Spontaneous bacterial peritonitis: The clinical challenge of a leaky gut and a cirrhotic liver

World Journal of Hepatology

Volumn 7, Issue 3, 2015, Pages 304-314

  Lutz, Philipp ^a,b   Nischalke, Hans Dieter ^a   Strassburg, Christian P ^a,b   Spengler, Ulrich ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Ascites; Cirrhosis; Farnesoid X receptor; Liver; Nucleotide binding oligomerization domain containing 2; Prophylaxis; Rifaximin; Spontaneous bacterial peritonitis; Toll like receptor 2

Indexed keywords

EID: 84928954300     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v7.i3.304     Document Type: Article

References (127)

1. Conn HO. Spontaneous peritonitis and bacteremia in laennec's cirrhosis caused by enteric organisms. a relatively common but rarely recognized syndrome. Ann Intern Med 1964; 60: 568-580 [PMID: 14138877 DOI: 10.7326/0003-4819-60-4-568]
2. Singal AK, Salameh H, Kamath PS. Prevalence and in-hospital mortality trends of infections among patients with cirrhosis: a nationwide study of hospitalised patients in the United States. Aliment Pharmacol Ther 2014; 40: 105-112 [PMID: 24832591 DOI: 10.1111/apt.12797]
3. Evans LT, Kim WR, Poterucha JJ, Kamath PS. Spontaneous bacterial peritonitis in asymptomatic outpatients with cirrhotic ascites. Hepatology 2003; 37: 897-901 [PMID: 12668984 DOI:10.1053/jhep.2003.50119]
4. Cadranel JF, Nousbaum JB, Bessaguet C, Nahon P, Nguyen-Khac E, Moreau R, Thévenot T, Silvain C, Bureau C, Nouel O, Pilette C, Paupard T, Pauwels A, Sapey T, Grangé JD, Tran A. Low incidence of spontaneous bacterial peritonitis in asymptomatic cirrhotic outpatients. World J Hepatol 2013; 5: 104-108 [PMID: 23556041 DOI: 10.4254/wjh.v5.i3.104]
5. Saab S, Hernandez JC, Chi AC, Tong MJ. Oral antibiotic prophylaxis reduces spontaneous bacterial peritonitis occurrence and improves short-term survival in cirrhosis: a meta-analysis. Am J Gastroenterol 2009; 104: 993-1001; quiz 1002 [PMID: 19277033 DOI: 10.1038/ajg.2009.3]
6. European Association for the Study of the Liver. EASL clinical practice guidelines on the management of ascites, spontaneous bacterial peritonitis, and hepatorenal syndrome in cirrhosis. J Hepatol 2010; 53: 397-417 [PMID: 20633946 DOI: 10.1016/ j.jhep.2010.05.004]
7. Runyon BA. Introduction to the revised American Association for the Study of Liver Diseases Practice Guideline management of adult patients with ascites due to cirrhosis 2012. Hepatology 2013; 57: 1651-1653 [PMID: 23463403 DOI: 10.1002/hep.26359]
8. Tandon P, Garcia-Tsao G. Renal dysfunction is the most important independent predictor of mortality in cirrhotic patients with spontaneous bacterial peritonitis. Clin Gastroenterol Hepatol 2011; 9: 260-265 [PMID: 21145427 DOI: 10.1016/j.cgh.2010.11.038]
9. Tandon P, Kumar D, Seo YS, Chang HJ, Chaulk J, Carbonneau M, Qamar H, Keough A, Mansoor N, Ma M. The 22/11 risk prediction model: a validated model for predicting 30-day mortality in patients with cirrhosis and spontaneous bacterial peritonitis. Am J Gastroenterol 2013; 108: 1473-1479 [PMID: 23877350 DOI:10.1038/ajg.2013.204]
10. Fernández J, Acevedo J, Castro M, Garcia O, de Lope CR, Roca D, Pavesi M, Sola E, Moreira L, Silva A, Seva-Pereira T, Corradi F, Mensa J, Ginès P, Arroyo V. Prevalence and risk factors of infections by multiresistant bacteria in cirrhosis: a prospective study. Hepatology 2012; 55: 1551-1561 [PMID: 22183941 DOI:10.1002/hep.25532]
11. Karlas T, Wiegand J, Berg T. Gastrointestinal complications of obesity: non-alcoholic fatty liver disease (NAFLD) and its sequelae. Best Pract Res Clin Endocrinol Metab 2013; 27: 195-208 [PMID:23731881 DOI: 10.1016/j.beem.2013.02.002]
12. Mandorfer M, Bota S, Schwabl P, Bucsics T, Pfisterer N, Kruzik M, Hagmann M, Blacky A, Ferlitsch A, Sieghart W, Trauner M, Peck-Radosavljevic M, Reiberger T. Nonselective β blockers increase risk for hepatorenal syndrome and death in patients with cirrhosis and spontaneous bacterial peritonitis. Gastroenterology 2014; 146:1680-90.e1 [PMID: 24631577 DOI: 10.1053/j.gastro.2014.03.005]
13. Piroth L, Pechinot A, Minello A, Jaulhac B, Patry I, Hadou T, Hansmann Y, Rabaud C, Chavanet P, Neuwirth C. Bacterial epidemiology and antimicrobial resistance in ascitic fluid: a 2-year retrospective study. Scand J Infect Dis 2009; 41: 847-851 [PMID:19922067 DOI: 10.3109/00365540903244535]
14. Cheong HS, Kang CI, Lee JA, Moon SY, Joung MK, Chung DR, Koh KC, Lee NY, Song JH, Peck KR. Clinical significance and outcome of nosocomial acquisition of spontaneous bacterial peritonitis in patients with liver cirrhosis. Clin Infect Dis 2009; 48:1230-1236 [PMID: 19302016 DOI: 10.1086/597585]
