Abstract
Purpose
Pancreatoduodenectomy is the most common operative procedure performed for distal bile duct carcinoma. Data on outcome after surgery for this rare malignancy is scarce, especially from western countries. The purpose of this study is to explore the prognostic factors and outcome after pancreatoduodenectomy for distal bile duct carcinoma.
Methods
Patients receiving pancreatoduodenectomy for distal bile duct carcinoma were identified from institutional databases of five German and one Russian academic centers for pancreatic surgery. Univariable and multivariable general linear model, Kaplan-Meier method, and Cox regression were used to identify prognostic factors for postoperative mortality and overall survival.
Results
N = 228 patients operated from 1994 to 2015 were included. Reoperation (OR 5.38, 95%CI 1.51–19.22, p = 0.010), grade B/C postpancreatectomy hemorrhage (OR 3.73, 95%CI 1.13–12.35, p = 0.031), grade B/C postoperative pancreatic fistula (OR 4.29, 95%CI 1.25–14.72, p = 0.038), and advanced age (OR 4.00, 95%CI 1.12–14.03, p = 0.033) were independent risk factors for in-hospital mortality in multivariable analysis. Median survival was 29 months, 5-year survival 27%. Positive resection margin (HR 2.07, 95%CI 1.29–3.33, p = 0.003), high tumor grade (HR 1.71, 95%CI 1.13–2.58, p = 0.010), lymph node (HR 1.68, 95%CI 1.13–2.51, p = 0.011), and distant metastases (HR 2.70, 95%CI 1.21–5.58, p = 0.014), as well as severe non-fatal postoperative complications (HR 1.64, 95%CI 1.04–2.58, p = 0.033) were independent negative prognostic factors for survival in multivariable analysis.
Conclusion
Distant metastases and positive resection margin are the strongest negative prognostic factors for survival after pancreatoduodenectomy for distal bile duct carcinoma; thus, surgery with curative intent is only warranted in patients with local disease, where R0 resection is feasible.
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References
Bosman FT, Carneiro F, Hruban RH et al (2010) WHO classification of tumors of the digestive system, 4th edn. International Agency for Research in Cancer, Lyon
Cardinale V, Semeraro R, Torrice A et al (2010) Intra-hepatic and extra-hepatic cholangiocarcinoma: new insight into epidemiology and risk factors. World J Gastrointest Oncol 2:407–416
Nakeeb A, Pitt HA, Sohn TA et al (1996) Cholangiocarcinoma. A spectrum of intrahepatic, perihilar, and distal tumors. Ann Surg 224:463–475
Schmuck RB, de Carvalho-Fischer CV, Neumann C et al (2016) Distal bile duct carcinomas and pancreatic ductal adenocarcinomas: postulating a common tumor entity. Cancer Med 5:88–99
Wellner UF, Shen Y, Keck T et al (2016) The survival outcome and prognostic factors for distal cholangiocarcinoma following surgical resection: a meta-analysis for the 5-year survival. Surg Today 47:271–279
Ferrone CR, Pieretti-Vanmarcke R, Bloom JP et al (2012) Pancreatic ductal adenocarcinoma: long-term survival does not equal cure. Surgery 152:S43–S49
Valle J, Wasan H, Palmer DH et al (2010) Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med 362:1273–1281
Kulke MH, Tempero MA, Niedzwiecki D et al (2009) Randomized phase II study of gemcitabine administered at a fixed dose rate or in combination with cisplatin, docetaxel, or irinotecan in patients with metastatic pancreatic cancer: CALGB 89904. J Clin Oncol Off J Am Soc Clin Oncol 27:5506–5512
Bartoli FG, Arnone GB, Ravera G et al (1991) Pancreatic fistula and relative mortality in malignant disease after pancreaticoduodenectomy. Review and statistical meta-analysis regarding 15 years of literature. Anticancer Res 11:1831–1848
Wellner UF, Kayser G, Lapshyn H et al (2010) A simple scoring system based on clinical factors related to pancreatic texture predicts postoperative pancreatic fistula preoperatively. HPB 12:696–702
Bassi C, Dervenis C, Butturini G et al (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13
Wente MN, Bassi C, Dervenis C et al (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142:761–768
Wente MN, Veit JA, Bassi C et al (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142:20–25
Rezvan PH, Lee KJ, Simpson JA (2015) The rise of multiple imputation: a review of the reporting and implementation of the method in medical research. BMC Med Res Methodol 15:30
National Cancer Institute, Common Terminology Criteria for Adverse Events v4.0, NCI, NIH, DHHS. May 29, 2009, NIH publication # 09-7473
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46
DeOliveira ML, Cunningham SC, Cameron JL et al (2007) Cholangiocarcinoma: thirty-one-year experience with 564 patients at a single institution. Ann Surg 245:755–762
Murakami Y, Uemura K, Sudo T et al (2011) Prognostic factors after surgical resection for intrahepatic, hilar, and distal cholangiocarcinoma. Ann Surg Oncol 18:651–658
