Revista do Colégio Brasileiro de Cirurgiões
http://www.rcbc.periodikos.com.br/article/doi/10.1590/0100-6991e-2026004226
Revista do Colégio Brasileiro de Cirurgiões
Original Article

Bacteriobilia Polimicrobiana Está Associada à Mortalidade em 90 Dias Após Duodenopancreatectomia

Polymicrobial Bacteriobilia Is Associated with 90-Day Mortality After Pancreaticoduodenectomy

Philipe Franco do Amaral Tafner; Fernando Girardi da Silva; Alice Lily Carranza Cunha; Isabella Ferreira de Oliveira dos Santos; Martinho Antonio Gestic; Murillo Pimentel Utrini; Francisco Callejas-Neto; Everton Cazzo

Downloads: 0
Views: 47

Resumo

Introdução: A bacteriobilia é comum em pacientes submetidos à duodenopancreatectomia (DP), especialmente após drenagem biliar pré-operatória. Seu impacto sobre os desfechos perioperatórios e a mortalidade precoce estendida permanece controverso. Este estudo avaliou a associação entre culturas de bile obtidas no intraoperatório e os desfechos pós-operatórios precoces após DP por tumores periampulares.

Métodos: Este estudo de coorte retrospectivo incluiu 176 pacientes submetidos à DP com coleta de cultura de bile no intraoperatório entre 2013 e 2024, em um centro terciário. Os pacientes foram estratificados de acordo com a presença de bacteriobilia. Foram analisadas variáveis perioperatórias, complicações pós-operatórias (classificação de Clavien-Dindo) e mortalidade em 30, 60 e 90 dias. Modelos de regressão logística multivariada foram utilizados para identificar preditores independentes de bacteriobilia e de mortalidade precoce.

Resultados: Bacteriobilia foi identificada em 146 pacientes (83%), dos quais 70% apresentaram culturas polimicrobianas. A colangiopancreatografia retrógrada endoscópica (CPRE) pré-operatória (OR 23,48; IC95% 6,47-85,22; p<0,001) e a colocação de prótese biliar (OR 8,78; IC95% 1,98-38,86; p=0,004) foram preditores independentes de bacteriobilia. A mortalidade global foi de 12,5% em 30 dias, 16,0% em 60 dias e 16,5% em 90 dias. A bacteriobilia, isoladamente, não esteve associada ao aumento da morbidade maior ou da mortalidade. Entretanto, culturas de bile polimicrobianas foram independentemente associadas à maior mortalidade em 60 dias (OR 2,32; IC95% 1,35-3,88; p=0,004) e em 90 dias (OR 20,07; IC95% 1,32-304,81; p=0,031), após ajuste para ressecção vascular, sangramento, transfusão e complicações graves.

Conclusões: Embora a bacteriobilia seja altamente prevalente após drenagem biliar pré-operatória, ela não piora de forma independente os desfechos perioperatórios. Em contrapartida, culturas de bile polimicrobianas estiveram associadas ao aumento da mortalidade em 60 e 90 dias, podendo identificar um subgrupo de pacientes com maior complexidade biológica e perioperatória, ressaltando a importância da estratificação microbiológica e da avaliação da mortalidade estendida após a duodenopancreatectomia.

Palavras-chave

Duodenopancreatectomia; Bacteriobilia; Infecções das Vias Biliares; Colangiopancreatografia Retrógrada Endoscópica; Complicações Pós-Operatórias

Abstract

Introduction: Bacteriobilia is common in patients undergoing pancreaticoduodenectomy (PD), particularly after preoperative biliary drainage. Its impact on perioperative outcomes and extended early mortality remains controversial. This study evaluated the association between intraoperative bile cultures and early postoperative outcomes following PD for periampullary tumors.

Methods: This retrospective cohort study included 176 patients who underwent PD with intraoperative bile culture between 2013 and 2024 at a tertiary center. Patients were stratified according to bacteriobilia status. Perioperative variables, postoperative complications (Clavien-Dindo classification), and mortality at 30, 60, and 90 days were analyzed. Multivariable logistic regression identified independent predictors of bacteriobilia and early mortality.

Results: Bacteriobilia was detected in 146 patients (83%), with 70% presenting polymicrobial cultures. Preoperative ERCP (OR 23.48; 95% CI 6.47-85.22; p<0.001) and biliary stent placement (OR 8.78; 95% CI 1.98-38.86; p=0.004) independently predicted bacteriobilia. Overall mortality was 12.5% at 30 days, 16.0% at 60 days, and 16.5% at 90 days. Bacteriobilia per se was not associated with increased major morbidity or mortality. However, polymicrobial bile cultures were independently associated with higher mortality at 60 (OR 2.32; 95% CI 1.35-3.88; p=0.004) and 90 days (OR 20.07; 95% CI 1.32-304.81; p=0.031), after adjustment for vascular resection, bleeding, transfusion, and severe complications.