15. Lee YY, Tee HP, Mahadeva S. Role of prophylactic antibiotics in cirrhotic patients with variceal bleeding. World J Gastroenterol 2014; 20: 1790-1796 [PMID: 24587656 DOI: 10.3748/wjg.v20. i7.1790]
16. Wiest R, Krag A, Gerbes A. Spontaneous bacterial peritonitis:recent guidelines and beyond. Gut 2012; 61: 297-310 [PMID:22147550 DOI: 10.1136/gutjnl-2011-300779]
17. Wiest R, Lawson M, Geuking M. Pathological bacterial translocation in liver cirrhosis. J Hepatol 2014; 60: 197-209 [PMID:23993913 DOI: 10.1016/j.jhep.2013.07.044]
18. Guarner C, González-Navajas JM, Sánchez E, Soriando G, Francés R, Chiva M, Zapater P, Benlloch S, Muñoz C, Pascual S, Balanzó J, Pérez-Mateo M, Such J. The detection of bacterial DNA in blood of rats with CCl4-induced cirrhosis with ascites represents episodes of bacterial translocation. Hepatology 2006; 44: 633-639 [PMID: 16941689 DOI: 10.1002/hep.21286]
19. Llovet JM, Bartolí R, March F, Planas R, Viñado B, Cabré E, Arnal J, Coll P, Ausina V, Gassull MA. Translocated intestinal bacteria cause spontaneous bacterial peritonitis in cirrhotic rats: molecular epidemiologic evidence. J Hepatol 1998; 28: 307-313 [PMID:9580278 DOI: 10.1016/0168-8278(88)80018-7]
20. Cirera I, Bauer TM, Navasa M, Vila J, Grande L, Taurá P, Fuster J, García-Valdecasas JC, Lacy A, Suárez MJ, Rimola A, Rodés J. Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol 2001; 34: 32-37 [PMID: 11211904 DOI:10.1016/S0168-8278(00)00013-1]
21. Albillos A, de la Hera A, González M, Moya JL, Calleja JL, Monserrat J, Ruiz-del-Arbol L, Alvarez-Mon M. Increased lipopolysaccharide binding protein in cirrhotic patients with marked immune and hemodynamic derangement. Hepatology 2003; 37:208-217 [PMID: 12500206 DOI: 10.1053/jhep.2003.50038]
22. Such J, Francés R, Muñoz C, Zapater P, Casellas JA, Cifuentes A, Rodríguez-Valera F, Pascual S, Sola-Vera J, Carnicer F, Uceda F, Palazón JM, Pérez-Mateo M. Detection and identification of bacterial DNA in patients with cirrhosis and culture-negative, nonneutrocytic ascites. Hepatology 2002; 36: 135-141 [PMID:12085357 DOI: 10.1053/jhep.2002.33715]
23. Rogers GB, van der Gast CJ, Bruce KD, Marsh P, Collins JE, Sutton J, Wright M. Ascitic microbiota composition is correlated with clinical severity in cirrhosis with portal hypertension. PLoS One 2013; 8: e74884 [PMID: 24086392 DOI: 10.1371/journal. pone.0074884]
24. Ashley BD, Noone M, Dwarakanath AD, Malnick H. Fatal Pasteurella dagmatis peritonitis and septicaemia in a patient with cirrhosis: a case report and review of the literature. J Clin Pathol 2004; 57: 210-212 [PMID: 14747455 DOI: 10.1136/jcp.2003.7419]
25. Lutz P, Parcina M, Bekeredjian-Ding I, Hoerauf A, Strassburg CP, Spengler U. Spontaneous bacterial peritonitis by Pasteurella multocida under treatment with rifaximin. Infection 2014; 42:175-177 [PMID: 23526308 DOI: 10.1007/s15010-013-0449-4]
26. Lee YL, Shih SD, Weng YJ, Chen C, Liu CE. Fatal spontaneous bacterial peritonitis and necrotizing fasciitis with bacteraemia caused by Bacillus cereus in a patient with cirrhosis. J Med Microbiol 2010; 59: 242-244 [PMID: 19850708 DOI: 10.1099/ jmm.0.011056-0]
27. Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, Guo J, Le Chatelier E, Yao J, Wu L, Zhou J, Ni S, Liu L, Pons N, Batto JM, Kennedy SP, Leonard P, Yuan C, Ding W, Chen Y, Hu X, Zheng B, Qian G, Xu W, Ehrlich SD, Zheng S, Li L. Alterations of the human gut microbiome in liver cirrhosis. Nature 2014; 513: 59-64 [PMID:25079328 DOI: 10.1038/nature13568]
28. Seki E, Schnabl B. Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut. J Physiol 2012; 590:447-458 [PMID: 22124143 DOI: 10.1113/jphysiol.2011.219691]
29. Su GL, Rahemtulla A, Thomas P, Klein RD, Wang SC, Nanji AA. CD14 and lipopolysaccharide binding protein expression in a rat model of alcoholic liver disease. Am J Pathol 1998; 152: 841-849 [PMID: 9502426]
30. Nakatani Y, Fukui H, Kitano H, Nagamoto I, Tsujimoto T, Kuriyama S, Kikuchi E, Hoppou K, Tsujii T. Endotoxin clearance and its relation to hepatic and renal disturbances in rats with liver cirrhosis. Liver 2001; 21: 64-70 [PMID: 11169075 DOI: 10.1034/ j.1600-0676.2001.210110.x]
31. Reiberger T, Ferlitsch A, Payer BA, Mandorfer M, Heinisch BB, Hayden H, Lammert F, Trauner M, Peck-Radosavljevic M, Vogelsang H. Non-selective betablocker therapy decreases intestinal permeability and serum levels of LBP and IL-6 in patients with cirrhosis. J Hepatol 2013; 58: 911-921 [PMID: 23262249 DOI:10.1016/j.jhep.2012.12.011]
