Abstract
Background
Minimally invasive pancreaticoduodenectomy, either laparoscopic or robotic, is a high-risk procedure with demanding learning curve. The aim of this prospective cohort study was to evaluate short-term clinical and oncologic outcomes of 3D-laparoscopic pancreaticoduodenectomy (3dLPD) with stented pancreaticogastrostomy (sPG) and Roux-en-Y gastroenterostomy (ryGES).
Methods
Between March 2016 and July 2021, 347 consecutive patients underwent 3dLPD for confirmed or suspected pancreatic or periampullary tumors. Pancreatic duct diameter measured 3 mm or less in 221 (64%) and pancreatic texture was soft in 191 (55%) patients. Simultaneous resection of the superior mesenteric or portal vein was performed in 52 (15%) patients.
Results
Postoperative complications were observed in 189 (54%) patients, with severe complications (Clavien–Dindo grade > 2) in 68 (20%) including 4 (1.2%) deaths. Clinically relevant pancreatic fistula (cPOPF) occurred in 88 (25%), hemorrhage in 25 (7%), and bile leakage in 10 (3%) patients. Clinical pancreatic fistula was strongly associated with soft pancreatic texture and small pancreatic duct diameter (p < 0.001) and managed by endoscopic trans-gastric drainage in 34 (38.6%) patients, reoperation in 12 (13.6%), and ICU admission in 11 (12.5%). The remaining 31 (35%) patients with cPOPF were managed without invasive intervention. Median length of hospital stay after surgery was 13 (range 5–112; IQR 8–18) days. In pancreatic adenocarcinoma (PDAC) the R0-resection rate was 66/186 (36%), R1-indirect 95/186 (51%), and R1-direct 25 (13%). Median number of locoregional lymph nodes retrieved in PDAC was 21 (IQR 15–28). R0-resection rate for malignancy other than PDAC was 78/86 (91%) with a median of 16 (IQR 12–22) locoregional lymph nodes retrieved.
Conclusion
3dLPD with sPG and ryGES is associated with 1.2% mortality and 25% cPOPF. About two-third of patients with cPOPF were managed with some type of invasive intervention, whereas the intraoperatively placed drains sufficed in one-third of patients.
Clinical trial registry
Clinicaltrials.gov NCT02671357.
Similar content being viewed by others
References
van Hilst J, de Rooij T, Bosscha K, Brinkman DJ, van Dieren S, Dijkgraaf MG, Gerhards MF, de Hingh IH, Karsten TM, Lips DJ, Luyer MD, Busch OR, Festen S, Besselink MG, Dutch Pancreatic Cancer Group (2019) Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumlours (LEOPARD-2): a multicentre, patient-blinded, randomized controlled phase 2/3 trial. Lancet Gastroenterol Hepatol 4:199–207
Wang M, Li D, Chen R, Huang X, Li J, Liu Y, Liu J, Cheng W, Chen X, Zhao W, Li J, Tan Z, Huang H, Li D, Zhu F, Qin T, Ma J, Yu G, Zhou B, Zheng S, Tang Y, Han W, Meng L, Ke J, Feng F, Chen B, Yin X, Chen W, Ma H, Xu J, Liu Y, Lin R, Dong Y, Yu Y, Liu J, Zhang H, Qin R, Minimally Invasive Treatment Group in the Pancreatic Disease Branch of China’s International Exchange and Promotion Association for Medicine and Healthcare (MITG-P-CPAM) (2021) Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours: a multicentre, open-label, randomised controlled trial. Lancet Gastroenterol Hepatol 6:438–447
Adam MA, Choudhury K, Dinan MA, Reed SD, Scheri RP, Blazer DG 3rd, Roamn SA, Sosa JA (2015) Minimally invasive versus open pancreaticoduodenectomy for cancer. Practice patterns and short-term outcomes among 7061 patients. Ann Surg 262:372–377
de Rooij T, Lu MZ, Steen MW, Gerhards MF, Dijkgraaf MG, Busch OR, Lips DJ, Festen S, Besselink MG, on behalf of the Dutch Pancreatic Cancer Group (2016) Minimally invasive versus open pancreatoduodenectomy. Systematic review and meta-analysis of comparative cohort and registry studies. Ann Surg 264:257–267
Topal B, Fieuws S, Aerts R, Weerts J, Feryn T, Roeyen G, Bertrand C, Hubert C, Janssens M, Closset J, on behalf of the Belgian Section of Hepatobiliary and Pancreatic Surgery (2013) Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after pancreaticoduodenectomy for pancreatic or periampullary tumors: a multicenter randomised trial. Lancet Oncol 14:655–662
Croome KP, Farnell MB, Que FG, Reid-Lombardo KM, Truty MJ, Nagorney DM, Kendrick ML (2014) Total laparoscopic pancreaticoduodenectomy for pancreatic ductal adenocarcinoma oncologic advantages over open approaches? Ann Surg 260:633–640
