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Minimally invasive versus open pancreaticoduodenectomy for distal bile duct cancer: an inverse probability of treatment weighting analysis of outcomes

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Abstract

Background

Minimally invasive pancreaticoduodenectomy (MIPD) has been extended to periampullary cancers, but the oncologic outcome of MIPD for distal bile duct cancer (DBDC) has not been confirmed yet.

Methods

Patients who underwent pancreaticoduodenectomy (PD) for DBDC of stage I–IIb from 2015 to 2019 at a tertiary referral center were identified and divided into open PD (OPD) and MIPD groups, the latter including laparoscopic and robotic procedures. Survival was compared between the two groups after inverse probability of treatment weighting (IPTW) using predetermined factors, and exploratory mediation analysis was performed using surgery-derived outcomes.

Results

MIPD (n = 81) group had more female patients (46.9% vs 31.6%, p = 0.011) and longer operation time (366.2 min vs. 279.1 min, p < 0.001) than the OPD (n = 288) group before IPTW. Otherwise, intraoperative and immediate postoperative outcomes were comparable between the two groups. In oncologic outcomes, MIPD group showed comparable 3-year overall survival (78.2% vs 75.0%, p = 0.062) and recurrence-free survival (51.2% vs 53.4%, p = 0.871) rates with OPD group before IPTW, and MIPD was not related with survival (hazard ratio [HR] 0.61, 95% confidence interval [CI] 0.29–1.26, p = 0.18) and recurrence (HR 1.01, 95% CI 0.67–1.53, p = 0.949) after IPTW with consideration of potential mediators. Sensitivity analysis using propensity score matching also showed similar results for survival (HR 0.68, 95% CI 0.32–1.44, p = 0.312) and recurrence (HR 1.12, 95% CI 0.67–1.88, p = 0.653).

Conclusion

MIPD and OPD groups showed similar postoperative and oncologic outcomes. MIPD could be a considerable treatment option without oncological compromise in high-volume centers.

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References

  1. Rizvi S, Khan SA, Hallemeier CL, Kelley RK, Gores GJ (2018) Cholangiocarcinoma—evolving concepts and therapeutic strategies. Nat Rev Clin Oncol 15:95–111

    Article  CAS  PubMed  Google Scholar 

  2. Esnaola NF, Meyer JE, Karachristos A, Maranki JL, Camp ER, Denlinger CS (2016) Evaluation and management of intrahepatic and extrahepatic cholangiocarcinoma. Cancer 122:1349–1369

    Article  PubMed  Google Scholar 

  3. Zhou W, Qian L, Rong Y, Zhou Q, Shan J, Li P, Shi L, Liu H, Sun X (2020) Prognostic factors and patterns of recurrence after curative resection for patients with distal cholangiocarcinoma. Radiother Oncol 147:111–117

    Article  PubMed  Google Scholar 

  4. Yoo C, Shin SH, Park JO, Kim KP, Jeong JH, Ryoo BY, Lee W, Song KB, Hwang DW, Park JH, Lee JH (2021) Current status and future perspectives of perioperative therapy for resectable biliary tract cancer: a multidisciplinary review. Cancers (Basel) 13:1647

    Article  PubMed  Google Scholar 

  5. Lee W, Han HS, Yoon YS, Cho JY, Choi Y, Shin HK, Jang JY, Choi H (2015) Laparoscopic resection of hilar cholangiocarcinoma. Ann Surg Treat Res 89:228–232

    Article  PubMed  PubMed Central  Google Scholar 

  6. Levi Sandri GB, Spoletini G, Masciana G, Colasanti M, Lepiane P, Vennarecci G, D’Andrea V, Ettorre GM (2017) The role of minimally invasive surgery in the treatment of cholangiocarcinoma. Eur J Surg Oncol 43:1617–1621

    Article  CAS  PubMed  Google Scholar 

  7. Chapman BC, Gleisner A, Ibrahim-Zada I, Overbey DM, Paniccia A, Meguid C, Brauer B, Gajdos C, McCarter MD, Schulick RD, Edil BH (2018) Laparoscopic pancreaticoduodenectomy: changing the management of ampullary neoplasms. Surg Endosc 32:915–922