32. Fukui H, Matsumoto M, Tsujita S, Takaya A, Kojima H, Matsumura M, Tsujii T. Plasma endotoxin concentration and endotoxin binding capacity of plasma acute phase proteins in cirrhotics with variceal bleeding: an analysis by new methods. J Gastroenterol Hepatol 1994; 9: 582-586 [PMID: 7532449 DOI:10.1111/j.1440-1746.1994.tb01565.x]
33. El-Naggar MM, Khalil el-SA, El-Daker MA, Salama MF. Bacterial DNA and its consequences in patients with cirrhosis and culturenegative, non-neutrocytic ascites. J Med Microbiol 2008; 57:1533-1538 [PMID: 19018026 DOI: 10.1099/jmm.0.2008/001867-0]
34. Jain L, Sharma BC, Sharma P, Srivastava S, Agrawal A, Sarin SK. Serum endotoxin and inflammatory mediators in patients with cirrhosis and hepatic encephalopathy. Dig Liver Dis 2012; 44:1027-1031 [PMID: 22883217 DOI: 10.1016/j.dld.2012.07.002]
35. Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology 2014; 146:1513-1524 [PMID: 24440671 DOI: 10.1053/j.gastro.2014.01.020]
36. Pijls KE, Jonkers DM, Elamin EE, Masclee AA, Koek GH. Intestinal epithelial barrier function in liver cirrhosis: an extensive review of the literature. Liver Int 2013; 33: 1457-1469 [PMID:23879434 DOI: 10.1111/liv.12271]
37. Sipeki N, Antal-Szalmas P, Lakatos PL, Papp M. Immune dysfunction in cirrhosis. World J Gastroenterol 2014; 20: 2564-2577 [PMID: 24627592 DOI: 10.3748/wjg.v20.i10.2564]
38. Dukowicz AC, Lacy BE, Levine GM. Small intestinal bacterial overgrowth: a comprehensive review. Gastroenterol Hepatol (N Y) 2007; 3: 112-122 [PMID: 21960820]
39. Pande C, Kumar A, Sarin SK. Small-intestinal bacterial overgrowth in cirrhosis is related to the severity of liver disease. Aliment Pharmacol Ther 2009; 29: 1273-1281 [PMID: 19302262 DOI:10.1111/j.1365-2036.2009.03994.x]
40. Bauer TM, Schwacha H, Steinbrückner B, Brinkmann FE, Ditzen AK, Aponte JJ, Pelz K, Berger D, Kist M, Blum HE. Small intestinal bacterial overgrowth in human cirrhosis is associated with systemic endotoxemia. Am J Gastroenterol 2002; 97: 2364-2370 [PMID: 12358257 DOI: 10.1111/j.1572-0241.2002.05791.x]
41. Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, White MB, Monteith P, Noble NA, Sikaroodi M, Gillevet PM. Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol 2012; 303: G675-G685 [PMID: 22821944 DOI: 10.1152/ajpgi.00152.2012]
42. Bajaj JS, Heuman DM, Sanyal AJ, Hylemon PB, Sterling RK, Stravitz RT, Fuchs M, Ridlon JM, Daita K, Monteith P, Noble NA, White MB, Fisher A, Sikaroodi M, Rangwala H, Gillevet PM. Modulation of the metabiome by rifaximin in patients with cirrhosis and minimal hepatic encephalopathy. PLoS One 2013; 8: e60042 [PMID: 23565181 DOI: 10.1371/journal.pone.0060042]
43. Kao CY, Lin WH, Tseng CC, Wu AB, Wang MC, Wu JJ. The complex interplay among bacterial motility and virulence factors in different Escherichia coli infections. Eur J Clin Microbiol Infect Dis 2014; 33: 2157-2162 [PMID: 24957011 DOI: 10.1007/ s10096-014-2171-2]
44. Soriano G, Coll P, Guarner C, Such J, Sánchez F, Prats G, Vilardell F. Escherichia coli capsular polysaccharide and spontaneous bacterial peritonitis in cirrhosis. Hepatology 1995; 21: 668-673 [PMID: 7875665 DOI: 10.1002/hep.1840210311]
45. Wang MC, Lin WH, Tseng CC, Wu AB, Teng CH, Yan JJ, Wu JJ. Role of K1 capsule antigen in cirrhotic patients with Escherichia coli spontaneous bacterial peritonitis in southern Taiwan. Eur J Clin Microbiol Infect Dis 2013; 32: 407-412 [PMID: 23052990 DOI:10.1007/s10096-012-1757-9]
46. Fouts DE, Torralba M, Nelson KE, Brenner DA, Schnabl B. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J Hepatol 2012; 56: 1283-1292 [PMID: 22326468 DOI: 10.1016/j.jhep.2012.01.019]
47. White JS, Hoper M, Parks RW, Clements WD, Diamond T. Patterns of bacterial translocation in experimental biliary obstruction. J Surg Res 2006; 132: 80-84 [PMID: 16154151 DOI: 10.1016/ j.jss.2005.07.026]
48. Inamura T, Miura S, Tsuzuki Y, Hara Y, Hokari R, Ogawa T, Teramoto K, Watanabe C, Kobayashi H, Nagata H, Ishii H. Alteration of intestinal intraepithelial lymphocytes and increased bacterial translocation in a murine model of cirrhosis. Immunol Lett 2003; 90: 3-11 [PMID: 14611901 DOI: 10.1016/ j.imlet.2003.05.002]
49. Campillo B, Pernet P, Bories PN, Richardet JP, Devanlay M, Aussel C. Intestinal permeability in liver cirrhosis: relationship with severe septic complications. Eur J Gastroenterol Hepatol 1999; 11: 755-759 [PMID:10445796 DOI: 10.1097/00042737-199907000-00013]
