Journal of Gastrointestinal Surgery

, Volume 22, Issue 4, pp 661–667 | Cite as

Clinical Factors and Postoperative Impact of Bile Leak After Liver Resection

  • Allison N. Martin
  • Sowmya Narayanan
  • Florence E. Turrentine
  • Todd W. Bauer
  • Reid B. Adams
  • George J. Stukenborg
  • Victor M. Zaydfudim
Original Article



Despite technical advances, bile leak remains a significant complication after hepatectomy. The current study uses a targeted multi-institutional dataset to characterize perioperative factors that are associated with bile leakage after hepatectomy to better understand the impact of bile leak on morbidity and mortality.


Adult patients in the 2014–2015 ACS NSQIP targeted hepatectomy dataset were linked to the ACS NSQIP PUF dataset. Bivariable and multivariable regression analyses were used to assess the associations between clinical factors and post-hepatectomy bile leak.


Of 6859 patients, 530 (7.7%) had a postoperative bile leak. Proportion of bile leaks was significantly greater in patients after major compared to minor hepatectomy (12.6 vs. 5.1%, p < 0.001). The proportion of patients with bile leak was significantly greater in patients after major hepatectomy who had concomitant enterohepatic reconstruction (31.8 vs. 10.1%, p < 0.001). Postoperative mortality was significantly greater in patients with bile leaks (6.0 vs. 1.7%, p < 0.001). After adjusting for significant covariates, bile leak was independently associated with increased risk of postoperative morbidity (OR = 4.55; 95% CI 3.72–5.56; p < 0.001). After adjusting for significant effects of postoperative complications, liver failure, and reoperation (all p<0.001), bile leak was not independently associated with increased risk of postoperative mortality (p = 0.262).


Major hepatectomy and enterohepatic biliary reconstruction are associated with significantly greater rates of bile leak after liver resection. Bile leak is independently associated with significant postoperative morbidity. Mitigation of bile leak is critical in reducing morbidity and mortality after liver resection.


Bile leak Hepatectomy Liver resection Major hepatectomy Biliary complication Drain Morbidity and mortality 



The American College of Surgeons National Surgical Quality Improvement Program and the hospitals participating in the ACS NSQIP are the source of the data used herein; they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the authors. This study was supported in part by funding support provided by the Institutional National Research Service Award T32 CA 163177 from the National Cancer Institute to ANM and Loan Repayment Program Award 1 L30 CA220861-01 from the National Cancer Institute to VMZ.

Author Contribution

Category 1

Conception and design of study: Martin, Stukenborg, Zaydfudim.

Acquisition of data: Martin, Narayanan, Turrentine.

Analysis and/or interpretation of data: Martin, Narayanan, Turrentine, Bauer, Adams, Stukenborg, Zaydfudim.

Category 2

Drafting the manuscript: Martin, Narayanan, Turrentine.

Revising the manuscript critically for important intellectual content: Bauer, Adams, Stukenborg, Zaydfudim.

Category 3

Final approval of the version of the manuscript to be published: Martin, Narayanan, Turrentine, Bauer, Adams, Zaydfudim.

G. Stukenborg significantly contributed to the entire project including manuscript composition and revision prior to his sudden and untimely death at the end of Summer 2017.

Category 4

Agreement to be accountable for all aspects of the work: Martin, Narayanan, Turrentine, Bauer, Adams, Stukenborg (posthumously), Zaydfudim.


This study was supported in part by funding support provided by the Institutional National Research Service Award T32 CA 163177 from the National Cancer Institute to ANM and Loan Repayment Program Award 1 L30 CA220861–01 from the National Cancer Institute to VMZ.

Compliance with Ethical Standards


Nothing to disclose.