    Article  PubMed  Google Scholar 

  8. Del Chiaro M, Valente R, Arnelo U (2017) Minimally invasive pancreaticoduodenectomy for the treatment of pancreatic-head and periampullary tumors. JAMA Surg 152:343

    Article  PubMed  Google Scholar 

  9. Ban D, Nishino H, Ohtsuka T, Nagakawa Y, Abu Hilal M, Asbun HJ, Boggi U, Goh BKP, He J, Honda G, Jang JY, Kang CM, Kendrick ML, Kooby DA, Liu R, Nakamura Y, Nakata K, Palanivelu C, Shrikhande SV, Takaori K, Tang CN, Wang SE, Wolfgang CL, Yiengpruksawan A, Yoon YS, Ciria R, Berardi G, Garbarino GM, Higuchi R, Ikenaga N, Ishikawa Y, Kozono S, Maekawa A, Murase Y, Watanabe Y, Zimmitti G, Kunzler F, Wang ZZ, Sakuma L, Osakabe H, Takishita C, Endo I, Tanaka M, Yamaue H, Tanabe M, Wakabayashi G, Tsuchida A, Nakamura M (2021) International expert consensus on precision anatomy for minimally invasive distal pancreatectomy: PAM-HBP surgery project. J Hepatobiliary Pancreat Sci 29:161

    Article  PubMed  Google Scholar 

  10. Asbun HJ, Moekotte AL, Vissers FL, Kunzler F, Cipriani F, Alseidi A, D’Angelica MI, Balduzzi A, Bassi C, Bjornsson 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 S (2020) The Miami International Evidence-based Guidelines on Minimally Invasive Pancreas Resection. Ann Surg 271:1–14

    Article  PubMed  Google Scholar 

  11. Melamed A, Margul DJ, Chen L, Keating NL, Del Carmen MG, Yang J, Seagle BL, Alexander A, Barber EL, Rice LW, Wright JD, Kocherginsky M, Shahabi S, Rauh-Hain JA (2018) Survival after minimally invasive radical hysterectomy for early-stage cervical cancer. N Engl J Med 379:1905–1914

    Article  PubMed  PubMed Central  Google Scholar 

  12. Austin PC (2011) An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivar Behav Res 46:399–424

    Article  Google Scholar 

  13. Song KB, Kim SC, Lee W, Hwang DW, Lee JH, Kwon J, Park Y, Lee SJ, Park G (2020) Laparoscopic pancreaticoduodenectomy for periampullary tumors: lessons learned from 500 consecutive patients in a single center. Surg Endosc 34:1343–1352

    Article  PubMed  Google Scholar 

  14. Kim H, Choi SH, Jang JY, Choi M, Lee JH, Kang CM (2021) Multicenter comparison of totally laparoscopic and totally robotic pancreaticoduodenectomy: propensity score and learning curve-matching analyses. J Hepatobiliary Pancreat Sci 29:311

    Article  PubMed  Google Scholar 

  15. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes 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

    Article  PubMed  Google Scholar 

  16. 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, International Study Group on Pancreatic S (2017) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery 161:584–591

    Article  PubMed  Google Scholar 

  17. Nickel F, Haney CM, Kowalewski KF, Probst P, Limen EF, Kalkum E, Diener MK, Strobel O, Muller-Stich BP, Hackert T (2020) Laparoscopic versus open pancreaticoduodenectomy: a systematic review and meta-analysis of randomized controlled trials. Ann Surg 271:54–66

    Article  PubMed  Google Scholar 

  18. Song KB, Kim SC, Hwang DW, Lee JH, Lee DJ, Lee JW, Park KM, Lee YJ (2015) Matched case-control analysis comparing laparoscopic and open pylorus-preserving pancreaticoduodenectomy in patients with periampullary tumors. Ann Surg 262:146–155

    Article  PubMed  Google Scholar 

  19. Mazzola M, Giani A, Crippa J, Morini L, Zironda A, Bertoglio CL, De Martini P, Magistro C, Ferrari G (2021) Totally laparoscopic versus open pancreaticoduodenectomy: a propensity score matching analysis of short-term outcomes. Eur J Surg Oncol 47:674–680