50. Pascual S, Such J, Esteban A, Zapater P, Casellas JA, Aparicio JR, Girona E, Gutiérrez A, Carnices F, Palazón JM, Sola-Vera J, Pérez-Mateo M. Intestinal permeability is increased in patients with advanced cirrhosis. Hepatogastroenterology 2003; 50: 1482-1486 [PMID: 14571769]
51. Modica S, Gadaleta RM, Moschetta A. Deciphering the nuclear bile acid receptor FXR paradigm. Nucl Recept Signal 2010; 8: e005 [PMID: 21383957 DOI: 10.1621/nrs.08005]
52. Inagaki T, Moschetta A, Lee YK, Peng L, Zhao G, Downes M, Yu RT, Shelton JM, Richardson JA, Repa JJ, Mangelsdorf DJ, Kliewer SA. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc Natl Acad Sci USA 2006; 103:3920-3925 [PMID: 16473946 DOI: 10.1073/pnas.0509592103]
53. Verbeke L, Farre R, Trebicka J, Komuta M, Roskams T, Klein S, Elst IV, Windmolders P, Vanuytsel T, Nevens F, Laleman W. Obeticholic acid, a farnesoid X receptor agonist, improves portal hypertension by two distinct pathways in cirrhotic rats. Hepatology 2014; 59: 2286-2298 [PMID: 24259407 DOI: 10.1002/hep.26939]
54. Lutz P, Berger C, Langhans B, Grünhage F, Appenrodt B, Nattermann J, Lammert F, Hoerauf A, Sauerbruch T, Strassburg CP, Spengler U, Nischalke HD. A farnesoid X receptor polymorphism predisposes to spontaneous bacterial peritonitis. Dig Liver Dis 2014; 46: 1047-1050 [PMID: 25086996 DOI: 10.1016/j.dld.2014.07.008]
55. Appenrodt B, Grünhage F, Gentemann MG, Thyssen L, Sauerbruch T, Lammert F. Nucleotide-binding oligomerization domain containing 2 (NOD2) variants are genetic risk factors for death and spontaneous bacterial peritonitis in liver cirrhosis. Hepatology 2010; 51: 1327-1333 [PMID: 20087966 DOI: 10.1002/ hep.23440]
56. Bruns T, Peter J, Reuken PA, Grabe DH, Schuldes SR, Brenmoehl J, Schölmerich J, Wiest R, Stallmach A. NOD2 gene variants are a risk factor for culture-positive spontaneous bacterial peritonitis and monomicrobial bacterascites in cirrhosis. Liver Int 2012; 32: 223-230 [PMID: 21745302 DOI: 10.1111/j.1478-3231.2011.02561.x]
57. Strober W, Watanabe T. NOD2, an intracellular innate immune sensor involved in host defense and Crohn's disease. Mucosal Immunol 2011; 4: 484-495 [PMID: 21750585 DOI: 10.1038/ mi.2011.29]
58. Senzolo M, Cholongitas E, Burra P, Leandro G, Thalheimer U, Patch D, Burroughs AK. beta-Blockers protect against spontaneous bacterial peritonitis in cirrhotic patients: a meta-analysis. Liver Int 2009; 29: 1189-1193 [PMID: 19508620 DOI: 10.1111/ j.1478-3231.2009.02038.x]
59. Rössle M. TIPS: 25 years later. J Hepatol 2013; 59: 1081-1093 [PMID: 23811307 DOI: 10.1016/j.jhep.2013.06.014]
60. Salerno F, Cammà C, Enea M, Rössle M, Wong F. Transjugular intrahepatic portosystemic shunt for refractory ascites: a metaanalysis of individual patient data. Gastroenterology 2007; 133:825-834 [PMID: 17678653 DOI: 10.1053/j.gastro.2007.06.020]
61. Nischalke HD, Berger C, Aldenhoff K, Thyssen L, Gentemann M, Grünhage F, Lammert F, Nattermann J, Sauerbruch T, Spengler U, Appenrodt B. Toll-like receptor (TLR) 2 promoter and intron 2 polymorphisms are associated with increased risk for spontaneous bacterial peritonitis in liver cirrhosis. J Hepatol 2011; 55:1010-1016 [PMID: 21356257 DOI: 10.1016/j.jhep.2011.02.022]
62. Gäbele E, Mühlbauer M, Paulo H, Johann M, Meltzer C, Leidl F, Wodarz N, Wiest R, Schölmerich J, Hellerbrand C. Analysis of monocyte chemotactic protein-1 gene polymorphism in patients with spontaneous bacterial peritonitis. World J Gastroenterol 2009; 15: 5558-5562 [PMID: 19938194 DOI: 10.3748/wjg.15.5558]
63. Salama MK, Sabry D, Al-Ghussein MA, Ahmed R, AbdAllah S, Taha FM, Fathy W, Wadie MS, Nabih M, Abul-Fotouh A, Darwish T. Molecular detection of monocyte chemotactic protein-1 polymorphism in spontaneous bacterial peritonitis patients. World J Gastroenterol 2014; 20: 11793-11799 [PMID: 25206284 DOI:10.3748/wjg.v20.i33.11793]
64. Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 2009; 21: 317-337 [PMID: 19246554 DOI: 10.1093/intimm/dxp017]
65. Gu L, Rutledge B, Fiorillo J, Ernst C, Grewal I, Flavell R, Gladue R, Rollins B. In vivo properties of monocyte chemoattractant protein-1. J Leukoc Biol 1997; 62: 577-580 [PMID: 9365111]
66. Rovin BH, Lu L, Saxena R. A novel polymorphism in the MCP-1 gene regulatory region that influences MCP-1 expression. Biochem Biophys Res Commun 1999; 259: 344-348 [PMID: 10362511 DOI:10.1006/bbrc.1999.0796]