  1. 1.
    Dimick JB, Wainess RM, Cowan JA, Upchurch GR, Jr., Knol JA, Colletti LM. National trends in the use and outcomes of hepatic resection. J Am Coll Surg. 2004;199(1):31–8. doi: PubMed
  2. 2.
    Foster JH, Berman MM. Solid liver tumors. Major Probl Clin Surg. 1977;22:1–342. PubMedGoogle Scholar
  3. 3.
    Jarnagin WR, Gonen M, Fong Y, DeMatteo RP, Ben-Porat L, Little S, et al. Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg. 2002;236(4):397–406; discussion −7. doi: PubMed PMID: 12368667; PubMed Central PMCID: PMCPMC1422593.
  4. 4.
    Yokoo H, Miyata H, Konno H, Taketomi A, Kakisaka T, Hirahara N, et al. Models predicting the risks of six life-threatening morbidities and bile leakage in 14,970 hepatectomy patients registered in the National Clinical Database of Japan. Medicine (Baltimore). 2016;95(49):e5466. doi: PubMed PMID: 27930526; PubMed Central PMCID: PMCPMC5265998.
  5. 5.
    Zimmitti G, Vauthey JN, Shindoh J, Tzeng CW, Roses RE, Ribero D, et al. Systematic use of an intraoperative air leak test at the time of major liver resection reduces the rate of postoperative biliary complications. J Am Coll Surg. 2013;217(6):1028–37. doi: PubMed PMID: 24246619; PubMed Central PMCID: PMCPMC3880182.
  6. 6.
    Brauer DG, Nywening TM, Jaques DP, Doyle MB, Chapman WC, Fields RC, et al. Operative Site Drainage after Hepatectomy: A Propensity Score Matched Analysis Using the American College of Surgeons NSQIP Targeted Hepatectomy Database. J Am Coll Surg. 2016;223(6):774–83 e2. doi: PubMed PMID: 27793459; PubMed Central PMCID: PMCPMC5125822.
  7. 7.
    Spolverato G, Ejaz A, Kim Y, Hall BL, Bilimoria K, Cohen M, et al. Patterns of care among patients undergoing hepatic resection: a query of the National Surgical Quality Improvement Program-targeted hepatectomy database. J Surg Res. 2015;196(2):221–8. doi: PubMed
  8. 8.
    Alexiou VG, Tsitsias T, Mavros MN, Robertson GS, Pawlik TM. Technology-assisted versus clamp-crush liver resection: a systematic review and meta-analysis. Surg Innov. 2013;20(4):414–28. doi: PubMed
  9. 9.
    Kaibori M, Ishizaki M, Matsui K, Kwon AH. Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery. 2011;150(1):91–8. doi: PubMed
  10. 10.
    Lam CM, Lo CM, Liu CL, Fan ST. Biliary complications during liver resection. World J Surg. 2001;25(10):1273–6. PubMedGoogle Scholar
  11. 11.
    Zimmitti G, Roses RE, Andreou A, Shindoh J, Curley SA, Aloia TA, et al. Greater complexity of liver surgery is not associated with an increased incidence of liver-related complications except for bile leak: an experience with 2,628 consecutive resections. J Gastrointest Surg. 2013;17(1):57–64; discussion p −5. doi: PubMed PMID: 22956403; PubMed Central PMCID: PMCPMC3855461.
  12. 12.
    Okumura K, Sugimachi K, Kinjo N, Shoji F, Ikebe M, Makino I, et al. Risk factors of bile leakage after hepatectomy for hepatocellular carcinoma. Hepatogastroenterology. 2013;60(127):1717–9. PubMedGoogle Scholar
  13. 13.
    Sadamori H, Yagi T, Shinoura S, Umeda Y, Yoshida R, Satoh D, et al. Risk factors for major morbidity after liver resection for hepatocellular carcinoma. Br J Surg. 2013;100(1):122–9. doi: PubMed
  14. 14.
    Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, et al. Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery. 2011;149(5):680–8. doi: PubMed
  15. 15.
