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Published in: Annals of Surgical Oncology 1/2021

01-01-2021 | Pancreatoduodenostomy | Pancreatic Tumors

Impact of Qualitative and Quantitative Biliary Contamination Status on the Incidence of Postoperative Infection Complications in Patients Undergoing Pancreatoduodenectomy

Authors: Masaya Suenaga, MD, PhD, Yukihiro Yokoyama, MD, PhD, Tsutomu Fujii, MD, PhD, Suguru Yamada, MD, PhD, Junpei Yamaguchi, MD, PhD, Masamichi Hayashi, MD, PhD, Takashi Asahara, PhD, Masato Nagino, MD, PhD, Yasuhiro Kodera, MD, PhD

Published in: Annals of Surgical Oncology | Issue 1/2021

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Abstract

Background

Bacterial contamination status may differ under different biliary drainage conditions. The purpose of this study was to determine the impact of qualitative and quantitative biliary bacterial contamination on the incidence of infection complications in patients undergoing pancreatoduodenectomy.

Methods

Patients undergoing pancreatoduodenectomy for periampullary diseases with different biliary drainage conditions, such as external drainage (ED), internal drainage (ID), and no drainage (ND), were included. Bile was collected intraoperatively, and biliary contamination status was qualified and quantified using bacterium-specific ribosomal RNA-targeted reverse transcription–quantitative polymerase chain reaction (RT-qPCR). The impact of biliary contamination status on infection complications was analyzed.

Results

A total of 152 patients were included (38 with ED, 40 with ID, and 74 with ND). The positive rate of microorganisms in bile was higher in the ID group (98%) compared with the ED group (82%, p = 0.021) and the ND group (65%, p < 0.001). The number of microorganisms detected in bile samples was higher in the ID group compared with the ED group (median 489,788 vs. 5375 bacteria/mL of bile, p < 0.001). With multivariate analysis, soft pancreas, intraoperative bleeding (> 600 mL), and biliary contamination by Atopobium cluster were identified as independent risk factors for infection complications. Biliary contamination by Atopobium cluster was significantly higher in the ID group compared with the other groups.

Conclusions

Biliary bacterial contamination is more frequently induced by ID than either ED or ND. In addition to the previously known risk factors, biliary contamination with Atopobium cluster may be one of the risk factors of infection complications following pancreatoduodenectomy.
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Literature
1.
go back to reference van der Gaag NA, Rauws EA, van Eijck CH, et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med. 2010;362:129–37.CrossRef van der Gaag NA, Rauws EA, van Eijck CH, et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med. 2010;362:129–37.CrossRef
2.
go back to reference Eshuis WJ, van der Gaag NA, Rauws EA, et al. Therapeutic delay and survival after surgery for cancer of the pancreatic head with or without preoperative biliary drainage. Ann Surg. 2010;252:840–9.CrossRef Eshuis WJ, van der Gaag NA, Rauws EA, et al. Therapeutic delay and survival after surgery for cancer of the pancreatic head with or without preoperative biliary drainage. Ann Surg. 2010;252:840–9.CrossRef
3.
go back to reference Singhirunnusorn J, Roger L, Chopin-Laly X, Lepilliez V, Ponchon T, Adham M. Value of preoperative biliary drainage in a consecutive series of resectable periampullary lesions. From randomized studies to real medical practice. Langenbecks Arch Surg. 2013;398:295–302.CrossRef Singhirunnusorn J, Roger L, Chopin-Laly X, Lepilliez V, Ponchon T, Adham M. Value of preoperative biliary drainage in a consecutive series of resectable periampullary lesions. From randomized studies to real medical practice. Langenbecks Arch Surg. 2013;398:295–302.CrossRef
4.
go back to reference Coates JM, Beal SH, Russo JE, et al. Negligible effect of selective preoperative biliary drainage on perioperative resuscitation, morbidity, and mortality in patients undergoing pancreaticoduodenectomy. Arch Surg. 2009;144:841–7.CrossRef Coates JM, Beal SH, Russo JE, et al. Negligible effect of selective preoperative biliary drainage on perioperative resuscitation, morbidity, and mortality in patients undergoing pancreaticoduodenectomy. Arch Surg. 2009;144:841–7.CrossRef
5.
go back to reference Farges O, Regimbeau JM, Fuks D, et al. Multicentre European study of preoperative biliary drainage for hilar cholangiocarcinoma. Br J Surg. 2013;100:274–83.CrossRef Farges O, Regimbeau JM, Fuks D, et al. Multicentre European study of preoperative biliary drainage for hilar cholangiocarcinoma. Br J Surg. 2013;100:274–83.CrossRef
6.
go back to reference Abdullah SA, Gupta T, Jaafar KA, Chung YF, Ooi LL, Mesenas SJ. Ampullary carcinoma: effect of preoperative biliary drainage on surgical outcome. World J Gastroenterol. 2009;15:2908–12.CrossRef Abdullah SA, Gupta T, Jaafar KA, Chung YF, Ooi LL, Mesenas SJ. Ampullary carcinoma: effect of preoperative biliary drainage on surgical outcome. World J Gastroenterol. 2009;15:2908–12.CrossRef
7.
go back to reference Zarzavadjian Le Bian A, Fuks D, Dalla Valle R, Cesaretti M, Violi V, Costi R. Effectiveness and risk of biliary drainage prior to pancreatoduodenectomy: review of current status. Surg Today. 2018;48:371–9.CrossRef Zarzavadjian Le Bian A, Fuks D, Dalla Valle R, Cesaretti M, Violi V, Costi R. Effectiveness and risk of biliary drainage prior to pancreatoduodenectomy: review of current status. Surg Today. 2018;48:371–9.CrossRef
8.
go back to reference Augenstein VA, Reuter NP, Bower MR, McMasters KM, Scoggins CR, Martin RC. Bile cultures: a guide to infectious complications after pancreaticoduodenectomy. J Surg Oncol. 2010;102:478–81.CrossRef Augenstein VA, Reuter NP, Bower MR, McMasters KM, Scoggins CR, Martin RC. Bile cultures: a guide to infectious complications after pancreaticoduodenectomy. J Surg Oncol. 2010;102:478–81.CrossRef
9.
go back to reference Jagannath P, Dhir V, Shrikhande S, Shah RC, Mullerpatan P, Mohandas KM. Effect of preoperative biliary stenting on immediate outcome after pancreaticoduodenectomy. Br J Surg. 2005;92:356–61.CrossRef Jagannath P, Dhir V, Shrikhande S, Shah RC, Mullerpatan P, Mohandas KM. Effect of preoperative biliary stenting on immediate outcome after pancreaticoduodenectomy. Br J Surg. 2005;92:356–61.CrossRef
10.
go back to reference Fujii T, Yamada S, Suenaga M, et al. Preoperative internal biliary drainage increases the risk of bile juice infection and pancreatic fistula after pancreatoduodenectomy: a prospective observational study. Pancreas. 2015;44:465–70.CrossRef Fujii T, Yamada S, Suenaga M, et al. Preoperative internal biliary drainage increases the risk of bile juice infection and pancreatic fistula after pancreatoduodenectomy: a prospective observational study. Pancreas. 2015;44:465–70.CrossRef
11.
go back to reference Sugawara G, Ebata T, Yokoyama Y, et al. The effect of preoperative biliary drainage on infectious complications after hepatobiliary resection with cholangiojejunostomy. Surgery. 2013;153:200–10.CrossRef Sugawara G, Ebata T, Yokoyama Y, et al. The effect of preoperative biliary drainage on infectious complications after hepatobiliary resection with cholangiojejunostomy. Surgery. 2013;153:200–10.CrossRef
12.
go back to reference Fong ZV, McMillan MT, Marchegiani G, et al. Discordance Between Perioperative Antibiotic Prophylaxis and Wound Infection Cultures in Patients Undergoing Pancreaticoduodenectomy. JAMA Surg. 2016;151:432–9.CrossRef Fong ZV, McMillan MT, Marchegiani G, et al. Discordance Between Perioperative Antibiotic Prophylaxis and Wound Infection Cultures in Patients Undergoing Pancreaticoduodenectomy. JAMA Surg. 2016;151:432–9.CrossRef
13.
go back to reference Matsuda K, Tsuji H, Asahara T, Kado Y, Nomoto K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol. 2007;73:32–9.CrossRef Matsuda K, Tsuji H, Asahara T, Kado Y, Nomoto K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol. 2007;73:32–9.CrossRef
14.
go back to reference Matsuda K, Tsuji H, Asahara T, Matsumoto K, Takada T, Nomoto K. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl Environ Microbiol. 2009;75:1961–9.CrossRef Matsuda K, Tsuji H, Asahara T, Matsumoto K, Takada T, Nomoto K. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl Environ Microbiol. 2009;75:1961–9.CrossRef
15.
go back to reference Nishigaki E, Abe T, Yokoyama Y, et al. The detection of intraoperative bacterial translocation in the mesenteric lymph nodes is useful in predicting patients at high risk for postoperative infectious complications after esophagectomy. Ann Surg. 2014;259:477–84.CrossRef Nishigaki E, Abe T, Yokoyama Y, et al. The detection of intraoperative bacterial translocation in the mesenteric lymph nodes is useful in predicting patients at high risk for postoperative infectious complications after esophagectomy. Ann Surg. 2014;259:477–84.CrossRef
16.
go back to reference Mizuno T, Yokoyama Y, Nishio H, et al. Intraoperative bacterial translocation detected by bacterium-specific ribosomal rna-targeted reverse-transcriptase polymerase chain reaction for the mesenteric lymph node strongly predicts postoperative infectious complications after major hepatectomy for biliary malignancies. Ann Surg. 2010;252:1013–9.CrossRef Mizuno T, Yokoyama Y, Nishio H, et al. Intraoperative bacterial translocation detected by bacterium-specific ribosomal rna-targeted reverse-transcriptase polymerase chain reaction for the mesenteric lymph node strongly predicts postoperative infectious complications after major hepatectomy for biliary malignancies. Ann Surg. 2010;252:1013–9.CrossRef
17.
go back to reference Yokoyama Y, Nishigaki E, Abe T, et al. Randomized clinical trial of the effect of perioperative synbiotics versus no synbiotics on bacterial translocation after oesophagectomy. Br J Surg. 2014;101:189–99.CrossRef Yokoyama Y, Nishigaki E, Abe T, et al. Randomized clinical trial of the effect of perioperative synbiotics versus no synbiotics on bacterial translocation after oesophagectomy. Br J Surg. 2014;101:189–99.CrossRef
18.
go back to reference Kawashima H, Itoh A, Ohno E, et al. Preoperative endoscopic nasobiliary drainage in 164 consecutive patients with suspected perihilar cholangiocarcinoma: a retrospective study of efficacy and risk factors related to complications. Ann Surg. 2013;257:121–7.CrossRef Kawashima H, Itoh A, Ohno E, et al. Preoperative endoscopic nasobiliary drainage in 164 consecutive patients with suspected perihilar cholangiocarcinoma: a retrospective study of efficacy and risk factors related to complications. Ann Surg. 2013;257:121–7.CrossRef
19.
go back to reference Fujii T, Kanda M, Kodera Y, et al. Preservation of the pyloric ring has little value in surgery for pancreatic head cancer: a comparative study comparing three surgical procedures. Ann Surg Oncol. 2012;19:176–83.CrossRef Fujii T, Kanda M, Kodera Y, et al. Preservation of the pyloric ring has little value in surgery for pancreatic head cancer: a comparative study comparing three surgical procedures. Ann Surg Oncol. 2012;19:176–83.CrossRef
20.
go back to reference Bassi C, Marchegiani G, Dervenis C, et al. The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery. 2017;161:584–91.CrossRef Bassi C, Marchegiani G, Dervenis C, et al. The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery. 2017;161:584–91.CrossRef
21.
go back to reference Kanazawa H, Nagino M, Kamiya S, et al. Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbecks Arch Surg. 2005;390:104–13.CrossRef Kanazawa H, Nagino M, Kamiya S, et al. Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbecks Arch Surg. 2005;390:104–13.CrossRef
22.
go back to reference Sugawara G, Nagino M, Nishio H, et al. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg. 2006;244:706–14.CrossRef Sugawara G, Nagino M, Nishio H, et al. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg. 2006;244:706–14.CrossRef
24.
go back to reference 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;240:205–13.CrossRef 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;240:205–13.CrossRef
25.
go back to reference Ohgi K, Sugiura T, Yamamoto Y, Okamura Y, Ito T, Uesaka K. Bacterobilia may trigger the development and severity of pancreatic fistula after pancreatoduodenectomy. Surgery. 2016;160:725–30.CrossRef Ohgi K, Sugiura T, Yamamoto Y, Okamura Y, Ito T, Uesaka K. Bacterobilia may trigger the development and severity of pancreatic fistula after pancreatoduodenectomy. Surgery. 2016;160:725–30.CrossRef
26.
go back to reference Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474:1823–36.CrossRef Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474:1823–36.CrossRef
27.
go back to reference Sung JY, Costerton JW, Shaffer EA. Defense system in the biliary tract against bacterial infection. Dig Dis Sci. 1992;37:689–96.CrossRef Sung JY, Costerton JW, Shaffer EA. Defense system in the biliary tract against bacterial infection. Dig Dis Sci. 1992;37:689–96.CrossRef
28.
go back to reference Scheithauer BK, Wos-Oxley ML, Ferslev B, Jablonowski H, Pieper DH. Characterization of the complex bacterial communities colonizing biliary stents reveals a host-dependent diversity. ISME J. 2009;3:797–807.CrossRef Scheithauer BK, Wos-Oxley ML, Ferslev B, Jablonowski H, Pieper DH. Characterization of the complex bacterial communities colonizing biliary stents reveals a host-dependent diversity. ISME J. 2009;3:797–807.CrossRef
29.
go back to reference Baughn AD, Malamy MH. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature. 2004;427:441–4.CrossRef Baughn AD, Malamy MH. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature. 2004;427:441–4.CrossRef
30.
go back to reference Song YG, Shim SG, Kim KM, et al. Profiling of the bacteria responsible for pyogenic liver abscess by 16S rRNA gene pyrosequencing. J Microbiol. 2014;52:504–9.CrossRef Song YG, Shim SG, Kim KM, et al. Profiling of the bacteria responsible for pyogenic liver abscess by 16S rRNA gene pyrosequencing. J Microbiol. 2014;52:504–9.CrossRef
31.
go back to reference Garcia-Sancho Tellez L, Rodriguez-Montes JA, Fernandez de Lis S, Garcia-Sancho Martin L. Acute emphysematous cholecystitis. Report of twenty cases. Hepatogastroenterology. 1999;46:2144–8. Garcia-Sancho Tellez L, Rodriguez-Montes JA, Fernandez de Lis S, Garcia-Sancho Martin L. Acute emphysematous cholecystitis. Report of twenty cases. Hepatogastroenterology. 1999;46:2144–8.
32.
go back to reference Ferris MJ, Masztal A, Aldridge KE, Fortenberry JD, Fidel PL, Jr., Martin DH. Association of Atopobium vaginae, a recently described metronidazole resistant anaerobe, with bacterial vaginosis. BMC Infect Dis. 2004;4:5.CrossRef Ferris MJ, Masztal A, Aldridge KE, Fortenberry JD, Fidel PL, Jr., Martin DH. Association of Atopobium vaginae, a recently described metronidazole resistant anaerobe, with bacterial vaginosis. BMC Infect Dis. 2004;4:5.CrossRef
Metadata
Title
Impact of Qualitative and Quantitative Biliary Contamination Status on the Incidence of Postoperative Infection Complications in Patients Undergoing Pancreatoduodenectomy
Authors
Masaya Suenaga, MD, PhD
Yukihiro Yokoyama, MD, PhD
Tsutomu Fujii, MD, PhD
Suguru Yamada, MD, PhD
Junpei Yamaguchi, MD, PhD
Masamichi Hayashi, MD, PhD
Takashi Asahara, PhD
Masato Nagino, MD, PhD
Yasuhiro Kodera, MD, PhD
Publication date
01-01-2021
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 1/2021
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-020-08645-w

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