Concise Review in Mechanisms of Disease

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Bacterial translocation (BT) in cirrhosis†

  1. Reiner Wiest1,
  2. Guadalupe Garcia-Tsao2,*

Article first published online: 18 FEB 2005

DOI: 10.1002/hep.20632

Issue

Hepatology

Hepatology

Volume 41, Issue 3, pages 422–433, March 2005

Additional Information

How to Cite

Wiest, R. and Garcia-Tsao, G. (2005), Bacterial translocation (BT) in cirrhosis. Hepatology, 41: 422–433. doi: 10.1002/hep.20632

Author Information

  1. 1

    Department of Internal Medicine I, University of Regensburg Hospital Franz-Josef-Strauss-Allee, Regensburg, Germany

  2. 2

    Yale University School of Medicine, New Haven, CT

*VA Connecticut Healthcare System and Section of Digestive Diseases, Yale University School of Medicine, 333 Cedar Street, 1080 CMP, P.O. Box 3333, New Haven, CT 06520-8019

  1. †

    Conflict of interest: Nothing to report.

Publication History

  1. Issue published online: 22 FEB 2005
  2. Article first published online: 18 FEB 2005
  3. Manuscript Accepted: 18 JAN 2005
  4. Manuscript Received: 30 SEP 2004

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References

  • 1
    Berg RD, Garlington AW. Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun 1979; 23: 403–411.
  • 2
    Garcia-Tsao G, Wiest R. Gut microflora in the pathogenesis of the complications of cirrhosis. Best Pract Res Clin Gastroenterol 2004; 18: 353–372.
  • 3
    Marteau P, Pochart P, Dore J, Bera-Maillet C, Bernalier A, Corthier G. Comparative study of bacterial groups within the human cecal and fecal microbiota. Appl Environ Microbiol 2001; 67: 4939–4942.
  • 4
    Steffen EK, Berg RD, Deitch EA. Comparison of translocation rates of various indigenous bacteria from the gastrointestinal tract to the mesenteric lymph node. J Infect Dis 1988; 157: 1032–1038.
  • 5
    Garcia-Tsao G. Spontaneous bacterial peritonitis. Gastroenterol Clin North Am 1991; 21: 257–275.
  • 6
    Ljungdahl M, Lundholm M, Katouli M, Rasmussen I, Engstrand L, Haglund U. Bacterial translocation in experimental shock is dependent on the strains in the intestinal flora. Scand J Gastroenterol 2000; 35: 389–397.
  • 7
    Alverdy J, Holbrook C, Rocha F, Seiden L, Wu RL, Musch M, et al. Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Ann Surg 2000; 232: 480–489.
  • 8
    Eaves-Pyles T, Alexander JW. Comparison of translocation of different types of microorganisms from the intestinal tract of burned mice. Shock 2001; 16: 148–152.
  • 9
    Steffen EK, Berg RD, Deitch EA. Comparison of translocation rates of various indigenous bacteria from the gastrointestinal tract to the mesenteric lymph node. J Infect Dis 1988; 157: 1032–1038.
  • 10
    Wells CL. Relationship between intestinal microecology and the translocation of intestinal bacteria. Antonie Van Leeuwenhoek 1990; 58: 87–93.
  • 11
    Wells CL. Colonization and translocation of intestinal bacterial flora. Transplant Proc 1996; 28: 2653–2656.
  • 12
    Wells CL, Maddaus MA, Reynolds CM, Jechorek RP, Simmons RL. Role of anaerobic flora in the translocation of aerobic and facultatively anaerobic intestinal bacteria. Infect Immun 1987; 55: 2689–2694.
  • 13
    Owens WE, Berg RD. Bacterial translocation from the gastrointestinal tract of athymic (nu/nu) mice. Infect Immun 1980; 27: 461–467.
  • 14
    Brook I, MacVittie TJ, Walker RI. Recovery of aerobic and anaerobic bacteria from irradiated mice. Infect Immun 1984; 46: 270–271.
  • 15
    Steffen EK, Berg RD. Relationship between cecal population levels of indigenous bacteria and translocation to the mesenteric lymph nodes. Infect Immun 1983; 39: 1252–1259.
  • 16
