0)
      Du 2013361 (3)0 (0)1 (2)0 (0)
      Goudard 201410072 (72)18 (18)44 (44)6 (6)2 (2)23 (23)2 (2)6 (6)6 (6)25 (18–32)3 (3)
      Lv 20171611 (68)4 (25)10 (62)3 (18)0 (0)0 (0)0 (0)31 ± 220 (0)
      Subtotal766382 (37)121 (20)101 (31)29 (5)7 (1)66 (9)39 (6)30 (6)47 (11)9 (5–71)8 (1)
      Laparoscopic MICP
      Sa chuna 200762 (33)0 (0)0 (0)0 (0)0 (0)0 (0)0 (0)18 (15 –25)0 (0)
      Rotellar 200893 (33)3 (33)1 (11)0 (0)1 (11)0 (0)0 (0)0 (0)5 (3–41)0 (0)
      Chen 2014102 (20)0 (0)0 (0)0 (0)0 (0)0 (0)0 (0)0 (0)0 (0)13 (10–23)0 (0)
      Song 20142610 (38)4 (15)0 (0)0 (0)2 (7)0 (0)14 (7–21)0 (0)
      Hong 2015105 (50)1 (10)0 (0)1 (10)1 (10)1 (10)0 (0)0 (0)0 (0)13 (8–20)0 (0)
      Senthilnathan 2015148 (57)4 (28)2 (14)0 (0)3 (21)0 (0)2 (14)0 (0)0 (0)8 (6–12)0 (0)
      Zhang 20171710 (59)3 (18)3 (18)4 (23)1 (6)4 (23)1 (6)0 (0)0 (0)16 (4–28)0 (0)
      Cienfuegos 201783 (37)3 (37)2 (25)3 (37)6 (5–7)0 (0)
      Dokmak 20173526 (74)9 (26)8 (23)6 (17)4 (11)1 (3)22 (13–54)0 (0)
      Zhang 2019238 (35)8 (35)5 (22)2 (8)2 (8)0 (0)2 (8)0 (0)
      Subtotal15877 (49)32 (21)18 (17)17 (11)4 (7)14 (9)8 (7)2 (2)1 (1)15 (3–54)0 (0)
      Robot-assisted MICP
      Kang51 (20)0 (0)0 (0)0 (0)15 ± 80 (0)
      Abood97 (77)1 (11)2 (22)0 (0)0 (0)10 (7–19)0 (0)
      Chen5023 (46)9 (18)2 (4)12 (24)1 (2)16 ± 50 (0)
      Boggi54 (80)0 (0)4 (80)0 (0)0 (0)2 (40)18 (12–22)0 (0)
      Wang117 (65)8 (72)7 (63)0 (0)0 (0)6 (5–9)0 (0)
      Subtotal8042 (53)9 (11)22 (29)2 (4)12 (20)0 (0)0 (0)0 (0)3 (5)13 (5–22)0 (0)
      Total1004501 (52)162 (20)141 (23)48 (6)25 (4)80 (9)47 (5)32 (5)51 (8)10 (3–71)8 (1)
      The percentages are based on the studies that reported on the outcome.
      LOS, length of hospital stay in days in median and range; MICP, minimally invasive central pancreatectomy; POPF, postoperative pancreatic fistula grade B/C; PPH, postpancreatectomy hemorrhage.
      Table IV reports outcomes for OCP, laparoscopic MICP, and robot-assisted MICP. There was a lower amount of blood transfusions (0% vs 8%, P < .01), EPI (1% vs 5% P = .032), and readmissions (2% vs 11% P = .010) in the MICP compared with the OCP group. The rest of the outcomes did not differ significantly between the minimally invasive and the open group.
      Table IVComparison of included studies per approach
      AuthorRobot MICPLaparoscopic MICPMICPOpen CPP value
      N studies5101526
      Baseline
      Patients n80158238766
      Female n (%)45 (60)103 (65)148 (62)415 (54)
      Age mean (SD)50 (18–75)50 (30–67)50 (18–75)54 (14–80)
      Operative
      OT median (IQR)204 (105–506)268 (120–509)246 (105–509)245 (110–471)
      Blood loss median (IQR)81 (20–350)193 (0–865)155 (0–865)377 (20–4070)
      Transfusion n (%)0 (0)1 (1)1 (0)39 (8)< .01
      Conversion n (%)1 (1)1 (1)2 (1)1.283
      Outcome
      Overall morbidity n (%)42 (53)77 (49)119 (50)382 (52).969
      Severe morbidity n (%)9 (11)32 (21)41 (17)121 (14).672
      POPF n (%)22 (29)18 (11)40 (17)101 (24).194
      PPH n (%)2 (4)17 (11)19 (8)29 (5).298
      NODM n (%)0 (0)8 (7)8 (3)39 (6).353
      EPI n (%)0 (0)2 (2)2 (1)30 (5).032
      Reintervention n (%)2 (4)14 (9)16 (7)66 (9).426
      Readmission n (%)3 (5)1 (1)4 (2)47 (11).010
      LOS median (IQR)13 (5–22)15 (3–54)14 (3–54)9 (5–71)
      Mortality n (%)0 (0)0 (0)0 (0)8 (1).614
      The percentages are based on the studies that reported on the outcome. Which studies reported on the outcome measures are given in Table III.
      CP, central pancreatectomy; EPI, exocrine pancreatic insufficiency; LOS, length of stay; MICP, minimally invasive central pancreatectomy; NODM, new-onset diabetes mellitus; OT, operative time; POPF, postoperative pancreatic fistula grade B/C; PPH, postpancreatectomy hemorrhage.