Kiriyama M, Ebata T, Aoba T et al (2015) Prognostic impact of lymph node metastasis in distal cholangiocarcinoma. Br J Surg. 102:399–406
Choi SB, Park SW, Kim KS et al (2009) The survival outcome and prognostic factors for middle and distal bile duct cancer following surgical resection. J Surg Oncol 99:335–342
Qiao Q-L, Zhang T-P, Guo J-C et al (2011) Prognostic factors after pancreatoduodenectomy for distal bile duct cancer. Am Surg 77:1445–1448
Hernandez J, Cowgill SM, Al-Saadi S et al (2008) An aggressive approach to extrahepatic cholangiocarcinomas is warranted: margin status does not impact survival after resection. Ann Surg Oncol 15:807–814
Cheng Q, Luo X, Zhang B et al (2007) Distal bile duct carcinoma: prognostic factors after curative surgery. A series of 112 cases. Ann Surg Oncol 14:1212–1219
Verbeke CS, Gladhaug IP (2012) Resection margin involvement and tumour origin in pancreatic head cancer. Br J Surg 99:1036–1049
Hong S-M, Pawlik TM, Cho H et al (2009) Depth of tumor invasion better predicts prognosis than the current American Joint Committee on Cancer T classification for distal bile duct carcinoma. Surgery 146:250–257
Moon A, Choi DW, Choi SH et al (2015) Validation of T stage according to depth of invasion and N stage subclassification based on number of metastatic lymph nodes for distal extrahepatic bile duct (EBD) carcinoma. Medicine (Baltimore) 94:e2064
Wiltberger G, Krenzien F, Benzing C et al (2016) Prognostic accuracy of the seventh edition of the TNM classification compared with the fifth and sixth edition for distal cholangiocarcinoma. Ann Surg Oncol 23:1320–1326
Kim HJ, Kim CY, Hur YH et al (2014) Prognostic factors for survival after curative resection of distal cholangiocarcinoma: perineural invasion and lymphovascular invasion. Surg Today 44:1879–1886
Addeo P, Delpero JR, Paye F et al (2014) Pancreatic fistula after a pancreaticoduodenectomy for ductal adenocarcinoma and its association with morbidity: a multicentre study of the French Surgical Association. HPB 16:46–55
Distler M, Rückert F, Hunger M et al (2013) Evaluation of survival in patients after pancreatic head resection for ductal adenocarcinoma. BMC Surg 13:12
Courtin-Tanguy L, Rayar M, Bergeat D et al (2016) The true prognosis of resected distal cholangiocarcinoma. J Surg Oncol 113:575–580
Kawai M, Murakami Y, Motoi F et al (2016) Grade B pancreatic fistulas do not affect survival after pancreatectomy for pancreatic cancer: a multicenter observational study. Surgery 160(2):293–305
Tol JA, Gouma DJ, Bassi C et al (2014) Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS). Surgery 156(3):591–600
Petrucciani N, Nigri G, Debs T et al (2016) Frozen section analysis of the pancreatic margin during pancreaticoduodenectomy for cancer: does extending the resection to obtain a secondary R0 provide a survival benefit? Results of a systematic review. Pancreatology 16(6):1037–1043
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Contributions
Study conception and design: Felix Rückert, Ulrich Wellner, Gabriel Seifert, Ekaterina Petrova. Acquisition of data: Sebastian Zach, Jürgen Weitz, Robert Grützmann, Uwe Wittel, Frank Makowiec, Ulrich Hopt, Peter Bronsert, Florian Kühn, Bettina M. Rau, Roman Izrailov, Igor Khatkov, Hryhoriy Lapshyn, Dirk Bausch. Analysis and interpretation of data: Ekaterina Petrova, Ulrich Wellner, Louisa Bolm, Gabriel Seifert, YinFen Shen, Tobias Keck. Drafting of manuscript: Ekaterina Petrova, YinFen Shen. Critical revision of manuscript: Ekaterina Petrova, Felix Rückert, Sebastian Zach, YinFeng Shen, Jürgen Weitz, Robert Grützmann, Uwe Wittel, Frank Makowiec, Ulrich Hopt, Peter Bronsert, Florian Kühn, Bettina M. Rau, Roman Izrailov, Igor Khatkov, Hryhoriy Lapshyn, Louisa Bolm, Dirk Bausch, Tobias Keck, Ulrich F. Wellner, Gabriel Seifert.
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Funding
This study was supported by the German Research Foundation (DFG WE5085/1-1), Scientific Research Fund from Hubei University of Chinese Medicine, Education Project of Medical Talents for Young and Middle-aged in Wuhan City (Grant No. Q2014037), and Young Talents Project of Science and Technology Research Program from Hubei Provincial Department of Education (Grant No. Q20132003).
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Approval for the study was obtained from the institutional ethics committee of the University of Lübeck (Ref 14-037A). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.
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Petrova, E., Rückert, F., Zach, S. et al. Survival outcome and prognostic factors after pancreatoduodenectomy for distal bile duct carcinoma: a retrospective multicenter study. Langenbecks Arch Surg 402, 831–840 (2017). https://doi.org/10.1007/s00423-017-1590-9
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DOI: https://doi.org/10.1007/s00423-017-1590-9