Abstract
Background
Pancreatoduodenectomy is the only potentially curative treatment for distal cholangiocarcinoma (DCC). In this study, we sought to compare the perioperative and oncological outcomes of robotic pancreaticoduodenectomy (RPD) and open pancreaticoduodenectomy (OPD) based on a multicenter propensity score-matched study.
Methods
Consecutive patients with DCC who underwent RPD or OPD from five centers in China between January 2014 and June 2019 were included. A 1:1 propensity score matching (PSM) was performed. Univariable and multivariable Cox regression analyses were used to identify independent prognosis factors for overall survival (OS) and recurrence-free survival (RFS) of these patients.
Results
A total of 217 patients and 228 patients underwent RPD and OPD, respectively. After PSM, 180 patients in each group were enrolled. There were no significant differences in operative time, lymph node harvest, intraoperative transfusion, vascular resection, R0 resection, postoperative major morbidity, reoperation, 90-day mortality, and long-term survival between the two groups before and after PSM. Whereas, compared with the OPD group, the RPD group had significantly lower estimated blood loss (150.0 ml vs. 250.0 ml; P < 0.001), and a shorter postoperative length of stay (LOS) (12.0 days vs. 15.0 days; P < 0.001). Multivariable analysis showed carbohydrate antigen 19-9 (CA19-9), R0 resection, N stage, perineural invasion, and tumor differentiation significantly associated with OS and RFS of these patients.
Conclusions
RPD was comparable to OPD in feasibility and safety. For patients with DCC, RPD resulted in similar oncologic and survival outcomes as OPD.
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Data availability
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
References
Amin M, Greene F, Edge S, Compton C, Gershenwald J, Brookland R, Meyer L, Gress D, Byrd D, Winchester D (2017) The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin 67:93–99
Lopez-Aguiar A, Ethun C, Pawlik T, Tran T, Poultsides G, Isom C, Idrees K, Krasnick B, Fields R, Salem A, Weber S, Martin R, Scoggins C, Shen P, Mogal H, Beal E, Schmidt C, Shenoy R, Hatzaras I, Maithel S (2019) Association of perioperative transfusion with recurrence and survival after resection of distal cholangiocarcinoma: a 10-Institution Study from the US Extrahepatic Biliary Malignancy Consortium. Ann Surg Oncol 26:1814–1823
Strijker M, Belkouz A, van der Geest L, van Gulik T, van Hooft J, de Meijer V, Haj Mohammad N, de Reuver P, Verheij J, de Vos-Geelen J, Wilmink J, Groot Koerkamp B, Klümpen H, Besselink M (2019) Treatment and survival of resected and unresected distal cholangiocarcinoma: a nationwide study. Acta Oncol (Stockholm, Sweden) 58:1048–1055
Liu Q, Zhao Z, Zhang X, Wang W, Han B, Chen X, Tan X, Xu S, Zhao G, Gao Y, Gan Q, Yuan J, Ma Y, Dong Y, Liu Z, Wang H, Fan F, Liu J, Lau WY, Liu R (2021) Perioperative and oncological outcomes of robotic versus open pancreaticoduodenectomy in low-risk surgical candidates: a multicenter propensity score-matched study. Ann Surg. https://doi.org/10.1097/SLA.0000000000005160
Hata T, Motoi F, Ishida M, Naitoh T, Katayose Y, Egawa S, Unno M (2016) Effect of hospital volume on surgical outcomes after pancreaticoduodenectomy: a systematic review and meta-analysis. Ann Surg 263:664–672
Kimura W, Miyata H, Gotoh M, Hirai I, Kenjo A, Kitagawa Y, Shimada M, Baba H, Tomita N, Nakagoe T, Sugihara K, Mori M (2014) A pancreaticoduodenectomy risk model derived from 8575 cases from a national single-race population (Japanese) using a web-based data entry system: the 30-day and in-hospital mortality rates for pancreaticoduodenectomy. Ann Surg 259:773–780
Zhang T, Zhao Z-M, Gao Y-X, Lau WY, Liu R (2019) The learning curve for a surgeon in robot-assisted laparoscopic pancreaticoduodenectomy: a retrospective study in a high-volume pancreatic center. Surg Endosc 33:2927–2933