Kamarajah SK, Bundred JR, Marc OS, Jiao LR, Hilal MA, Manas DM, White SA (2020) A systematic review and network meta-analysis of different surgical approaches for pancreaticoduodenectomy. HPB 22:329–339
Geers J, Topal H, Jaekers J, Topal B (2020) 3D-laparoscopic pancreaticoduodenectomy with superior mesenteric or portal vein resection for pancreatic cancer. Surg Endosc 34:5616–5624
Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Büchler MW (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142:761–768
Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M, Allen P, Andersson R, Asbun HJ, Besselink MG, Conlon K, Del Chiaro M, Falconi M, Fernandez-Cruz L, Fernandez-Del Castillo C, Fingerhut A, Friess H, Gouma DJ, Hackert T, Izbicki J, Lillemoe KD, Neoptolemos JP, Olah A, Schulick R, Shrikhande SV, Takada T, Takaori K, Traverso W, Vollmer CR, Wolfgang CL, Yeo CJ, Salvia R, Buchler M (2016) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 161:584–591
Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Yeo CJ, Büchler MW (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142:20–25
Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, Fan ST, Yokoyama Y, Crawford M, Makuuchi M, Christophi C, Banting S, Brooke-Smith M, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Nimura Y, Figueras J, DeMatteo RP, Büchler MW, Weitz J (2011) Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery (ISGLS). Surgery 149:680–688
Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213
Al-Hawary MM, Francis IR, Chari ST, Fishman EK, Hough DM, Lu DS, Macari M, Megibow AJ, Miller FH, Mortele KJ, Merchant NB, Minter RM, Tamm EP, Sahani DV, Simeone DM (2014) Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the Society of Abdominal Radiology and the American Pancreatic Association. Radiology 270:248–260
Klompmaker S, van Hilst J, Wellner UF, Busch OR, Coratti A, D’Hondt M, Dokmak S, Festen S, Kerem M, Khatkov I, Lips DJ, Lombardo C, Luyer M, Manzoni A, Molenaar IQ, Rosso E, Saint-Marc O, Vansteenkiste F, Wittel UA, Bonsing B, Koerkamp BG, Hilal MA, Fuks D, Poves I, Keck T, Boggi U, Besselink MG, European consortium on Minimally Invasive Pancreatic Surgery (E-MIPS) (2020) Outcomes After minimally-invasive versus open pancreatoduodenectomy: a pan-European propensity score matched study. Ann Surg 271:356–363
Andrianello S, Marchegiani G, Malleo G, Masini G, Balduzzi A, Paiella S, Esposito A, Landoni L, Casetti L, Tuveri M, Salvia R, Bassi C (2020) Pancreaticojejunostomy with externalized stent vs pancreaticogastrostomy with externalized stent for patients with high-risk pancreatic anastomosis: a single-center, phase 3, randomized clinical trial. JAMA Surg 155:313–321
Veziant J, Selvy M, Buc E, Slim K (2021) Evidence-based evaluation of abdominal drainage in pancreatic surgery. J Visc Surg 158:220–230
Liu X, Chen K, Chu X, Liu G, Yang Y, Tian X (2021) Prophylactic intra-operative drainage after pancreatic resection: an updated meta-analysis. Front Oncol 11:658829
Lyu Y, Cheng Y, Wang B, Zhao S, Chen L (2020) Peritoneal drainage or no drainage after pancreaticoduodenectomy and/or distal pancreatectomy: a meta-analysis and systematic review. Surg Endosc 34:4991–5005
Aiolfi A, Lombardo F, Bonitta G, Danelli P, Bona D (2021) Systematic review and updated network meta-analysis comparing open, laparoscopic, and robotic pancreaticoduodenectomy. Updates Surg 73:909–922
Nickel F, Haney CM, Kowalewski KF, Probst P, Limen EF, Kalkum E, Diener MK, Strobel O, Müller-Stich BP, Hackert T (2020) Laparoscopic versus open pancreaticoduodenectomy: a systematic review and meta-analysis of randomized controlled trials. Ann Surg 271:54–66
Palanivelu C, Senthilnathan P, Sabnis SC, Babu NS, Gurumurthy SS, Vijai NA, Nalankili VP, Raj PP, Parthasarathy R, Rajapandian S (2017) Randomized clinical trial of laparoscopic versus open pancreatoduodenectomy for periampullary tumours. Br J Surg 104:1443–1450
Poves I, Burdío F, Morató O, Iglesias M, Radosevic A, Ilzarbe L, Visa L, Grande L (2018) Comparison of perioperative outcomes between laparoscopic and open approach for pancreatoduodenectomy: the PADULAP randomized controlled trial. Ann Surg 268:731–739
