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The Relative Role of Bile Bacterial Isolation on Outcome in Stent-Bearing Patients Undergoing Pancreatoduodenectomy

  • Original Article
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Journal of Gastrointestinal Surgery

Abstract

Background

Biliary stenting leads to antimicrobial-resistant (AMR) microorganism retrievement in bile cultures. However, the impact of intraoperative bile colonizations on post-pancreaticoduodenectomy complications remains unclear. Aims of our study were to characterize the bile flora of stented patients in comparison with postoperative cultures and to analyze whether patterns of drug resistance affected postoperative outcomes.

Methods

We analyzed records from stent-bearing pancreaticoduodenectomy patients at 3 European centers. Intra- and postoperative cultures were compared and classified as multidrug sensitive (MDS), multidrug resistant (MDR), and extensively drug resistant (XDR). Thirty-day complications were graded according to international standards.

Results

Out of 270 patients, intraoperative cultures were positive in 219 (81.1%) cases. In 36.7%, MDS species were isolated; in 35.9%, MDR; and in 8.5%, XDR species. A solid correspondence between the species isolated intra- and postoperatively (p < 0.001) was observed. Intraoperative MDR/XDR isolation was associated with an increased rate of surgical (p = 0.043) and infectious complications (p = 0.030), but not severe complication rate (p = 0.973). Postoperative MDR/XDR isolation was associated with higher risk of major complications (45.6% vs. 15.8%, p < 0.001), postoperative pancreatic fistula (p < 0.001), and post-pancreatectomy hemorrhage (p = 0.002). By multivariate analysis, intraoperative AMR isolation was associated with high likelihood of postoperative AMR infections. However, only in 43/121 cases, intraoperative MDR/XDR microorganisms turned into the occurrence of postoperative infections.

Conclusion

Intraoperative AMR isolates do not translate into severe outcomes, despite being significantly associated with surgical and infectious complications.

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References

  1. Teillant A, Gandra S, Barter D, Morgan DJ, Laxminarayan R. Potential burden of antibiotic resistance on surgery and cancer chemotherapy antibiotic prophylaxis in the USA: a literature review and modelling study. Lancet Infect Dis 2015;15:1429–1437

    Article  Google Scholar 

  2. Kirby A, Santoni N. Antibiotic resistance in Enterobacteriaceae: what impact on the efficacy of antibiotic prophylaxis in colorectal surgery? J Hosp Infect 2015;89:259–63

    Article  CAS  Google Scholar 

  3. Okano K, Hirao T, Unno M, et al. Postoperative infectious complications after pancreatic resection Br J Surg. 2015;102:1551–1560

    Article  CAS  Google Scholar 

  4. Marston HD, Dixon DM, Knisely JM, Palmore TN, Fauci AS. Antimicrobial Resistance. JAMA. 2016;316:1193–1204

    Article  CAS  Google Scholar 

  5. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009 ;48(1):1-12

    Article  Google Scholar 

  6. Gandra S, Barter DM, Laxminarayan R. Economic burden of antibiotic resistance: how much do we really know? Clin Microbiol Infect. 2014;20(10):973-80

    Article  CAS  Google Scholar 

  7. Wu W, He J, Cameron JL, Makary M, Soares K, Ahuja N, et al. The impact of postoperative complications on the administration of adjuvant therapy following pancreaticoduodenectomy for adenocarcinoma. Annals of surgical oncology. 2014;21(9):2873-81

    Article  Google Scholar 

  8. Mokart D, Giaoui E, Barbier L, Lambert J, Sannini A, Chow-Chine L, Brun JP, Faucher M, Guiramand J, Ewald J, Bisbal M, Blache JL, Delpero JR, Leone M, Turrini O. Postoperative sepsis in cancer patients undergoing major elective digestive surgery is associated with increased long-term mortality. J Crit Care. 2016 Feb;31(1):48-53

    Article  Google Scholar 

  9. Lavu H, Klinge MJ, Nowcid LJ, Cohn HE, Grenda DR, Sauter PK, Leiby BE, Croker SP, Kennedy EP, Yeo CJ. Perioperative surgical care bundle reduces pancreaticoduodenectomy wound infections. J Surg Res. 2012;174(2):215-21

    Article  Google Scholar 

  10. 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(3):356-61

    Article  CAS  Google Scholar 

  11. Liu C, Lu JW, Du ZQ, Liu XM, Lv Y, Zhang XF. Association of Preoperative Biliary Drainage with Postoperative Morbidity after Pancreaticoduodenectomy. Gastroenterol Res Pract. 2015;2015:796893. https://doi.org/10.1155/2015/796893