Liu R, Zhang T, Zhao Z-M, Tan X-L, Zhao G-D, Zhang X, Xu Y (2017) The surgical outcomes of robot-assisted laparoscopic pancreaticoduodenectomy versus laparoscopic pancreaticoduodenectomy for periampullary neoplasms: a comparative study of a single center. Surg Endosc 31:2380–2386
Baker EH, Ross SW, Seshadri R, Swan RZ, Iannitti DA, Vrochides D, Martinie JB (2015) Robotic pancreaticoduodenectomy for pancreatic adenocarcinoma: role in 2014 and beyond. J Gastrointest Oncol 6:396–405
Giulianotti PC, Coratti A, Angelini M, Sbrana F, Cecconi S, Balestracci T, Caravaglios G (2003) Robotics in general surgery: personal experience in a large community hospital. Arch Surg (Chicago) 138:777–784
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
Liu R, Wakabayashi G, Palanivelu C, Tsung A, Yang K, Goh BKP, Chong CC-N, Kang CM, Peng C, Kakiashvili E, Han H-S, Kim H-J, He J, Lee JH, Takaori K, Marino MV, Wang S-N, Guo T, Hackert T, Huang T-S, Anusak Y, Fong Y, Nagakawa Y, Shyr Y-M, Wu Y-M, Zhao Y (2019) International consensus statement on robotic pancreatic surgery. Hepatobil Surg Nutr 8:345–360
Podda M, Gerardi C, Di Saverio S, Marino MV, Davies RJ, Pellino G, Pisanu A (2020) Robotic-assisted versus open pancreaticoduodenectomy for patients with benign and malignant periampullary disease: a systematic review and meta-analysis of short-term outcomes. Surg Endosc 34:2390–2409
Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250:187–196
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 (2017) 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, 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
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 J-N, 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. Surgery 149:680–688
Chen Z, Yu B, Bai J, Li Q, Xu B, Dong Z, Zhi X, Li T (2021) The impact of intraoperative frozen section on resection margin status and survival of patients underwent pancreatoduodenectomy for distal cholangiocarcinoma. Front Oncol 11:650585
Chun YS, Pawlik TM, Vauthey J-N (2018) 8th Edition of the AJCC cancer staging manual: pancreas and hepatobiliary cancers. Ann Surg Oncol 25:845–847
Liu Q, Zhao Z, Gao Y, Zhao G, Tan X, Wang C, Liu R (2020) Novel single-layer continuous suture of pancreaticojejunostomy for robotic pancreaticoduodenectomy. J Hepato-Bil-Pan Sci 27:56–63
Wang C-Y, Huang T-S, Zhang K-D, Wang Z-Z, Wang F, Zhao Z-M, Gao Y-X, Liu R (2019) Retrocolic versus antecolic gastrointestinal reconstruction in robotic pancreaticoduodenectomy. J Hepato-Bil-Pan Sci 26:517–523
Razumilava N, Gores G (2014) Cholangiocarcinoma. Lancet (London, England) 383:2168–2179
Xu S, Zhang X, Zhao G, Zhao Z, Gao Y, Hu M, Tan X, Liu R (2021) Development and validation of an online calculator to predict early recurrence and long-term survival in patients with distal cholangiocarcinoma after pancreaticoduodenectomy. J Hepato-Bil-Pan Sci. https://doi.org/10.1002/jhbp.1058
Kim HS, Han Y, Kang JS, Kim H, Kim JR, Kwon W, Kim S-W, Jang J-Y (2018) Comparison of surgical outcomes between open and robot-assisted minimally invasive pancreaticoduodenectomy. J Hepato-Bil-Pan Sci 25:142–149
Zureikat AH, Postlewait LM, Liu Y, Gillespie TW, Weber SM, Abbott DE, Ahmad SA, Maithel SK, Hogg ME, Zenati M, Cho CS, Salem A, Xia B, Steve J, Nguyen TK, Keshava HB, Chalikonda S, Walsh RM, Talamonti MS, Stocker SJ, Bentrem DJ, Lumpkin S, Kim HJ, Zeh HJ, Kooby DA (2016) A multi-institutional comparison of perioperative outcomes of robotic and open pancreaticoduodenectomy. Ann Surg 264:640–649
Giulianotti PC, Addeo P, Buchs NC, Ayloo SM, Bianco FM (2011) Robotic extended pancreatectomy with vascular resection for locally advanced pancreatic tumors. Pancreas 40:1264–1270
Wang S-E, Shyr B-U, Chen S-C, Shyr Y-M (2018) Comparison between robotic and open pancreaticoduodenectomy with modified Blumgart pancreaticojejunostomy: a propensity score-matched study. Surgery 164:1162–1167