      Risk of bias of included studies

      Risk of bias is displayed in Supplementary Table A through C. None of the included studies have a very high risk of bias (0–3 points), and the majority is classified from 6 to 8 points. Inconsistency was determined based on the heterogeneity factor P and I2 as shown in Supplementary Table D. For the outcomes POPF and overall morbidity substantial heterogeneity was found with P < .01 and I2 > 50%. For major morbidity moderate heterogeneity was found with P = .03 and I2 = 35%. The heterogeneity of new-onset DM was low with P = .80 and I2 = 0%. The definitions used in the included studies for POPF, EPI, and new-onset DM are displayed in Supplementary Table E, and the indications for which central pancreatectomy was performed are displayed in Supplementary Table F.

      Meta-analysis

      A meta-regression was performed with laparoscopic MICP and robot-assisted MICP combined into MICP, because there were only 5 robot-assisted MICP with 80 cases included. Meta-regression revealed no significant difference between MICP and OCP for the risk of POPF (Random Effects Model [REM] 0.16 [0.10; 0.24] with P = .953), overall postoperative morbidity (REM 0.48 [0.41; 0.54] with P = .446), major postoperative morbidity (REM 0.20 [0.15; 0.26] with P = .388), and new-onset DM (REM 0.04 [0.02; 0.07] with P = .651) as shown in Figures 2 Figures 3 Figures 4 Figures 5 Figures 6 and Table V. There were not enough events to perform a meta-regression for exocrine dysfunction between these groups. A subgroup meta-regression compared the risk of POPF based on a PJ or PG anastomosis. There was no significant difference between PJ and PG (REM 0.28 [0.18; 0.40] with P = .945) as shown in Figures 2 Figures 3 Figures 4 Figures 5 Figures 6 and Table VI.
      Figure thumbnail gr2
      Figure 2Meta-analysis for POPF between OCP and MICP with REM. MI, minimally invasive apparoach.
      Figure thumbnail gr3
      Figure 3Meta-analysis for severe morbidity between OCP and MICP with REM.
      Figure thumbnail gr4
      Figure 4Meta-analysis for morbidity between OCP and MICP with REM.
      Figure thumbnail gr5
      Figure 5Meta-analysis for NODM between OCP and MICP with REM.
      Figure thumbnail gr6
      Figure 6Meta-analysis for POPF between PJ and PG with REM.
      Table VMeta-regression MICP versus OCP
      OutcomeMICP n (%)Mi remOCP n (%)Open REMTotal n (%)Total REMP value
      POPF B/C40 (17.5%)0.17 [0.10; 0.27]96 (21.9%)0.15 [0.07; 0.29]136 (20.4%)0.16 [0.10; 0.24].789
      Overall morbidity101 (43.4%)0.42 [0.30; 0.56]382 (52.2%)0.50 [0.42; 0.57]488 (50.2%)0.47 [0.41; 0.54].349
      Major morbidity
      Clavien-Dindo ≥3 morbidity.
      46 (20.9%)0.15 [0.07; 0.31]121 (20.7%)0.21 [0.16; 0.27]167 (20.7%)0.20 [0.15; 0.25].410
      NODM8 (5.3%)0.03 [0.01; 0.14]39 (5.5%)0.04 [0.03; 0.08]47 (5.5%)0.04 [0.02; 0.07].651
      MI, minimally invasive approach, REM: random-effects model; OCP, open central pancreatectomy; POPF, postoperative pancreatic fistula; NODM, new-onset diabetes mellitus; MICP, minimally invasive central pancreatectomy.
      Clavien-Dindo ≥3 morbidity.
      Table VIMeta-regression PJ versus PG
      OutcomePJ n (%)PJ REMPG n (%)PG REMTotal n (%)Total REMP value
      POPF B/C30 (31.9%)0.28 [0.15; 0.46]67 (33.8%)0.28 [0.16; 0.45]94 (32.2%)0.28 [0.18; 0.40].945
      PJ, pancreaticojejunostomy; PG, pancreaticogastrostomy; POPF, postoperative pancreatic fistula; REM, random-effects model.