67. Taylor NJ, Manakkat Vijay GK, Abeles RD, Auzinger G, Bernal W, Ma Y, Wendon JA, Shawcross DL. The severity of circulating neutrophil dysfunction in patients with cirrhosis is associated with 90-day and 1-year mortality. Aliment Pharmacol Ther 2014; 40:705-715 [PMID: 25060167 DOI: 10.1111/apt.12886]
68. Ono Y, Watanabe T, Matsumoto K, Ito T, Kunii O, Goldstein E. Opsonophagocytic dysfunction in patients with liver cirrhosis and low responses to tumor necrosis factor-alpha and lipopolysaccharide in patients' blood. J Infect Chemother 2004; 10: 200-207 [PMID:15365859 DOI: 10.1007/s10156-004-0321-7]
69. Schirren CA, Jung MC, Zachoval R, Diepolder H, Hoffmann R, Riethmüller G, Pape GR. Analysis of T cell activation pathways in patients with liver cirrhosis, impaired delayed hypersensitivity and other T cell-dependent functions. Clin Exp Immunol 1997; 108: 144-150 [PMID: 9097923 DOI: 10.1046/j.1365-2249.1997. d01-985.x]
70. Kakazu E, Ueno Y, Kondo Y, Fukushima K, Shiina M, Inoue J, Tamai K, Ninomiya M, Shimosegawa T. Branched chain amino acids enhance the maturation and function of myeloid dendritic cells ex vivo in patients with advanced cirrhosis. Hepatology 2009; 50: 1936-1945 [PMID: 19885880 DOI: 10.1002/hep.23248]
71. Tapia-Abellán A, Martínez-Esparza M, Ruiz-Alcaraz AJ, Hernández-Caselles T, Martínez-Pascual C, Miras-López M, Such J, Francés R, García-Peñarrubia P. The peritoneal macrophage inflammatory profile in cirrhosis depends on the alcoholic or hepatitis C viral etiology and is related to ERK phosphorylation. BMC Immunol 2012; 13: 42 [PMID:22866973 DOI: 10.1186/1471-2172-13-42]
72. Runyon BA. Monomicrobial nonneutrocytic bacterascites: a variant of spontaneous bacterial peritonitis. Hepatology 1990; 12: 710-715 [PMID: 2210672 DOI: 10.1002/hep.1840120415]
73. Sugihara T, Koda M, Maeda Y, Matono T, Nagahara T, Mandai M, Ueki M, Murawaki Y. Rapid identification of bacterial species with bacterial DNA microarray in cirrhotic patients with spontaneous bacterial peritonitis. Intern Med 2009; 48: 3-10 [PMID: 19122350 DOI: 10.2169/internalmedicine.48.1539]
74. Bruns T, Sachse S, Straube E, Assefa S, Herrmann A, Hagel S, Lehmann M, Stallmach A. Identification of bacterial DNA in neutrocytic and non-neutrocytic cirrhotic ascites by means of a multiplex polymerase chain reaction. Liver Int 2009; 29: 1206-1214 [PMID: 19602138 DOI: 10.1111/j.1478-3231.2009.02073.x]
75. Appenrodt B, Lehmann LE, Thyssen L, Gentemann M, Rabe C, Molitor E, Trebicka J, Stüber F, Sauerbruch T. Is detection of bacterial DNA in ascitic fluid of clinical relevance? Eur J Gastroenterol Hepatol 2010; 22: 1487-1494 [PMID: 21048463 DOI: 10.1097/MEG.0b013e328340c43a]
76. Soriano G, Esparcia O, Montemayor M, Guarner-Argente C, Pericas R, Torras X, Calvo N, Román E, Navarro F, Guarner C, Coll P. Bacterial DNA in the diagnosis of spontaneous bacterial peritonitis. Aliment Pharmacol Ther 2011; 33: 275-284 [PMID:21083594 DOI: 10.1111/j.1365-2036.2010.04506.x]
77. Enomoto H, Inoue S, Matsuhisa A, Aizawa N, Imanishi H, Saito M, Iwata Y, Tanaka H, Ikeda N, Sakai Y, Takashima T, Shimomura S, Iijima H, Nakamura H, Nishiguchi S. Development of a new in situ hybridization method for the detection of global bacterial DNA to provide early evidence of a bacterial infection in spontaneous bacterial peritonitis. J Hepatol 2012; 56: 85-94 [PMID: 21835139 DOI: 10.1016/j.jhep.2011.06.025]
78. Jalan R, Fernandez J, Wiest R, Schnabl B, Moreau R, Angeli P, Stadlbauer V, Gustot T, Bernardi M, Canton R, Albillos A, Lammert F, Wilmer A, Mookerjee R, Vila J, Garcia-Martinez R, Wendon J, Such J, Cordoba J, Sanyal A, Garcia-Tsao G, Arroyo V, Burroughs A, Ginès P. Bacterial infections in cirrhosis: a position statement based on the EASL Special Conference 2013. J Hepatol 2014; 60:1310-1324 [PMID: 24530646 DOI: 10.1016/j.jhep.2014.01.024]
79. Ariza X, Castellote J, Lora-Tamayo J, Girbau A, Salord S, Rota R, Ariza J, Xiol X. Risk factors for resistance to ceftriaxone and its impact on mortality in community, healthcare and nosocomial spontaneous bacterial peritonitis. J Hepatol 2012; 56: 825-832 [PMID: 22173153 DOI: 10.1016/j.jhep.2011.11.010]
80. Mendler MH, Agarwal A, Trimzi M, Madrigal E, Tsushima M, Joo E, Santiago M, Flores E, David G, Workman A, Runyon B. A new highly sensitive point of care screen for spontaneous bacterial peritonitis using the leukocyte esterase method. J Hepatol 2010; 53:477-483 [PMID: 20646775 DOI: 10.1016/j.jhep.2010.04.011]
81. Burri E, Schulte F, Muser J, Meier R, Beglinger C. Measurement of calprotectin in ascitic fluid to identify elevated polymorphonuclear cell count. World J Gastroenterol 2013; 19: 2028-2036 [PMID:23599621 DOI: 10.3748/wjg.v19.i13.2028]