    Boedeker EC. Adherent bacteria: breaching the mucosal barrier? Gastroenterology 1994; 106: 255–257.
  • 17
    Bauer TM, Schwacha H, Steinbrückner B, Brinkmann FE, Ditzen AK, Aponte JJ, et al. Small intestinal bacterial overgrowth in human cirrhosis is associated with systemic endotoxemia. Am J Gastroenterol 2002; 97: 2364–2370.
    Direct Link:
  • 18
    Guarner C, Runyon BA, Young S, Heck M, Sheikh MY. Intestinal bacterial overgrowth and bacterial translocation in cirrhotic rats with ascites. J Hepatol 1997; 26: 1372–1378.
  • 19
    Pardo A, Bartoli R, Lorenzo-Zuniga V, Planas R, Vinado B, Riba J, et al. Effect of cisapride on intestinal bacterial overgrowth and bacterial translocation in cirrhosis. HEPATOLOGY 2000; 31: 858–863.
    Direct Link:
  • 20
    Chang CS, Chen GH, Lien HC, Yeh HZ. Small intestine dysmotility and bacterial overgrowth in cirrhotic patients with spontaneous bacterial peritonitis. HEPATOLOGY 1998; 28: 1187–1190.
    Direct Link:
  • 21
    Bauer TM, Steinbruckner B, Brinkmann FE, Ditzen AK, Schwacha H, Aponte JJ, et al. Small intestinal bacterial overgrowth in patients with cirrhosis: prevalence and relation with spontaneous bacterial peritonitis. Am J Gastroenterol 2001; 96: 2962–2967.
    Direct Link:
  • 22
    Chesta J, Defilippi C, Defilippi C. Abnormalities in proximal small bowel motility in patients with cirrhosis. HEPATOLOGY 1993; 17: 828–832.
  • 23
    Sadik R, Abrahamsson H, Björnsson E, Gunnarsdottir A, Stotzer PO. Etiology of portal hypertension may influence gastrointestinal transit time. Scand J Gastroenterol 2003; 38: 1039–1044.
  • 24
    Stewart JJ, Battarbee HD, Farrar GE, Betzing KW. Intestinal myoelectrical activity and transit time in chronic portal hypertension. Am J Physiol 1992; 263: G474–479.
  • 25
    Aranow JS, Fink MP. Determinants of intestinal barrier failure in critical illness. Br J Anaesth 1996; 77: 71–81.
  • 26
    Spaeth G, Gottwald T, Specian RD, Mainous MR, Berg RD, Deitch EA. Secretory immunoglobulin A, intestinal mucin, and mucosal permeability in nutritionally induced bacterial translocation in rats. Ann Surg 1994; 220: 798–808.
  • 27
    Levi AC, Borghi F, Petrino R, Bargoni A, Fronticelli CM, Gentelini S. Modifications of the trophism of intestinal mucosa after intestinal and bilio-pancreatic diversion in the rat. Ital J Gastroenterol 1991; 23: 202–207.
  • 28
    Wells CL, Jechorek RP, Erlandsen SL. Inhibitory effect of bile on bacterial invasion of enterocytes: possible mechanism for increased translocation associated with obstructive jaundice. Crit Care Med 1995; 23: 301–307.
  • 29
    Bertok L. Physico-chemical defense of vertebrate organisms: the role of bile acids in defense against bacterial endotoxins. Perspect Biol Med 1977; 21: 70–76.
  • 30
    Van Bossuyt H, Desmaretz C, Gaeta GB, Wisse E. The role of bile acids in the development of endotoxemia during obstructive jaundice in the rat. J Hepatol 1990; 10: 274–279.
  • 31
    Clements WD, Parks R, Erwin P, Halliday MI, Barr J, Rowlands BJ. Role of the gut in the pathophysiology of extrahepatic biliary obstruction. Gut 1996; 39: 587–593.
  • 32
    Parks RW, Clements WD, Smye MG, Pope C, Rowlands BJ, Diamond T. Intestinal barrier dysfunction in clinical and experimental obstructive jaundice and its reversal by internal biliary drainage. Br J Surg 1996; 83: 1345–1349.
    Direct Link:
  • 33
    Reynolds JV, Murchan P, Leonard N, Clarke P, Keane FB, Tanner WA. Gut barrier failure in experimental obstructive jaundice. J Surg Res 1996; 62: 11–16.
  • 34
    Slocum MM, Sittig KM, Specian RD, Deitch EA. Absence of intestinal bile promotes bacterial translocation. Am Surg 1992; 58: 305–310.
  • 35
    Reynolds JV, Murchan P, Leonard N, Clarke P, Keane FB, Tanner WA. Gut barrier failure in experimental obstructive jaundice. J Surg Res 1996; 62: 11–16.