Allan BJ, Novak SM, Hogg ME, Zeh HJ (2018) Robotic vascular resections during Whipple procedure. J Vis Surg 4:13
Xu S, Zhang X, Zhao G, Zou W, Zhao Z, Hu M, Gao Y, Tan X, Liu Q, Liu R (2021) A novel online calculator to predict recurrence risk in patients with distal cholangiocarcinoma after radical pancreaticoduodenectomy. J Surg Oncol 125:377
Mantel H, Wiggers J, Verheij J, Doff J, Sieders E, van Gulik T, Gouw A, Porte R (2015) Lymph node micrometastases are associated with worse survival in patients with otherwise node-negative hilar cholangiocarcinoma. Ann Surg Oncol 22:1107–1115
Komaya K, Ebata T, Shirai K, Ohira S, Morofuji N, Akutagawa A, Yamaguchi R, Nagino M (2017) Recurrence after resection with curative intent for distal cholangiocarcinoma. Br J Surg 104:426–433
Yonemura K, Kajiwara Y, Ao T, Mochizuki S, Shinto E, Okamoto K, Hase K, Ueno H (2019) Prognostic value of poorly differentiated clusters in liver metastatic lesions of colorectal carcinoma. Am J Surg Pathol 43:1341–1348
Lamarca A, Edeline J, McNamara MG, Hubner RA, Nagino M, Bridgewater J, Primrose J, Valle JW (2020) Current standards and future perspectives in adjuvant treatment for biliary tract cancers. Cancer Treat Rev 84:101936
Di Franco G, Lorenzoni V, Palmeri M, Furbetta N, Guadagni S, Gianardi D, Bianchini M, Pollina LE, Melfi F, Mamone D, Milli C, Di Candio G, Turchetti G, Morelli L (2021) Robot-assisted pancreatoduodenectomy with the: can the costs of advanced technology be offset by clinical advantages? A case-matched cost analysis versus open approach. Surg Endosc. https://doi.org/10.1007/s00464-021-08793-4
Kowalsky SJ, Zenati MS, Steve J, Esper SA, Lee KK, Hogg ME, Zeh HJ, Zureikat AH (2019) A combination of robotic approach and ERAS pathway optimizes outcomes and cost for pancreatoduodenectomy. Ann Surg 269:1138–1145
Nabi J, Friedlander DF, Chen X, Cole AP, Hu JC, Kibel AS, Dasgupta P, Trinh Q-D (2020) Assessment of out-of-pocket costs for robotic cancer surgery in US adults. JAMA Netw Open 3:e1919185
Acknowledgements
We would like to sincerely thank the Chinese Alliance of Hepato-Biliary-Pancreatic Surgery, including Bing Han, from Department of Hepatobiliary and Pancreatic Surgery, The Affiliated Hospital of Qingdao University, Qingdao, Shandong, China; Jian-Lei Yuan, from Department of Hepatobiliary and Pancreatic Surgery, People Hospital of Cangzhou city, Cangzhou, Hebei, China; Wei Wang, from the Department of General Surgery, The First Affiliated Hospital of Jinzhou Medical University, Jinzhou, Liaoning, China; and Jia-Ning Liu, from Department of Thyroid and Pancreatic Surgery, The Second Hospital of Shandong University, Jinan, Shandong, China, for their valuable data.
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Conception and design: RL, SX, X-PZ, G-DZ; Provision of study materials or patients: Z-MZ, G-DZ, M-GH, Y-XG, X-LT, QL; Collection and assembly of data: SX, X-PZ, W-BZ; Data analysis and interpretation: SX, X-PZ, W-BZ; Manuscript writing: SX, X-PZ, G-DZ; Final approval of manuscript: All authors. Financial support: RL.
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Dr. Shuai Xu, Xiu-Ping Zhang, Guo-Dong Zhao, Wen-Bo Zou, Zhi-Ming Zhao, Ming-Gen Hu, Yuan-Xing Gao, Xiang-Long Tan, Qu Liu, and Rong Liu have no conflicts of interest or financial ties to disclose.
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This study was approved by the Ethics Committee of the five hospitals (S2020-252-09).
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Xu, S., Zhang, XP., Zhao, GD. et al. Robotic versus open pancreaticoduodenectomy for distal cholangiocarcinoma: a multicenter propensity score-matched study. Surg Endosc 36, 8237–8248 (2022). https://doi.org/10.1007/s00464-022-09271-1
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DOI: https://doi.org/10.1007/s00464-022-09271-1