82. Sort P, Navasa M, Arroyo V, Aldeguer X, Planas R, Ruiz-del-Arbol L, Castells L, Vargas V, Soriano G, Guevara M, Ginès P, Rodés J. Effect of intravenous albumin on renal impairment and mortality in patients with cirrhosis and spontaneous bacterial peritonitis. N Engl J Med 1999; 341: 403-409 [PMID: 10432325 DOI: 10.1056/ NEJM199908053410603]
83. Reuken PA, Pletz MW, Baier M, Pfister W, Stallmach A, Bruns T. Emergence of spontaneous bacterial peritonitis due to enterococci - risk factors and outcome in a 12-year retrospective study. Aliment Pharmacol Ther 2012; 35: 1199-1208 [PMID: 22449290 DOI:10.1111/j.1365-2036.2012.05076.x]
84. Umgelter A, Reindl W, Miedaner M, Schmid RM, Huber W. Failure of current antibiotic first-line regimens and mortality in hospitalized patients with spontaneous bacterial peritonitis. Infection 2009; 37:2-8 [PMID: 19169633 DOI: 10.1007/s15010-008-8060-9]
85. Fernández J, Gustot T. Management of bacterial infections in cirrhosis. J Hepatol 2012; 56 Suppl 1: S1-12 [PMID: 22300459 DOI: 10.1016/S0168-8278(12)60002-6]
86. Piano S, Salinas F, Morando F, Cavalin M, Romano A, Rosi S, Stanco M, Fasolato S, Sticca A, Senzolo M, Burra P, Gringeri E, Cillo U, Gatta A, Angeli P. Poster Session 1: Infections and Acute on Chronic Liver Failure. Abstract 574: The empirical antibiotic treatment of nosocomial spontaneous bacterial peritonitis in patients with decompensated liver cirrhosis: results of a randomized controlled clinical trial. Hepatology 2014; 60: 478A-501A [DOI:10.1002/hep.27505]
87. Wong F, O'Leary JG, Reddy KR, Patton H, Kamath PS, Fallon MB, Garcia-Tsao G, Subramanian RM, Malik R, Maliakkal B, Thacker LR, Bajaj JS. New consensus definition of acute kidney injury accurately predicts 30-day mortality in patients with cirrhosis and infection. Gastroenterology 2013; 145: 1280128-8.e1 [PMID:23999172 DOI: 10.1053/j.gastro.2013.08.051]
88. Fernández J, Ruiz del Arbol L, Gómez C, Durandez R, Serradilla R, Guarner C, Planas R, Arroyo V, Navasa M. Norfloxacin vs ceftriaxone in the prophylaxis of infections in patients with advanced cirrhosis and hemorrhage. Gastroenterology 2006; 131: 1049-1056; quiz 1285 [PMID: 17030175 DOI: 10.1053/ j.gastro.2006.07.010]
89. Chavez-Tapia NC, Barrientos-Gutierrez T, Tellez-Avila FI, Soares-Weiser K, Uribe M. Antibiotic prophylaxis for cirrhotic patients with upper gastrointestinal bleeding. Cochrane Database Syst Rev 2010; (9): CD002907 [PMID: 20824832 DOI: 10.1002/14651858. CD002907.pub2]
90. Andreu M, Sola R, Sitges-Serra A, Alia C, Gallen M, Vila MC, Coll S, Oliver MI. Risk factors for spontaneous bacterial peritonitis in cirrhotic patients with ascites. Gastroenterology 1993; 104:1133-1138 [PMID: 8462803]
91. Such J, Guarner C, Enriquez J, Rodriguez JL, Seres I, Vilardell F. Low C3 in cirrhotic ascites predisposes to spontaneous bacterial peritonitis. J Hepatol 1988; 6: 80-84 [PMID: 3279108 DOI:10.1016/S0168-8278(88)80465-3]
92. Fernández J, Navasa M, Planas R, Montoliu S, Monfort D, Soriano G, Vila C, Pardo A, Quintero E, Vargas V, Such J, Ginès P, Arroyo V. Primary prophylaxis of spontaneous bacterial peritonitis delays hepatorenal syndrome and improves survival in cirrhosis. Gastroenterology 2007; 133: 818-824 [PMID: 17854593 DOI:10.1053/j.gastro.2007.06.065]
93. Ginés P, Rimola A, Planas R, Vargas V, Marco F, Almela M, Forné M, Miranda ML, Llach J, Salmerón JM. Norfloxacin prevents spontaneous bacterial peritonitis recurrence in cirrhosis: results of a double-blind, placebo-controlled trial. Hepatology 1990; 12:716-724 [PMID: 2210673 DOI: 10.1002/hep.1840120416]
94. Segarra-Newnham M, Henneman A. Antibiotic prophylaxis for prevention of spontaneous bacterial peritonitis in patients without gastrointestinal bleeding. Ann Pharmacother 2010; 44: 1946-1954 [PMID: 21098755 DOI: 10.1345/aph.1P317]
95. Tandon P, Delisle A, Topal JE, Garcia-Tsao G. High prevalence of antibiotic-resistant bacterial infections among patients with cirrhosis at a US liver center. Clin Gastroenterol Hepatol 2012; 10:1291-1298 [PMID: 22902776 DOI: 10.1016/j.cgh.2012.08.017]
96. Deshpande A, Pasupuleti V, Thota P, Pant C, Mapara S, Hassan S, Rolston DD, Sferra TJ, Hernandez AV. Acid-suppressive therapy is associated with spontaneous bacterial peritonitis in cirrhotic patients: a meta-analysis. J Gastroenterol Hepatol 2013; 28:235-242 [PMID: 23190338 DOI: 10.1111/jgh.12065]