      Discussion

      This first systematic review comparing laparoscopic and robot-assisted MICP with OCP found no difference between MICP and OCP regarding the rates of POPF, major morbidity, and new-onset DM. An MICP was associated with fewer blood transfusions, less EPI, and fewer readmissions compared to OCP. In a subgroup analysis, no difference in the rates of POPF was found between PJ and PG anastomoses during central pancreatectomy.
      The MICP was introduced in the late 1990s with an unclear impact on clinical outcome.
      • Zureikat Amer H.
      • Nguyen Kevin T.
      • Bartlett David L.
      • Herbert J.
      • Zeh A.J.M.
      Robotic-assisted major pancreatic resection and reconstruction.
      ,
      • Stafford A.T.
      • Walsh R.M.
      Robotic surgery of the pancreas: the current state of the art.
      Since then, many studies have demonstrated the safety and feasibility of the minimally invasive approach for pancreatic resections in selected patients and in experienced hands with similar rates of POPF and overall and major morbidity but a shorter hospital stay, compared to open approach.
      • Byung K.
      • Song S.
      • Kim C.
      • et al.
      Laparoscopic central pancreatectomy for benign or low-grade malignant lesions in the pancreatic neck and proximal body.
      ,
      • Giulianotti P.C.
      • Sbrana F.
      • Bianco F.M.
      Robot-assisted laparoscopic middle pancreatectomy.
      ,
      • Zureikat Amer H.
      • Nguyen Kevin T.
      • Bartlett David L.
      • Herbert J.
      • Zeh A.J.M.
      Robotic-assisted major pancreatic resection and reconstruction.
      The multicenter LEOPARD trial reported that minimally invasive distal pancreatectomy reduced the time to functional recovery and was associated with better a quality of life without increasing costs compared with open distal pancreatectomy.
      • Xiao W.
      • Zhu J.
      • Peng L.
      • Hong L.
      • Sun G.
      • Li Y.
      The role of central pancreatectomy in pancreatic surgery : a systematic review and meta-analysis.
      A recent network meta-analysis including 4 randomized trials reported that when laparoscopic pancreatoduodenectomy and robot-assisted pancreatoduodenectomy are performed in high-volume centers, the short-term perioperative and oncologic outcomes are largely comparable, if not slightly improved, compared with open pancreatoduodenectomy.68 Since Giulianotti described the first robot-assisted distal pancreatectomy in 2001, robot-assisted pancreatic surgery has been gradually implemented over the years.
      • Giulianotti P.C.
      • Sbrana F.
      • Bianco F.M.
      Robot-assisted laparoscopic middle pancreatectomy.
      Overall, current data suggests thats MICP is safe and feasible. In a retrospective comparative study, LCP compared with OCP demonstrated a prolonged operative duration, similar rates of overall morbidity, major morbidity, and clinically significant POPF but a shorter length of stay.
      • Byung K.
      • Song S.
      • Kim C.
      • et al.
      Laparoscopic central pancreatectomy for benign or low-grade malignant lesions in the pancreatic neck and proximal body.
      In another comparative study, LCP demonstrated lower blood loss and shorter diet start time. However, there was no difference regarding clinically significant POPF and the hospital stay.
      • Bin R.Z.
      • Mou Z.Y.
      • Zhou X.X.Y.
      Comparison of clinical outcomes and quality of life between laparoscopic and open central pancreatectomy with pancreaticojejunostomy.
      In 2017, a randomized controlled trial comparing robot-assisted MICP with OCP was published.
      • Chen S.
      • Zhan Q.
      • Jin J.
      • Wu Z.
      • Shi Y.
      Robot-assisted laparoscopic versus open middle pancreatectomy: short-term results of a randomized controlled trial.
      After randomizing 100 patients, the authors reported that robot-assisted MICP was associated with a significantly shorter hospital stay, reduced operative time, blood loss, POPF, and expected postoperative recovery, compared with OCP. Theoretically, MICP could combine the advantages of minimally invasive laparoscopic approach with the implementation of the robot-assisted technology. The magnified, steady, 3-dimensional high-definition imaging and the integrated ultrasonography system allows the surgeon a precise anatomical localization of the lesion and of the vascular structures.