Asbun HJ, Moekotte AL, Vissers FL, Kunzler F, Cipriani F, Alseidi A, D’Angelica MI, Balduzzi A, Bassi C, Björnsson B, Boggi U, Callery MP, Del Chiaro M, Coimbra FJ, Conrad C, Cook A, Coppola A, Dervenis C, Dokmak S, Edil BH, Edwin B, Giulianotti PC, Han HS, Hansen PD, van der Heijde N, van Hilst J, Hester CA, Hogg ME, Jarufe N, Jeyarajah DR, Keck T, Kim SC, Khatkov IE, Kokudo N, Kooby DA, Korrel M, de Leon FJ, Lluis N, Lof S, Machado MA, Demartines N, Martinie JB, Merchant NB, Molenaar IQ, Moravek C, Mou YP, Nakamura M, Nealon WH, Palanivelu C, Pessaux P, Pitt HA, Polanco PM, Primrose JN, Rawashdeh A, Sanford DE, Senthilnathan P, Shrikhande SV, Stauffer JA, Takaori K, Talamonti MS, Tang CN, Vollmer CM, Wakabayashi G, Walsh RM, Wang SE, Zinner MJ, Wolfgang CL, Zureikat AH, Zwart MJ, Conlon KC, Kendrick ML, Zeh HJ, Hilal MA, Besselink MG, International Study Group on Minimally Invasive Pancreas Surgery (I-MIPS) (2020) The Miami international evidence-based guidelines on minimally invasive pancreas resection. Ann Surg 271:1–14
Torphy R, Friedman C, Halpern A, Chapman BC, Ahrendt SS, McCarter MM, Edil BH, Schulick RD, Gleisner A (2019) Comparing short-term and oncologic outcomes of minimally invasive versus open pancreaticoduodenectomy across low and high volume centers. Ann Surg 270:1147–1155
van der Geest LGM, van Rijssen LB, Molenaar IQ, de Hingh IH, Koerkamp BG, Busch ORC, Lemmens VEPP, Besselink MGH, Dutch Pancreatic Cancer Group (2016) Volume-outcome relationships in pancreatoduodenectomy for cancer. HPB 18:317–324
Shi Y, Jin J, Qiu W, Weng Y, Wang J, Zhao S, Huo Z, Qin K, Wang Y, Chen H, Deng X, Peng C, Shen B (2020) Short-term outcomes after robot-assisted vs open pancreaticoduodenectomy after the learning curve. JAMA Surg 155:389–394
Fung G, Sha M, Kunduzi B, Froghi F, Rehman S, Froghi S (2022) Learning curves in minimally invasive pancreatic surgery a systematic review. Langenbecks Arch Surg. https://doi.org/10.1007/s00423-022-02470-3
Klaiber U, Probst P, Strobel O, Michalski CW, Dörr-Harim C, Diener MK, Büchler MW, Hackert T (2018) Meta-analysis of delayed gastric emptying after pylorus-preserving versus pylorus-resecting pancreatoduodenectomy. Br J Surg 105:339–349
Cheng Y, Briarava M, Lai M, Wang X, Tu B, Cheng N, Gong J, Yuan Y, Pilati P, Mocellin S (2017) Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction for the prevention of postoperative pancreatic fistula following pancreaticoduodenectomy. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD012257.pub2
Keck T, Wellner UF, Bahra M, Klein F, Sick O, Niedergethmann M, Wilhelm TJ, Farkas SA, Börner T, Bruns C, Kleespies A, Kleeff J, Mihaljevic AL, Uhl W, Chromik A, Fendrich V, Heeger K, Padberg W, Hecker A, Neumann UP, Junge K, Kalff JC, Glowka TR, Werner J, Knebel P, Piso P, Mayr M, Izbicki J, Vashist Y, Bronsert P, Bruckner T, Limprecht R, Diener MK, Rossion I, Wegener I, Hopt UT (2016) Pancreatogastrostomy versus pancreatojejunostomy for RECOnstruction after PANCreatoduodenectomy (RECOPANC, DRKS 00000767): perioperative and long-term results of a multicenter randomized controlled trial. Ann Surg 263:440–449
Daamen LA, Smits FJ, Besselink MG, Busch OR, Borel Rinkes IH, van Santvoort HC, Molenaar IQ, Dutch Pancreatic Cancer Group (2018) A web-based overview, systematic review and meta-analysis of pancreatic anastomosis techniques following pancreatoduodenectomy. HPB 20:777–785
Sun R, Yu J, Zhang Y, Liang Z, Han X (2021) Perioperative and oncological outcomes following minimally invasive versus open pancreaticoduodenectomy for pancreatic duct adenocarcinoma. Surg Endosc 35:2273–2285
Funding
The authors have not disclosed any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosures
Halit Topal, Joris Jaekers, Joachim Geers, and Baki Topal have no conflicts of interest or financial ties to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Topal, H., Jaekers, J., Geers, J. et al. Prospective cohort study on short-term outcomes of 3D-laparoscopic pancreaticoduodenectomy with stented pancreaticogastrostomy. Surg Endosc 37, 1203–1212 (2023). https://doi.org/10.1007/s00464-022-09609-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-022-09609-9