97. Bajaj JS, Zadvornova Y, Heuman DM, Hafeezullah M, Hoffmann RG, Sanyal AJ, Saeian K. Association of proton pump inhibitor therapy with spontaneous bacterial peritonitis in cirrhotic patients with ascites. Am J Gastroenterol 2009; 104: 1130-1134 [PMID:19337238 DOI: 10.1038/ajg.2009.80]
98. Garcia-Martinez I, Francés R, Zapater P, Giménez P, Gómez-Hurtado I, Moratalla A, Lozano-Ruiz B, Bellot P, González-Navajas JM, Such J. Use of proton pump inhibitors decrease cellular oxidative burst in patients with decompensated cirrhosis. J Gastroenterol Hepatol 2015; 30: 147-154 [PMID: 25039465 DOI:10.1111/jgh.12667]
99. Bauer TM, Steinbrückner B, Brinkmann FE, Ditzen AK, Schwacha H, Aponte JJ, Pelz K, Kist M, Blum HE. Small intestinal bacterial overgrowth in patients with cirrhosis: prevalence and relation with spontaneous bacterial peritonitis. Am J Gastroenterol 2001; 96:2962-2967 [PMID: 11693333 DOI: 10.1111/j.1572-0241.2001.04668.x]
100. Zhang W, Gu Y, Chen Y, Deng H, Chen L, Chen S, Zhang G, Gao Z. Intestinal flora imbalance results in altered bacterial translocation and liver function in rats with experimental cirrhosis. Eur J Gastroenterol Hepatol 2010; 22: 1481-1486 [PMID: 20739895 DOI: 10.1097/MEG.0b013e32833eb8b0]
101. Sánchez E, Nieto JC, Boullosa A, Vidal S, Sancho FJ, Rossi G, Sancho-Bru P, Oms R, Mirelis B, Juárez C, Guarner C, Soriano G. VSL#3 probiotic treatment decreases bacterial translocation in rats with carbon tetrachloride-induced cirrhosis. Liver Int 2015; 35:735-745 [PMID: 24750552 DOI: 10.1111/liv.12566]
102. Pereg D, Kotliroff A, Gadoth N, Hadary R, Lishner M, Kitay-Cohen Y. Probiotics for patients with compensated liver cirrhosis: a double-blind placebo-controlled study. Nutrition 2011; 27: 177-181 [PMID: 20452184 DOI: 10.1016/j.nut.2010.01.006]
103. Pande C, Kumar A, Sarin SK. Addition of probiotics to norfloxacin does not improve efficacy in the prevention of spontaneous bacterial peritonitis: a double-blind placebo-controlled randomizedcontrolled trial. Eur J Gastroenterol Hepatol 2012; 24: 831-839 [PMID: 22522141 DOI: 10.1097/MEG.0b013e3283537d61]
104. Scarpignato C, Pelosini I. Rifaximin, a poorly absorbed antibiotic:pharmacology and clinical potential. Chemotherapy 2005; 51 Suppl 1: 36-66 [PMID: 15855748 DOI: 10.1159/000081990]
105. Bass NM, Mullen KD, Sanyal A, Poordad F, Neff G, Leevy CB, Sigal S, Sheikh MY, Beavers K, Frederick T, Teperman L, Hillebrand D, Huang S, Merchant K, Shaw A, Bortey E, Forbes WP. Rifaximin treatment in hepatic encephalopathy. N Engl J Med 2010; 362: 1071-1081 [PMID: 20335583 DOI: 10.1056/ NEJMoa0907893]
106. Eltawil KM, Laryea M, Peltekian K, Molinari M. Rifaximin vs. conventional oral therapy for hepatic encephalopathy: a metaanalysis. World J Gastroenterol 2012; 18: 767-777 [PMID:22371636 DOI: 10.3748/wjg.v18.i8.767]
107. DuPont HL, Jiang ZD. Influence of rifaximin treatment on the susceptibility of intestinal Gram-negative flora and enterococci. Clin Microbiol Infect 2004; 10: 1009-1011 [PMID: 15522005 DOI:10.1111/j.1469-0691.2004.00997.x]
108. Vlachogiannakos J, Viazis N, Vasianopoulou P, Vafiadis I, Karamanolis DG, Ladas SD. Long-term administration of rifaximin improves the prognosis of patients with decompensated alcoholic cirrhosis. J Gastroenterol Hepatol 2013; 28: 450-455 [PMID:23216382 DOI: 10.1111/jgh.12070]
109. Hanouneh MA, Hanouneh IA, Hashash JG, Law R, Esfeh JM, Lopez R, Hazratjee N, Smith T, Zein NN. The role of rifaximin in the primary prophylaxis of spontaneous bacterial peritonitis in patients with liver cirrhosis. J Clin Gastroenterol 2012; 46: 709-715 [PMID: 22878533 DOI: 10.1097/MCG.0b013e3182506dbb]
110. Lutz P, Parcina M, Bekeredjian-Ding I, Nischalke HD, Nattermann J, Sauerbruch T, Hoerauf A, Strassburg CP, Spengler U. Impact of rifaximin on the frequency and characteristics of spontaneous bacterial peritonitis in patients with liver cirrhosis and ascites. PLoS One 2014; 9: e93909 [PMID: 24714550 DOI: 10.1371/journal. pone.0093909]
111. Valentin T, Leitner E, Rohn A, Zollner-Schwetz I, Hoenigl M, Salzer HJ, Krause R. Rifaximin intake leads to emergence of rifampin-resistant staphylococci. J Infect 2011; 62: 34-38 [PMID:21073894 DOI: 10.1016/j.jinf.2010.11.004]
112. Kothary V, Scherl EJ, Bosworth B, Jiang ZD, Dupont HL, Harel J, Simpson KW, Dogan B. Rifaximin resistance in Escherichia coli associated with inflammatory bowel disease correlates with prior rifaximin use, mutations in rpoB, and activity of Phe-Arg-β-naphthylamide-inhibitable efflux pumps. Antimicrob Agents Chemother 2013; 57: 811-817 [PMID: 23183443 DOI: 10.1128/ AAC.02163-12]