Conclusions: Although bacteriobilia is highly prevalent after preoperative biliary drainage, it does not independently worsen perioperative outcomes. Polymicrobial bile cultures were associated with increased 60- and 90-day mortality and may identify a subgroup of patients with greater biological and perioperative complexity, highlighting the importance of microbiological stratification and extended mortality assessment after PD.

Keywords

Pancreaticoduodenectomy; Bacteriobilia; Biliary Tract Infections; Cholangiopancreatography, Endoscopic Retrograde; Postoperative Complications

References

1 Abu Hilal M, Uijterwijk BA, Lemmers DHL, Janssen BV, Besselink MG, Bianchi D, et al. The Brescia International Multidisciplinary Consensus Guidelines on the Optimal Pathology Assessment and Multidisciplinary Pathways of Non-Pancreatic Neoplasms in and Around the Ampulla of Vater (PERIPAN). United European Gastroenterol J. 2025;13(7):1048-1068. doi: 10.1002/ueg2.70074.

2 Uijterwijk BA, Lemmers DH, Ghidini M, Wilmink H, Zaniboni A, Salvia R, et al. ISGACA Consortium. The Five Periampullary Cancers, not Just Different Siblings but Different Families: An International Multicenter Cohort Study. Ann Surg Oncol. 2024;31(9):6157-6169. doi: 10.1245/s10434-024-15555-8.

3 Chiorean EG, Chiaro MD, Tempero MA, Malafa MP, Benson AB, Cardin DB, et al. Ampullary Adenocarcinoma, Version 1.2023, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2023;21(7):753-782. doi: 10.6004/jnccn.2023.0034.

4 Skórzewska M, Kurzawa P, Ciszewski T, Pelc Z, Polkowski WP. Controversies in the diagnosis and treatment of periampullary tumours. Surg Oncol. 2022;44:101853.

5 Are C, Dhir M, Ravipati L. History of pancreaticoduodenectomy: early misconceptions, initial milestones and the pioneers. HPB (Oxford). 2011;13(6):377-84. doi: 10.1111/j.1477-2574.2011.00305.x.

6 Crile G Jr. The advantages of bypass operations over radical pancreatoduodenectomy in the treatment of pancreatic carcinoma. Surg Gynecol Obstet. 1970;130(6):1049-53.

7 Cameron JL, Riall TS, Coleman J, Belcher KA. One thousand consecutive pancreaticoduodenectomies. Ann Surg. 2006;244(1):10-5. doi: 10.1097/01.sla.0000217673.04165.ea.

8 Pavlidis ET, Pavlidis TE. Pathophysiological consequences of obstructive jaundice and perioperative management. Hepatobiliary Pancreat Dis Int. 2018;17(1):17-21. doi: 10.1016/j.hbpd.2018.01.008.

9 Van Laethem JL, De Broux S, Eisendrath P, Cremer M, Le Moine O, Devière J. Clinical impact of biliary drainage and jaundice resolution in patients with obstructive metastases at the hilum. Am J Gastroenterol. 2003;98(6):1271-7. doi: 10.1111/j.1572-0241.2003.07504.x.

10 Nehme F, Lee JH. Preoperative biliary drainage for pancreatic cancer. Dig Endosc. 2022;34(3):428-438. doi: 10.1111/den.14081.

11 Tamm EP, Silverman PM, Charnsangavej C, Evans DB. Diagnosis, staging, and surveillance of pancreatic cancer. AJR Am J Roentgenol. 2003;180(5):1311-23. doi: 10.2214/ajr.180.5.1801311.

12 Sutton TL, O'Grady J, Martindale R, Mayo SC, Gilbert EW, Sheppard BC. Intraoperative Bile Culture in Pancreaticoduodenectomy: Teaching Old Dogma New Tricks. J Gastrointest Surg. 2022;26(1):30-38. doi: 10.1007/s11605-021-05182-z.

13 Gavazzi F, Ridolfi C, Capretti G, Angiolini MR, Morelli P, Casari E, et al. Role of preoperative biliary stents, bile contamination and antibiotic prophylaxis in surgical site infections after pancreaticoduodenectomy. BMC Gastroenterol. 2016;16:43. doi: 10.1186/s12876-016-0460-1.

14 Sandini M, Honselmann KC, Cereda M, Angrisani M, Gavazzi F, Wellner U, et al. The Relative Role of Bile Bacterial Isolation on Outcome in Stent-Bearing Patients Undergoing Pancreatoduodenectomy. J Gastrointest Surg. 2020;24(10):2269-2276. doi: 10.1007/s11605-019-04388-6.