    Article  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. Chen K, Liu XL, Pan Y, Maher H, Wang XF (2018) Expanding laparoscopic pancreaticoduodenectomy to pancreatic-head and periampullary malignancy: major findings based on systematic review and meta-analysis. BMC Gastroenterol 18:102

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kang CM, Lee WJ (2020) Is Laparoscopic pancreaticoduodenectomy feasible for pancreatic ductal adenocarcinoma? Cancers (Basel) 12:3430

    Article  PubMed  Google Scholar 

  23. 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 260:633–638 (discussion 638-640)

    Article  PubMed  Google Scholar 

  24. Choi M, Hwang HK, Rho SY, Lee WJ, Kang CM (2020) Comparing laparoscopic and open pancreaticoduodenectomy in patients with pancreatic head cancer: oncologic outcomes and inflammatory scores. J Hepatobiliary Pancreat Sci 27:124–131

    Article  PubMed  Google Scholar 

  25. Valle JW, Palmer D, Jackson R, Cox T, Neoptolemos JP, Ghaneh P, Rawcliffe CL, Bassi C, Stocken DD, Cunningham D, O’Reilly D, Goldstein D, Robinson BA, Karapetis C, Scarfe A, Lacaine F, Sand J, Izbicki JR, Mayerle J, Dervenis C, Olah A, Butturini G, Lind PA, Middleton MR, Anthoney A, Sumpter K, Carter R, Buchler MW (2014) Optimal duration and timing of adjuvant chemotherapy after definitive surgery for ductal adenocarcinoma of the pancreas: ongoing lessons from the ESPAC-3 study. J Clin Oncol 32:504–512

    Article  PubMed  Google Scholar 

  26. Lee W, Yoon YS, Han HS, Jang JY, Cho JY, Jung W, Kwon W, Choi Y, Kim SW (2017) Prognostic relevance of the timing of initiating and the completion of adjuvant therapy in patients with resected pancreatic ductal adenocarcinoma. World J Surg 41:562–573

    Article  PubMed  Google Scholar 

  27. Choe JW, Kim HJ, Kim JS (2020) Survival improvement and prognostic factors in recent management of extrahepatic cholangiocarcinoma: a single-center study. Hepatobiliary Pancreat Dis Int 19:153–156

    Article  PubMed  Google Scholar 

  28. Park Y, Hwang DW, Kim JH, Hong SM, Jun SY, Lee JH, Song KB, Jun ES, Kim SC, Park KM (2019) Prognostic comparison of the longitudinal margin status in distal bile duct cancer: R0 on first bile duct resection versus R0 after additional resection. J Hepatobiliary Pancreat Sci 26:169–178

    Article  PubMed  Google Scholar 

  29. Benedetto U, Head SJ, Angelini GD, Blackstone EH (2018) Statistical primer: propensity score matching and its alternatives. Eur J Cardiothorac Surg 53:1112–1117

    Article  PubMed  Google Scholar 

  30. Benedetto U, Puskas J, Kappetein AP, Brown WM 3rd, Horkay F, Boonstra PW, Bogats G, Noiseux N, Dressler O, Angelini GD, Stone GW, Serruys PW, Sabik JF, Taggart DP (2019) Off-pump versus on-pump bypass surgery for left main coronary artery disease. J Am College Cardiol 74:729–740

    Article  Google Scholar 

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Correspondence to Song Cheol Kim.

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Woohyung Lee, Ki Byung Song, Sarang Hong, Yejong Park, Bong Jun Kwak, Eunsung Jun, Dae Wook Hwang, Sehee Kim, Jae Hoon Lee, and Song Cheol Kim have no conflict of interest or financial ties to declare.

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Lee, W., Song, K.B., Hong, S. et al. Minimally invasive versus open pancreaticoduodenectomy for distal bile duct cancer: an inverse probability of treatment weighting analysis of outcomes. Surg Endosc 37, 881–890 (2023). https://doi.org/10.1007/s00464-022-09533-y

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