113. Carman RJ, Boone JH, Grover H, Wickham KN, Chen L. In vivo selection of rifamycin-resistant Clostridium difficile during rifaximin therapy. Antimicrob Agents Chemother 2012; 56:6019-6020 [PMID: 22908175 DOI: 10.1128/AAC.00974-12]
114. Silveira MG, Lindor KD. Obeticholic acid and budesonide for the treatment of primary biliary cirrhosis. Expert Opin Pharmacother 2014; 15: 365-372 [PMID: 24382005 DOI: 10.1517/14656566.2014.873404]
115. Mudaliar S, Henry RR, Sanyal AJ, Morrow L, Marschall HU, Kipnes M, Adorini L, Sciacca CI, Clopton P, Castelloe E, Dillon P, Pruzanski M, Shapiro D. Efficacy and safety of the farnesoid X receptor agonist obeticholic acid in patients with type 2 diabetes and nonalcoholic fatty liver disease. Gastroenterology 2013; 145:574-582.e1 [PMID: 23727264 DOI: 10.1053/j.gastro.2013.05.042]
116. Obstein KL, Campbell MS, Reddy KR, Yang YX. Association between model for end-stage liver disease and spontaneous bacterial peritonitis. Am J Gastroenterol 2007; 102: 2732-2736 [PMID:17714556 DOI: 10.1111/j.1572-0241.2007.01485.x]
117. Felisart J, Rimola A, Arroyo V, Perez-Ayuso RM, Quintero E, Gines P, Rodes J. Cefotaxime is more effective than is ampicillintobramycin in cirrhotics with severe infections. Hepatology 1985; 5:457-462 [PMID: 3888810 DOI: 10.1002/hep.1840050319]
118. Rimola A, Salmerón JM, Clemente G, Rodrigo L, Obrador A, Miranda ML, Guarner C, Planas R, Solá R, Vargas V. Two different dosages of cefotaxime in the treatment of spontaneous bacterial peritonitis in cirrhosis: results of a prospective, randomized, multicenter study. Hepatology 1995; 21: 674-679 [PMID: 7875666 DOI: 10.1002/hep.1840210312]
119. Navasa M, Follo A, Llovet JM, Clemente G, Vargas V, Rimola A, Marco F, Guarner C, Forné M, Planas R, Bañares R, Castells L, Jimenez De Anta MT, Arroyo V, Rodés J. Randomized, comparative study of oral ofloxacin versus intravenous cefotaxime in spontaneous bacterial peritonitis. Gastroenterology 1996; 111: 1011-1017 [PMID:8831596 DOI: 10.1016/S0016-5085(96)70069-0]
120. Ricart E, Soriano G, Novella MT, Ortiz J, Sàbat M, Kolle L, Sola-Vera J, Miñana J, Dedéu JM, Gómez C, Barrio JL, Guarner C. Amoxicillin-clavulanic acid versus cefotaxime in the therapy of bacterial infections in cirrhotic patients. J Hepatol 2000; 32:596-602 [PMID: 10782908 DOI: 10.1016/S0168-8278(00)80221-4]
121. Terg R, Cobas S, Fassio E, Landeira G, Ríos B, Vasen W, Abecasis R, Ríos H, Guevara M. Oral ciprofloxacin after a short course of intravenous ciprofloxacin in the treatment of spontaneous bacterial peritonitis: results of a multicenter, randomized study. J Hepatol 2000; 33: 564-569 [PMID: 11059861 DOI: 10.1016/ S0168-8278(00)80008-2]
122. Soriano G, Guarner C, Teixidó M, Such J, Barrios J, Enríquez J, Vilardell F. Selective intestinal decontamination prevents spontaneous bacterial peritonitis. Gastroenterology 1991; 100:477-481 [PMID: 1985045]
123. Singh N, Gayowski T, Yu VL, Wagener MM. Trimethoprimsulfamethoxazole for the prevention of spontaneous bacterial peritonitis in cirrhosis: a randomized trial. Ann Intern Med 1995; 122: 595-598 [PMID: 7887554 DOI: 10.7326/0003-4819-122-8-199504150-00007]
124. Grangé JD, Roulot D, Pelletier G, Pariente EA, Denis J, Ink O, Blanc P, Richardet JP, Vinel JP, Delisle F, Fischer D, Flahault A, Amiot X. Norfloxacin primary prophylaxis of bacterial infections in cirrhotic patients with ascites: a double-blind randomized trial. J Hepatol 1998; 29: 430-436 [PMID: 9764990 DOI: 10.1016/ S0168-8278(98)80061-5]
125. Rolachon A, Cordier L, Bacq Y, Nousbaum JB, Franza A, Paris JC, Fratte S, Bohn B, Kitmacher P, Stahl JP. Ciprofloxacin and long-term prevention of spontaneous bacterial peritonitis: results of a prospective controlled trial. Hepatology 1995; 22: 1171-1174 [PMID: 7557868]
126. Novella M, Solà R, Soriano G, Andreu M, Gana J, Ortiz J, Coll S, Sàbat M, Vila MC, Guarner C, Vilardell F. Continuous versus inpatient prophylaxis of the first episode of spontaneous bacterial peritonitis with norfloxacin. Hepatology 1997; 25: 532-536 [PMID:9049193 DOI: 10.1002/hep.510250306]
127. Terg R, Fassio E, Guevara M, Cartier M, Longo C, Lucero R, Landeira C, Romero G, Dominguez N, Muñoz A, Levi D, Miguez C, Abecasis R. Ciprofloxacin in primary prophylaxis of spontaneous bacterial peritonitis: a randomized, placebo-controlled study. J Hepatol 2008; 48: 774-779 [PMID: 18316137 DOI: 10.1016/ j.jhep.2008.01.024]