    Article  PubMed  PubMed Central  Google Scholar 

  12. Povoski SP, Karpeh MS Jr, Conlon KC, Blumgart LH, Brennan MF. Association of preoperative biliary drainage with postoperative outcome following pancreaticoduodenectomy. Ann Surg. 1999;230(2):131-42

    Article  CAS  Google Scholar 

  13. Scheufele F, Aichinger L, Jäger C, Demir IE, Schorn S, Sargut M, Erkan M, Kleeff J, Friess H, Ceyhan GO. Effect of preoperative biliary drainage on bacterial flora in bile of patients with periampullary cancer. Br J Surg. 2017;104(2):e182-e188

    Article  CAS  Google Scholar 

  14. Mohammed S, Evans C, VanBuren G, Hodges SE, Silberfein E, Artinyan A, Mo Q, Issazadeh M, McElhany AL, Fisher WE. Treatment of bacteriobilia decreases wound infection rates after pancreaticoduodenectomy. HPB (Oxford). 2014;16(6):592-8

    Article  Google Scholar 

  15. Sudo T, Murakami Y, Uemura K, Hashimoto Y, Kondo N, Nakagawa N, Ohge H, Sueda T. Perioperative antibiotics covering bile contamination prevent abdominal infectious complications after pancreatoduodenectomy in patients with preoperative biliary drainage. World J Surg. 2014;38(11):2952-9

    Article  Google Scholar 

  16. Fong ZV, McMillan MT, Marchegiani G, Sahora K, Malleo G, De Pastena M, Loehrer AP, Lee GC, Ferrone CR, Chang DC, Hutter MM, Drebin JA, Bassi C, Lillemoe KD, Vollmer CM, Fernández-Del Castillo C. Discordance Between Perioperative Antibiotic Prophylaxis and Wound Infection Cultures in Patients Undergoing Pancreaticoduodenectomy. JAMA Surg. 2016;151(5):432-9

    Article  Google Scholar 

  17. Gianotti L, Tamini N, Gavazzi F, Mariani A, Sandini M, Ferla F, Cereda M, Capretti G, Di Sandro S, Bernasconi DP, De Carlis L, Zerbi A. Consequences of Increases in Antibiotic Resistance Pattern on Outcome of Pancreatic Resection for Cancer. J Gastrointest Surg. 2017 Oct;21(10):1650-1657

    Article  Google Scholar 

  18. McManus MC. Mechanisms of bacterial resistance to antimicrobial agents. Am J Health Syst Pharm. 1997 Jun 15;54(12):1420-33

    Article  CAS  Google Scholar 

  19. Magiorakos AP, Srinivasan A, Carey RB et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012 Mar;18(3):268-81

    Article  CAS  Google Scholar 

  20. 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. Annals of surgery. 2004;240(2):205-13

    Article  Google Scholar 

  21. 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(3):584-591

    Article  Google Scholar 

  22. Wente MN, Bassi C, Dervenis C et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142(5):761-8

    Article  Google Scholar 

  23. Wente MN, Veit JA, Bassi C et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery. 2007;142(1):20-5.

    Article  Google Scholar 

  24. Gianotti L, Biffi R, Sandini M, Marrelli D, Vignali A, Caccialanza R, Viganò J, Sabbatini A, Di Mare G, Alessiani M, Antomarchi F, Valsecchi MG, Bernasconi DP. Preoperative Oral Carbohydrate Load Versus Placebo in Major Elective Abdominal Surgery (PROCY): A Randomized, Placebo-controlled, Multicenter, Phase III Trial. Ann Surg. 2018;267(4):623-630

    Article  Google Scholar 

  25. O’Neill J. Tackling drug-resistant infections globally: Final report and recommendations. The review on antimicrobial resistance. http://amrreview.org/sites/default/files/160518_Final%20paper_ with%20cover.pdf (accessed July, 2016)

  26. Teillant A, Gandra S, Barter D, Morgan DJ, Laxminarayan R. Potential burden of antibiotic resistance on surgery and cancer chemotherapy antibiotic prophylaxis in the USA: a literature review and modelling study. Lancet Infect Dis. 2015;15(12):1429-37

    Article  Google Scholar 

  27. De Pastena M, Paiella S, Marchegiani G, Malleo G, Ciprani D, Gasparini C, Secchettin E, Salvia R, Bassi C. Postoperative infections represent a major determinant of outcome after pancreaticoduodenectomy: Results from a high-volume center. Surgery. 2017;162(4):792-801

    Article  Google Scholar 

  28. Loos M, Strobel O, Legominski M, Dietrich M, Hinz U, Brenner T, Heininger A, Weigand MA, Büchler MW, Hackert T. Postoperative pancreatic fistula: Microbial growth determines outcome. Surgery. 2018 Dec;164(6):1185-1190

    Article  Google Scholar 

  29. Sourrouille I, Gaujoux S, Lacave G, Bert F, Dokmak S, Belghiti J, Paugam-Burtz C, Sauvanet A. Five days of postoperative antimicrobial therapy decreases infectious complications following pancreaticoduodenectomy in patients at risk for bile contamination. HPB (Oxford). 2013;15(6):473-80

    Article  Google Scholar 

  30. Department of Health and Human Services/Centers for Disease Control and Prevention/National Center for Emerging and Zoonotic Infectious Diseases/Division of Healthcare Quality Promotion/Healthcare Infection Control Practices Advisory Committee (HICPAC) meeting summary report, April 10th–11th, 2014. CDC, Atlanta, GA. Available at: https: //www.cdc.gov/hicpac/.../HICPAC_April2014_Summary_With_Liaison_Reports [last accessed December 2016].

  31. Pitt HA, Postier RG, Cameron JL. Biliary bacteria: significance and alterations after antibiotic therapy. Arch Surg. 1982;117(4):445-9

    Article  CAS  Google Scholar 

  32. Cohen J: The immunopathogenesis of sepsis. Nature 2002; 420:885–891

    Article  CAS  Google Scholar 

  33. Darton T, Guiver M, Naylor S, et al: Severity of meningococcal disease associated with genomic bacterial load. Clin Infect Dis 2009; 48:587–594

    Article  Google Scholar 

  34. Minami T, Sasaki T, Serikawa M, Ishigaki T, Murakami Y, Chayama K. Antibiotic prophylaxis for endoscopic retrograde chlangiopancreatography increases the detection rate of drug-resistant bacteria in bile. J Hepatobiliary Pancreat Sci. 2014 Sep;21(9):712-8

    Article  Google Scholar 

  35. Sandini M, Honselmann KC, Birnbaum DJ, Gavazzi F, Chirica M, Wellner U, Guilbaud T, Bolm L, Angrisani M, Moutardier V, Cereda M, Girard É, Montorsi M, Keck T, Zerbi A, Gianotti L. Preoperative Biliary Stenting and Major Morbidity After Pancreatoduodenectomy: Does Elapsed Time Matter?: The FRAGERITA Study Group. Ann Surg. 2018;268(5):808-814

    Google Scholar 

  36. Tang K, Lu W, Qin W, Wu Y. Neoadjuvant therapy for patients with borderline resectable pancreatic cancer: A systematic review and meta-analysis of response and resection percentages. Pancreatology. 2016;16(1):28-37

    Article  Google Scholar 

Download references

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Authors and Affiliations

  1. School of Medicine and Surgery, Department of Surgery, San Gerardo Hospital, Milano Bicocca University, Monza, Italy

    Marta Sandini, Marco Cereda, Marco Angrisani & Luca Gianotti

  2. Department of Surgery, University Medical Center Schleswig-Holstein, Campus Lübeck, Lübeck, Germany

    Kim C. Honselmann, Ulrich Wellner, Louisa Bolm & Tobias Keck

  3. Pancreatic Surgery Unit, Department of Surgery, Humanitas Research Hospital and University, Rozzano, Milan, Italy

    Marco Cereda, Francesca Gavazzi & Alessandro Zerbi

Authors
  1. Marta Sandini
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  2. Kim C. Honselmann
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Contributions

MS, KH, MC, MA, LB, FG, UW, TK, AZ, and LG are involved in the preparation of the proposal and study design and participated in data collection, data entry, and data analysis. MS, KH, and LG are involved in manuscript preparation. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Luca Gianotti.

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The authors declare that they have no conflict of interest.

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The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

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Not applicable given the retrospective nature of the study design.

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Sandini, M., Honselmann, K.C., Cereda, M. et al. The Relative Role of Bile Bacterial Isolation on Outcome in Stent-Bearing Patients Undergoing Pancreatoduodenectomy. J Gastrointest Surg 24, 2269–2276 (2020). https://doi.org/10.1007/s11605-019-04388-6

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