15 Maatman TK, Weber DJ, Qureshi B, Ceppa EP, Nakeeb A, Schmidt CM, et al. Does the Microbiology of Bactibilia Drive Postoperative Complications After Pancreatoduodenectomy? J Gastrointest Surg. 2020;24(11):2544-2550. doi: 10.1007/s11605-019-04432-5.

16 Wang Q, Gurusamy KS, Lin H, Xie X, Wang C. Preoperative biliary drainage for obstructive jaundice. Cochrane Database Syst Rev. 2008;(3):CD005444. doi: 10.1002/14651858.CD005444.pub2.

17 Sewnath ME, Birjmohun RS, Rauws EAl, Huibregtse K, Obertop H, Gouma DJ. The effect of preoperative bilary drainage on postoperative complications after pancreaticoduodenectomy. J Am Coil Surg. 2001;192:726-34. doi: 10.1016/s1072-7515(01)00819-5.

18 van der Gaag NA, Rauws EA, van Eijck CH, Bruno MJ, van der Harst E, Kubben FJ, et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med. 2010;362(2):129-37. doi: 10.1056/NEJMoa0903230.

19 Forster K, Klein F, Simon N, Chhatwal P, Ziesing S, Heidrich B, Solbach P. Cultivation-based characterization of biliary microbiota in bile samples collected during routine endoscopic retrograde cholangiography: 10 years of experience at a tertiary center. Eur J Gastroenterol Hepatol. 2023;35(10):1159-1167. doi: 10.1097/MEG.0000000000002633.

20 van der Gaag NA, de Castro SM, Rauws EA, Bruno MJ, van Eijck CH, Kuipers EJ, et al. Preoperative biliary drainage for periampullary tumors causing obstructive jaundice; DRainage vs. (direct) OPeration (DROP-trial). BMC Surg. 2007;7:3. doi: 10.1186/1471-2482-7-3.

21 Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205-213. doi: 10.1097/01.sla.0000133083.54934.ae.

22 Kagedan DJ, Mosko JD, Dixon ME, Karanicolas PJ, Wei AC, Goyert N, et al. Changes in preoperative endoscopic and percutaneous bile drainage in patients with periampullary cancer undergoing pancreaticoduodenectomy in Ontario: effect on clinical practice of a randomized trial. Curr Oncol. 2018;25(5):e430-e435. doi: 10.3747/co.25.4007.

23 Yamamoto Y, Sugiura T, Esaki M, Takahashi Y, Arita J, Hashimoto M, et al. Impact of biliary drainage method before pancreaticoduodenectomy on short- and long-term outcomes in patients with periampullary carcinoma and obstructive jaundice: A multicenter retrospective analysis. Surgery. 2024;176(3):616-625. doi: 10.1016/j.surg.2024.05.011.

24 Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1-12. doi: 10.1086/595011.

25 Ishiwatari H, Sato J, Sakamoto H, Doi T, Ono H. Current status of preoperative endoscopic biliary drainage for distal and hilar biliary obstruction. Dig Endosc. 2024;36(9):969-980. doi: 10.1111/den.14786.

26 Dupont B, Dejardin O, Kam W, Launay L, Mosquet L, Gloro R, et al. Impact of timing of access to endoscopic drainage and social determinants of health on the prognosis of patients with periampullary cancer diagnosed through jaundice: a multicenter retrospective study. Ther Adv Gastroenterol. 2026;19:17562848261426095. doi: 10.1177/17562848261426095.

27 Pandey M, Dilip TR, Chopade A, Shrikhande SV, Bhandare M. Financial burden due to distance traveled to access treatment from specialized cancer hospitals in public sector in India: a case study of patients treated for gastric and pancreatic cancer. J Cancer Policy. 2025;45:100632. doi: 10.1016/j.jcpo.2025.100632.

28 Rustgi SD, Amin SP, Kim MK, Nagula S, Kumta NA, DiMaio CJ, Boffetta P, Lucas AL. Age, socioeconomic features, and clinical factors predict receipt of endoscopic retrograde cholangiopancreatography in pancreatic cancer. World J Gastrointest Endosc. 2019;11(2):133-144. doi: 10.4253/wjge.v11.i2.133.

29 Soares PFDC, Gestic MA, Utrini MP, Callejas-Neto F, Chaim EA, Cazzo E. Epidemiological profile, referral routes and diagnostic accuracy of cases of acute cholangitis among individuals with obstructive jaundice admitted to a tertiary-level university hospital: a cross-sectional study. Sao Paulo Med J. 2019;137(6):491-497. doi: 10.1590/1516-3180.2019.0109170919.

30 Gilliam AD, Lobo DN, Rowlands BJ, Beckingham IJ. The 'two-week' target for the diagnosis of pancreatic carcinoma: an achievable aim? Eur J Surg Oncol. 2003;29(7):575-9. doi: 10.1016/s0748-7983(03)00112-4.