    Wiggers JK, Groot Koerkamp B, Cieslak KP, Doussot A, van Klaveren D, Allen PJ, et al. Postoperative Mortality after Liver Resection for Perihilar Cholangiocarcinoma: Development of a Risk Score and Importance of Biliary Drainage of the Future Liver Remnant. J Am Coll Surg. 2016;223(2):321–31 e1. doi: PubMed PMID: 27063572; PubMed Central PMCID: PMCPMC4961586.
  16. 16.
    Zaydfudim VM, Rosen CB, Nagorney DM. Hilar cholangiocarcinoma. Surg Oncol Clin N Am. 2014;23(2):247–63. doi: PubMed
  17. 17.
    Shubert CR, Habermann EB, Truty MJ, Thomsen KM, Kendrick ML, Nagorney DM. Defining perioperative risk after hepatectomy based on diagnosis and extent of resection. J Gastrointest Surg. 2014;18(11):1917–28. doi: PubMed
  18. 18.
    Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg. 2009;250(5):831–41. doi: PubMed
  19. 19.
    Mehta VV, Fisher SB, Maithel SK, Sarmiento JM, Staley CA, Kooby DA. Is it time to abandon routine operative drain use? A single institution assessment of 709 consecutive pancreaticoduodenectomies. J Am Coll Surg. 2013;216(4):635–42; discussion 42-4. doi: PubMed
  20. 20.
    van der Wilt AA, Coolsen MM, de Hingh IH, van der Wilt GJ, Groenewoud H, Dejong CH, et al. To drain or not to drain: a cumulative meta-analysis of the use of routine abdominal drains after pancreatic resection. HPB (Oxford). 2013;15(5):337–44. doi: PubMed PMID: 23557407; PubMed Central PMCID: PMCPMC3633034.
  21. 21.
    Van Buren G, 2nd, Bloomston M, Hughes SJ, Winter J, Behrman SW, Zyromski NJ, et al. A randomized prospective multicenter trial of pancreaticoduodenectomy with and without routine intraperitoneal drainage. Ann Surg. 2014;259(4):605–12. doi: PubMed
  22. 22.
    Ferrero A, Russolillo N, Vigano L, Sgotto E, Lo Tesoriere R, Amisano M, et al. Safety of conservative management of bile leakage after hepatectomy with biliary reconstruction. J Gastrointest Surg. 2008;12(12):2204–11. doi: PubMed
  23. 23.
    Vigano L, Ferrero A, Sgotto E, Tesoriere RL, Calgaro M, Capussotti L. Bile leak after hepatectomy: predictive factors of spontaneous healing. Am J Surg. 2008;196(2):195–200. doi: PubMed
  24. 24.
    Lo CM, Fan ST, Liu CL, Lai EC, Wong J. Biliary complications after hepatic resection: risk factors, management, and outcome. Arch Surg. 1998;133(2):156–61. PubMedGoogle Scholar
  25. 25.
    Li SQ, Liang LJ, Peng BG, Lu MD, Lai JM, Li DM. Bile leakage after hepatectomy for hepatolithiasis: risk factors and management. Surgery. 2007;141(3):340–5. doi: PubMed
  26. 26.
    Capussotti L, Ferrero A, Vigano L, Sgotto E, Muratore A, Polastri R. Bile leakage and liver resection: Where is the risk? Arch Surg. 2006;141(7):690–4; discussion 5. doi: PubMed
  27. 27.
    Kubo S, Sakai K, Kinoshita H, Hirohashi K. Intraoperative cholangiography using a balloon catheter in liver surgery. World J Surg. 1986;10(5):844–50. PubMedGoogle Scholar
  28. 28.
    Yamashita Y, Hamatsu T, Rikimaru T, Tanaka S, Shirabe K, Shimada M, et al. Bile leakage after hepatic resection. Ann Surg. 2001;233(1):45–50. PubMed PMID: 11141224; PubMed Central PMCID: PMCPMC1421165.Google Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2017

Authors and Affiliations

  • Allison N. Martin
    • 1
  • Sowmya Narayanan
    • 1
  • Florence E. Turrentine
    • 1
    • 2
  • Todd W. Bauer
    • 1
    • 3
  • Reid B. Adams
    • 1
    • 3
  • George J. Stukenborg
    • 1
    • 2
  • Victor M. Zaydfudim
    • 1
    • 2
    • 3
  1. 1.Department of SurgeryUniversity of VirginiaCharlottesvilleUSA
  2. 2.Surgical Outcomes Research CenterUniversity of VirginiaCharlottesvilleUSA
  3. 3.Section of Hepatobiliary and Pancreatic SurgeryUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations