Prognostic Impact of Bacterobilia on Morbidity and Postoperative Management After Pancreatoduodenectomy: A Systematic Review and Meta-analysis
Benjamin Müssle
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorSebastian Hempel
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorChristoph Kahlert
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorMarius Distler
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorJürgen Weitz
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorCorresponding Author
Thilo Welsch
- [email protected]
- 49 (0)351 458 18283
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Tel.: 49 (0)351 458 18283, [email protected]Search for more papers by this authorBenjamin Müssle
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorSebastian Hempel
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorChristoph Kahlert
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorMarius Distler
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorJürgen Weitz
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Search for more papers by this authorCorresponding Author
Thilo Welsch
- [email protected]
- 49 (0)351 458 18283
Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Tel.: 49 (0)351 458 18283, [email protected]Search for more papers by this authorJürgen Weitz and Thilo Welsch have contributed equally to this work.
Electronic supplementary material: The online version of this article (https://doi.org/10.1007/s00268-018-4546-5) contains supplementary material, which is available to authorized users.
Abstract
Background
Intraoperative bile analysis during pancreatoduodenectomy (PD) is performed routinely at specialized centers worldwide. However, it remains controversial if and how intraoperative bacterobilia during PD affects morbidity and its management. The aim of the study was a systematic review and meta-analysis of intraoperative bacterobilia and its impact on patient outcome after PD.
Methods
Five relevant outcomes of interest were defined, and a systematic review of the literature with meta-analysis was performed according to the PRISMA guidelines.
Results
A total of 28 studies (8523 patients) were included. The median incidence of bacterobilia was 58% (interquartile range 51–67%). The most frequently isolated bacteria were Enterococcus species (51%), Klebsiella species (28%), and Escherichia coli (27%). Preoperative biliary drainage was significantly associated with bacterobilia (86 vs. 25%; RR 3.27; 95% confidence interval (CI) 2.42–4.42; p < 0.001). The incidence of surgical site infections (SSI) was significantly increased in cases with bacterobilia (RR 2.84; 95% CI 2.17–3.73; p < 0.001). Postoperative pancreatic fistula, overall postoperative morbidity, and mortality were not significantly influenced. Identical bacteria in bile and the infectious sources were found in 48% (interquartile range 34–59%) of the cases.
Conclusions
Bacterobilia is detected during almost every second PD and is associated with an increased rate of SSI. The microbiome from intraoperative bile and postoperative infectious sources match in ~50% of patients, providing the option of early administration of calculated antibiotics and the determination of resistance patterns.
Supporting Information
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References
- 1DeOliveiraML, WinterJM, SchaferM et al. Assessment of complications after pancreatic surgery: a novel grading system applied to 633 patients undergoing pancreaticoduodenectomy. Ann Surg (2006) 244: 931–93710.1097/01.sla.0000246856.03918.9a17122618(discussion 937–939)
- 2KamphuesC, BovaR, SchrickeD et al. Postoperative complications deteriorate long-term outcome in pancreatic cancer patients. Ann Surg Oncol (2012) 19: 856–86310.1245/s10434-011-2041-421879265
- 3HataT, MotoiF, IshidaM et al. Effect of hospital volume on surgical outcomes after pancreaticoduodenectomy: a systematic review and meta-analysis. Ann Surg (2016) 263: 664–67210.1097/SLA.000000000000143726636243
- 4De PastenaM, PaiellaS, MarchegianiG et al. Postoperative infections represent a major determinant of outcome after pancreaticoduodenectomy: results from a high-volume center. Surgery (2017) 162: 792–80110.1016/j.surg.2017.05.01628676333
- 5VollmerCMJr, SanchezN, GondekS et al. A root-cause analysis of mortality following major pancreatectomy. J Gastrointest Surg Off J Soc Surg Aliment Tract (2012) 16: 89–10210.1007/s11605-011-1753-x(discussion 102–103)
10.1007/s11605-011-1753-x Google Scholar
- 6WelschT, FrommholdK, HinzU et al. Persisting elevation of C-reactive protein after pancreatic resections can indicate developing inflammatory complications. Surgery (2008) 143: 20–2810.1016/j.surg.2007.06.01018154929
- 7ScheufeleF, SchornS, DemirIE et al. Preoperative biliary stenting versus operation first in jaundiced patients due to malignant lesions in the pancreatic head: a meta-analysis of current literature. Surgery (2017) 161: 939–95010.1016/j.surg.2016.11.00128043693
- 8van der GaagNA, RauwsEA, van EijckCH et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med (2010) 362: 129–13710.1056/NEJMoa090323020071702
- 9PovoskiSP, KarpehMSJr, ConlonKC et al. Association of preoperative biliary drainage with postoperative outcome following pancreaticoduodenectomy. Ann Surg (1999) 230: 131–14210.1097/00000658-199908000-0000110450725
- 10LimongelliP, PaiM, BansiD et al. Correlation between preoperative biliary drainage, bile duct contamination, and postoperative outcomes for pancreatic surgery. Surgery (2007) 142: 313–31810.1016/j.surg.2007.04.02217723881
- 11di MolaFF, TavanoF, RagoRR et al. Influence of preoperative biliary drainage on surgical outcome after pancreaticoduodenectomy: single centre experience. Langenbeck’s Arch Surg Deutsche Ges Chir (2014) 399: 649–657
- 12CortesA, SauvanetA, BertF et al. Effect of bile contamination on immediate outcomes after pancreaticoduodenectomy for tumor. J Am Coll Surg (2006) 202: 93–9910.1016/j.jamcollsurg.2005.09.00616377502
- 13SivarajSM, VimalrajV, SaravanaboopathyP et al. Is bactibilia a predictor of poor outcome of pancreaticoduodenectomy?. Hepatobiliary Pancreat Dis Int (2010) 9: 65–6820133232
- 14IslaAM, GriniatsosJ, RiazA et al. Pancreaticoduodenectomy for periampullary malignancies: the effect of bile colonization on the postoperative outcome. Langenbeck’s Arch Surg Deutsche Ges Chir (2007) 392: 67–7310.1007/s00423-006-0102-0
- 15GreggJA, De GirolamiP, Carr-LockeDL Effects of sphincteroplasty and endoscopic sphincterotomy on the bacteriologic characteristics of the common bile duct. Am J Surg (1985) 149: 668–67110.1016/S0002-9610(85)80152-53993851
- 16HerzogT, BelyaevO, MullerCA et al. Bacteribilia after preoperative bile duct stenting: a prospective study. J Clin Gastroenterol (2009) 43: 457–46210.1097/MCG.0b013e318186b19b19276992
- 17NomuraT, ShiraiY, HatakeyamaK Enterococcal bactibilia in patients with malignant biliary obstruction. Dig Dis Sci (2000) 45: 2183–218610.1023/A:102664060331211215736
- 18StroupDF, BerlinJA, MortonSC et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA (2000) 283: 2008–201210.1001/jama.283.15.200810789670
- 19MoherD, LiberatiA, TetzlaffJ et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med (2009) 6: e100009710.1371/journal.pmed.100009719621072
- 20SterneJA, HernanMA, ReevesBC et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ (Clin Res ed) (2016) 355: i4919
- 21OhgiK, SugiuraT, YamamotoY et al. Bacterobilia may trigger the development and severity of pancreatic fistula after pancreatoduodenectomy. Surgery (2016) 160: 725–73010.1016/j.surg.2016.03.03227233637
- 22MezhirJJ, BrennanMF, BaserRE et al. A matched case-control study of preoperative biliary drainage in patients with pancreatic adenocarcinoma: routine drainage is not justified. J Gastrointest Surg Off J Soc Surg Aliment Tract (2009) 13: 2163–216910.1007/s11605-009-1046-9
10.1007/s11605-009-1046-9 Google Scholar
- 23FujiiT, YamadaS, SuenagaM 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: 465–47010.1097/MPA.000000000000035225423556
- 24SudoT, MurakamiY, UemuraK et al. Perioperative antibiotics covering bile contamination prevent abdominal infectious complications after pancreatoduodenectomy in patients with preoperative biliary drainage. World J Surg (2014) 38: 2952–295910.1007/s00268-014-2688-725022981
- 25Morris-StiffG, TamijmaraneA, TanYM et al. Pre-operative stenting is associated with a higher prevalence of post-operative complications following pancreatoduodenectomy. Int J Surg (Lond, Engl) (2011) 9: 145–14910.1016/j.ijsu.2010.10.008
- 26CoatesJM, BealSH, RussoJE et al. Negligible effect of selective preoperative biliary drainage on perioperative resuscitation, morbidity, and mortality in patients undergoing pancreaticoduodenectomy. Arch Surg (Chicago, IL: 1960) (2009) 144: 841–847
- 27GrizasS, StakyteM, KinciusM et al. Etiology of bile infection and its association with postoperative complications following pancreatoduodenectomy. Medicina (Kaunas) (2005) 41: 386–391
- 28JagannathP, DhirV, ShrikhandeS et al. Effect of preoperative biliary stenting on immediate outcome after pancreaticoduodenectomy. Br J Surg (2005) 92: 356–36110.1002/bjs.486415672425
- 29ScheufeleF, AichingerL, JagerC et al. Effect of preoperative biliary drainage on bacterial flora in bile of patients with periampullary cancer. Br J Surg (2017) 104: e182–e18810.1002/bjs.1045028121036
- 30HerzogT, BelyaevO, AkkuzuR et al. The impact of bile duct cultures on surgical site infections in pancreatic surgery. Surg Infect (2015) 16: 443–44910.1089/sur.2014.104
- 31CammannS, TimrottK, VonbergRP et al. Cholangitis in the postoperative course after biliodigestive anastomosis. Langenbeck’s Arch Surg Deutsche Ges Chir (2016) 401: 715–72410.1007/s00423-016-1450-z
- 32SahoraK, Morales-OyarvideV, FerroneC et al. Preoperative biliary drainage does not increase major complications in pancreaticoduodenectomy: a large single center experience from the Massachusetts General Hospital. J Hepato Biliary Pancreat Sci (2016) 23: 181–18710.1002/jhbp.322
- 33SourrouilleI, GaujouxS, LacaveG et al. Five days of postoperative antimicrobial therapy decreases infectious complications following pancreaticoduodenectomy in patients at risk for bile contamination. HPB Off J Int Hepato Pancreato Biliary Assoc (2013) 15: 473–48010.1111/hpb.12012
- 34AugensteinVA, ReuterNP, BowerMR et al. Bile cultures: a guide to infectious complications after pancreaticoduodenectomy. J Surg Oncol (2010) 102: 478–48110.1002/jso.2161220872951
- 35LermiteE, PessauxP, TeyssedouC et al. Effect of preoperative endoscopic biliary drainage on infectious morbidity after pancreatoduodenectomy: a case-control study. Am J Surg (2008) 195: 442–44610.1016/j.amjsurg.2007.03.01618304506
- 36SudoT, MurakamiY, UemuraK et al. Specific antibiotic prophylaxis based on bile cultures is required to prevent postoperative infectious complications in pancreatoduodenectomy patients who have undergone preoperative biliary drainage. World J Surg (2007) 31: 2230–223510.1007/s00268-007-9210-417726628
- 37HowardTJ, YuJ, GreeneRB et al. Influence of bactibilia after preoperative biliary stenting on postoperative infectious complications. J Gastrointest Surg Off J Soc Surg Aliment Tract (2006) 10: 523–53110.1016/j.gassur.2005.08.011
10.1016/j.gassur.2005.08.011 Google Scholar
- 38KarstenTM, AllemaJH, ReindersM et al. Preoperative biliary drainage, colonisation of bile and postoperative complications in patients with tumours of the pancreatic head: a retrospective analysis of 241 consecutive patients. Eur J Surg Acta chirurgica (1996) 162: 881–8888956957
- 39KirklandKB, BriggsJP, TrivetteSL et al. The impact of surgical-site infections in the 1990s: attributable mortality, excess length of hospitalization, and extra costs. Infect Control Hosp Epidemiol (1999) 20: 725–73010.1086/50157210580621
- 40RerknimitrR, FogelEL, KalayciC et al. Microbiology of bile in patients with cholangitis or cholestasis with and without plastic biliary endoprosthesis. Gastrointest Endosc (2002) 56: 885–88910.1016/S0016-5107(02)70365-912447303
- 41MelzerM, TonerR, LaceyS et al. Biliary tract infection and bacteraemia: presentation, structural abnormalities, causative organisms and clinical outcomes. Postgrad Med J (2007) 83: 773–77610.1136/pgmj.2007.06468318057178
- 42den HoedPT, BoelhouwerRU, VeenHF et al. Infections and bacteriological data after laparoscopic and open gallbladder surgery. J Hosp Infect (1998) 39: 27–3710.1016/S0195-6701(98)90240-7
- 43HambraeusA, LaurellG, NybackaO et al. Biliary tract surgery: a bacteriologic and epidemiologic study. Acta Chir Scand (1990) 156: 155–1622330794
- 44KwonW, JangJY, KimEC et al. Changing trend in bile microbiology and antibiotic susceptibilities: over 12 years of experience. Infection (2013) 41: 93–10210.1007/s15010-012-0358-y23180506
- 45McBrideSJ, UptonA, RobertsSA Clinical characteristics and outcomes of patients with vancomycin-susceptible Enterococcus faecalis and Enterococcus faecium bacteraemiaߝa five-year retrospective review. Eur J Clin Microbiol Infect Dis Off Public Eur Soc Clin Microbiol (2010) 29: 107–11410.1007/s10096-009-0830-5
- 46Caballero-GranadoFJ, BecerrilB, CuberosL et al. Attributable mortality rate and duration of hospital stay associated with enterococcal bacteremia. Clin Infect Dis Off Publ Infect Dis Soc Am (2001) 32: 587–59410.1086/318717
- 47FongZV, McMillanMT, MarchegianiG et al. Discordance between perioperative antibiotic prophylaxis and wound infection cultures in patients undergoing pancreaticoduodenectomy. JAMA Surg (2016) 151: 432–43910.1001/jamasurg.2015.451026720272
- 48GavazziF, RidolfiC, CaprettiG et al. Role of preoperative biliary stents, bile contamination and antibiotic prophylaxis in surgical site infections after pancreaticoduodenectomy. BMC Gastroenterol (2016) 16: 4310.1186/s12876-016-0460-127036376
- 49LiuC, LuJW, DuZQ et al. Association of preoperative biliary drainage with postoperative morbidity after pancreaticoduodenectomy. Gastroenterol Res Pract (2015) 2015: 79689326798333
- 50MohammedS, EvansC, VanBurenG et al. Treatment of bacteriobilia decreases wound infection rates after pancreaticoduodenectomy. HPB Off J Int Hepato Pancreato Biliary Assoc (2014) 16: 592–59810.1111/hpb.12170
- 51NguW, JonesM, NealCP et al. Preoperative biliary drainage for distal biliary obstruction and post-operative infectious complications. ANZ J Surg (2013) 83: 280–28610.1111/j.1445-2197.2012.06296.x23043467
- 52SinghirunnusornJ, RogerL, Chopin-LalyX et al. Value of preoperative biliary drainage in a consecutive series of resectable periampullary lesions. From randomized studies to real medical practice. Langenbeck’s Arch Surg Deutsche Ges Chir (2013) 398: 295–30210.1007/s00423-012-1000-2