31 Liang X, Shi LG, Hao J, Liu AA, Chen DL, Hu XG, Shao CH. Risk factors and managements of hemorrhage associated with pancreatic fistula after pancreaticoduodenectomy. Hepatobiliary Pancreat Dis Int. 2017;16(5):537-544. doi: 10.1016/S1499-3872(17)60061-4.

32 Li Z, Zhang Z, Hu W, Zeng Y, Liu X, Mai G, et al. Pancreaticoduodenectomy with preoperative obstructive jaundice: drainage or not. Pancreas. 2009;38(4):379-86. doi: 10.1097/MPA.0b013e31819f638b.

33 Iskandar ME, Wayne MG, Steele JG, Cooperman AM. A Tale of 2 Techniques: Preoperative Biliary Drainage and Routine Surgical Drainage with Pancreaticoduodenectomy. Surg Clin North Am. 2018;98(1):49-55. doi: 10.1016/j.suc.2017.09.004.

34 Gong S, Song S, Cheng Q, Huang Y, Tian H, Jing W, et al. Efficacy and safety of preoperative biliary drainage in patients undergoing pancreaticoduodenectomy: an updated systematic review and meta-analysis. Expert Rev Gastroenterol Hepatol. 2021;15(12):1411-1426. doi: 10.1080/17474124.2021.2013805.

35 Kone LB, Torres C, Banulescu M, Maker VK, Maker AV. Perioperative Broad-spectrum Antibiotics are Associated With Decreased Surgical Site Infections Compared to 1st-3rd Generation Cephalosporins After Open Pancreaticoduodenectomy in Patients With Jaundice or a Biliary Stent. Ann Surg. 2022;275(6):1175-1183. doi: 10.1097/SLA.0000000000004216.

36 Yang Y, Sheng J, Cai Z, Zhu L, Lu C, Mao L, et al. Antibiotic prophylaxis with piperacillin-tazobactam reduces organ/space surgical site infection after pancreaticoduodenectomy: a retrospective and propensity score-matched analysis. BMC Cancer. 2024 Feb;24(1):251. doi: 10.1186/s12885-024-11955-x.

37 Naffouje SA, Allenson K, Hodul P, Malafa M, Pimiento JM, Anaya DA, et al. Prophylactic Perioperative Antibiotics in Open Pancreaticoduodenectomy: When Less Is More and When It Is Not. A National Surgical Quality Improvement Program Propensity-Matched Analysis. J Surg Res. 2022;279:722-732. doi: 10.1016/j.jss.2022.06.028.

38 Stecca T, Nistri C, Pauletti B, Greco A, Di Giacomo A, Caratozzolo E, et al. Bacteriobilia resistance to antibiotic prophylaxis increases morbidity after pancreaticoduodenectomy: a monocentric retrospective study of 128 patients. Updates Surg. 2020;72(4):1073-1080. doi: 10.1007/s13304-020-00772-z.

39 Gibiino G, Cucchetti A, Mocchegiani F, Bocchino A, Gaudenzi F, Binda C, et al. Alarming correlation between multidrug-resistant bacteriobilia and morbidity after pancreatic surgery. Dig Liver Dis. 2023;55(11):1502-1508. doi: 10.1016/j.dld.2023.05.012.

40 Yoon SJ, Huh K, Lee O, Jung JH, Han IW, Heo JS, et al. Effect of Intraoperatively Detected Bacteriobilia on Surgical Outcomes After Pancreatoduodenectomy: Analysis of a Prospective Database in a Single Institute. J Gastrointest Surg. 2022;26(10):2158-2166. doi: 10.1007/s11605-022-05405-x.

41 Blacker S, Lahiri RP, Phillips M, Pinn G, Pencavel TD, Kumar R,et al. Which patients benefit from preoperative biliary drainage in resectable pancreatic cancer? Expert Rev Gastroenterol Hepatol. 2021;15(8):855-863. doi: 10.1080/17474124.2021.1915127.

42 Mise Y, Vauthey JN, Zimmitti G, Parker NH, Conrad C, Aloia TA, et al. Ninety-day Postoperative Mortality Is a Legitimate Measure of Hepatopancreatobiliary Surgical Quality. Ann Surg. 2015;262(6):1071-8. doi: 10.1097/SLA.0000000000001048.

43 Swanson RS, Pezzi CM, Mallin K, Loomis AM, Winchester DP. The 90-day mortality after pancreatectomy for cancer is double the 30-day mortality: more than 20,000 resections from the national cancer data base. Ann Surg Oncol. 2014;21(13):4059-67. doi: 10.1245/s10434-014-4036-4.
 

 

Submitted date:
04/09/2026

Accepted date:
06/25/2026

6aa7eef8a9539519b633d414 rcbc Articles

RCBC

Share this page
Page Sections