      • Stafford A.T.
      • Walsh R.M.
      Robotic surgery of the pancreas: the current state of the art.
      Implementation of robot-assisted MICP has been shown to be feasible and safe, with specific emphasis on vascular dissection, suturing and reconstructions.
      • Boone B.A.
      • Zenati M.
      • Hogg M.E.
      • et al.
      Assessment of quality outcomes for robotic pancreaticoduodenectomy: identification of the learning curve.
      Our findings adhered to the current evidence available, as we found a lower amount of blood transfusions, EPI, and readmissions after MICP compared with OCP. However, the direct impact on the occurrence of POPF between MICP and OCP remains unclear. The impact of POPF after central pancreatectomy may be larger compared with distal pancreatectomy, because the former involves an enteral anastomosis. Further research is required on MICP focusing on POPF, endocrine, and exocrine function.
      In order to minimalize the POPF rate, the optimal pancreatico-enteric anastomosis in central pancreatectomy is still open to debate. A PJ is commonly used, although PG is highly implemented in central pancreatectomy in France, United States, and Japan.
      • Dagradi A S.G.
      Pancreatectomia intermedia.
      ,
      • Sauvanet A.
      • Partensky C.
      • Sastre B.
      • et al.
      Medial pancreatectomy: a multi- institutional retrospective study of 53 patients by the French Pancreas Club.
      ,
      • Goldstein M.J.
      • Toman J.
      • Chabot J.A.
      Pancreaticogastrostomy: a novel application after central pancreatectomy.
      ,
      • van Hilst J.
      • De Rooij T.
      • Bosscha K.
      • et al.
      Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours (LEOPARD-2): a multicentre, patient-blinded, randomised controlled phase 2/3 trial.
      ,
      • Sudo T.
      • Murakami Y.
      • Uemura K.
      • et al.
      Middle pancreatectomy with pancreaticogastrostomy: a technique, operative outcomes, and long-term pancreatic function.
      No RCTs have compared PJ versus PG in patients undergoing central pancreatectomy. A 2017 Cochrane review with 10 RCTs concluded that reliable evidence to support the use of pancreatojejunostomy over pancreatogastrostomy is lacking.
      As previously stated, the rationale of central pancreatectomy is to preserve pancreatic parenchyma and, thus, to avoid endocrine and exocrine insufficiency. The present meta-analysis confirmed low rates of endocrine insufficiency, new-onset, and worsening diabetes rates between MICP and OCP, but there was a large heterogeneity regarding the definition of exocrine insufficiency in the studies. New-onset DM after pancreatic surgery leads to lower quality of life and long-term morbidity.
      • Forbes J.M.
      • Cooper M.E.
      Mechanisms of diabetic complications.
      ,
      • Scholten L.
      • Mungroop T.H.
      • Haijtink S.A.L.
      • et al.
      New-onset diabetes after pancreatoduodenectomy: a systematic review and meta-analysis.
      Two previous meta-analyses
      • Xiao W.
      • Zhu J.
      • Peng L.
      • Hong L.
      • Sun G.
      • Li Y.
      The role of central pancreatectomy in pancreatic surgery : a systematic review and meta-analysis.
      ,
      • Zhang R.
      • Xu X.
      • Yan J.
      • Wu D.
      Laparoscopic central pancreatectomy with pancreaticojejunostomy: preliminary experience with 8 cases.
      have shown lower rates of overall endocrine insufficiency after central pancreatectomy, compared to distal pancreatectomy.
      Central pancreatectomy is a good alternative in younger patients because the risk of insulin-dependent new-onset DM increases significantly with age.
      • Scholten L.
      • Mungroop T.H.
      • Haijtink S.A.L.
      • et al.
      New-onset diabetes after pancreatoduodenectomy: a systematic review and meta-analysis.
      Additionally, the severity of new-onset DM increases with time.
      • Bock E.A.
      • Hurtuk M.G.
      • Shoup M.
      • Aranha G.V.
      Late complications after pancreaticoduodenectomy with pancreaticogastrostomy.
      On top of that, the patients receiving central pancreatectomy for benign and premalignant lesions have a longer prospect of recurrence-free survival compared to patients receiving pancreatic resection for malignant lesions. The additional benefits of central pancreatectomy for benign and premalignant lesions positively decrease the chance of long-term quality of life diminishing postoperative morbidity.
      The outcomes of this study should be interpreted in light of several limitations. First, the meta-regression only included non-RCTs, and these could have been subjected to selection bias, information bias, and follow-up bias. Second, the studies reporting on MICP were published more recently compared to studies reporting on OCP, which could have contributed to a certain degree of bias as perioperative care has improved. Third, as analyzed, there was substantial heterogeneity for POPF and moderate heterogeneity for major morbidity between the included studies. This could have been subjected to the annual volume of central pancreatectomy performed and therefore heterogeneity between surgeons’ experience. A recent study suggested that the outcomes after distal pancreatectomy can be improved when the procedure is performed by more experienced surgeons due to the impact of learning curves, and this would count for central pancreatectomy as well, being a more complex procedure.
      • Shakir M.
      • Boone B.A.
      • Polanco P.M.
      • et al.
      The learning curve for robotic distal pancreatectomy: an analysis of outcomes of the first 100 consecutive cases at a high-volume pancreatic centre.
      Fourth, the hospital stay was found to be longer in the studies focusing on MICP compared with OCP. This might have been the result of unknown confounders but deserves further study. However, the 1 RCT published comparing robotic MICP with OCP found a significantly shorter hospital stay after MICP.
      • Chen S.
      • Zhan Q.
      • Jin J.
      • Wu Z.
      • Shi Y.
      Robot-assisted laparoscopic versus open middle pancreatectomy: short-term results of a randomized controlled trial.
      Fifth, because not all of the studies reported on exocrine and endocrine insufficiency, or did report on the rates but without mentioning the definitions, the current study could not draw any firm conclusions on this topic. Sixth, the recommendations of this review and further research of the superiority of (MI)CP should be seen in light of the surgeons’ experience. However, because operative steps are essentially equal, once a surgeon has mastered both minimally invasive pancreatoduodenectomy and distal pancreatectomy, a MICP could be a feasible procedure.
      In conclusion, this systematic review and meta-analysis found no differences between laparoscopic and robot-assisted MICP and OCP regarding the risk of POPF, major morbidity, and new-onset DM. With the previously established superior time to functional recovery with minimally invasive pancreatic surgery,
      • Poves I.
      • Burdío F.
      • Morató O.
      • et al.
      Comparison of perioperative outcomes between laparoscopic and open approach for pancreatoduodenectomy: the Padulap randomized controlled trial.
      • van Hilst J.
      • De Rooij T.
      • Bosscha K.
      • et al.
      Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours (LEOPARD-2): a multicentre, patient-blinded, randomised controlled phase 2/3 trial.
      • de Rooij T.
      • van Hilst J.
      • Vogel J.A.
      • et al.
      Minimally invasive versus open distal pancreatectomy (LEOPARD): study protocol for a randomized controlled trial.
      MICP could be considered for benign and low-grade malignant lesions of the neck and body of the pancreas in case of sufficient surgical experience with minimally invasive pancreatic surgery. Prospective studies are needed to identify the true benefits of MICP compared to OCP, with specific emphasis on POPF.

      Funding/Support:

      This research did not receive any specific funding from any agencies in the public, commercial, or not-for-profit areas.

      Conflict of interest/Disclosure:

      The authors have no conflicts of interests or disclosures to report.

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