  • 36
    O'Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC. Microbiology of bacterial translocation in humans. Gut 1998; 42: 29–35.
  • 37
    Sedman PC, MacFie J, Sagar P, Mitchell CJ, May J, Mancey-Jones B, et al. The prevalence of gut translocation in humans. Gastroenterology 1994; 107: 643–649.
  • 38
    Kuzu MA, Kale IT, Col C, Tekeli A, Tanik A, Koksoy C. Obstructive jaundice promotes bacterial translocation in humans. Hepatogastroenterology 1999; 46: 2159–2164.
  • 39
    Astaldi G, Strosselli E. Peroral biopsy of the intestinal mucosa in hepatic cirrhosis. Am J Dig Dis 1960; 5: 603–612.
  • 40
    Norman DA, Atkins JM, Seelig LL, Jr., Gomez-Sanchez C, Krejs GJ. Water and electrolyte movement and mucosal morphology in the jejunum of patients with portal hypertension. Gastroenterology 1980; 79: 707–715.
  • 41
    Misra V, Misra S, Dwivedi M, Gupta S. Histomorphometric study of portal hypertensive enteropathy. Am J Clin Pathol 1997; 108: 652–657.
  • 42
    Such J, Guardiola JV, de Juan J, Casellas JA, Pascual S, Aparicio JR, et al. Ultrastructural characteristics of distal duodenum mucosa in patients with cirrhosis. Eur J Gastroenterol Hepatol 2002; 14: 371–376.
  • 43
    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.
  • 44
    Ersoz G, Aydin A, Erdem S, Yuksel D, Akarca U, Kumanlioglu K. Intestinal permeability in liver cirrhosis. Eur J Gastroenterol Hepatol 1999; 11: 409–412.
  • 45
    Pascual S, Such J, Esteban A, Zapater P, Casellas JA, Aparicio JR, et al. Intestinal permeability is increased in patients with advanced cirrhosis. Hepatogastroenterology 2003; 50: 1482–1486.
  • 46
    Zuckerman MJ, Menzies IS, Ho H, Gregory GG, Casner NA, Crane RS, et al. Assessment of intestinal permeability and absorption in cirrhotic patients with ascites using combined sugar probes. Dig Dis Sci 2004; 49: 621–626.
  • 47
    Ramachandran A, Prabhu R, Thomas S, Reddy JB, Pulimood A, Balasubramanian KA. Intestinal mucosal alterations in experimental cirrhosis in the rat: role of oxygen free radicals. HEPATOLOGY 2002; 35: 622–629.
    Direct Link:
  • 48
    Guarner C, Soriano G, Tomas A, Bulbena O, Novella MT, Balanzo J, et al. Increased serum nitrite and nitrate levels in patients with cirrhosis: relationship to endotoxemia. HEPATOLOGY 1993; 18: 1139–1143.
    Direct Link:
  • 49
    Tilg H, Wilmer A, Vogel W, Herold M, Nolchen B, Judmaier G, et al. Serum levels of cytokines in chronic liver diseases [see comments]. Gastroenterology 1992; 103: 264–274.
  • 50
    Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002; 415: 389–395.
  • 51
    Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 2000; 1: 113–118.
  • 52
    Ogle CK, Noel JG, Guo X, Wells DA, Valente JF, Ogle JD, et al. The ability of endotoxin-stimulated enterocytes to produce bactericidal factors. Crit Care Med 2002; 30: 428–434.
  • 53
    Mason DY, Taylor CR. The distribution of muramidase (lysozyme) in human tissue. J Clin Pathol 1975; 28: 124–132.
  • 54
    Harwig SS, Tan L, Qu XD, Cho Y, Eisenhauer PB, Lehrer RI. Bactericidal properties of murine intestinal phopholipase A2. J Clin Invest 1995; 95: 603–610.
  • 55
    O'Neil DA, Porter E, Elewaut D, Anderson GM, Eckmann L, Ganz T, et al. Expression and regulation of the human beta-defensins hBD-1 and hBD-2 in intestinal epithelium. J Immunol 1999; 163: 6718–6724
  • 56
    Garcia-Tsao G, Lee FY, Barden GE, Cartun R, West AB. Bacterial translocation to mesenteric lymph nodes is increased in cirrhotic rats with ascites. Gastroenterology 1995; 108: 1835–1841.
  • 57
    Powell DW. Barrier function of epithelia. Am J Physiol 1981; 241: G275–G288.
  • 58
    Koh IH, Guatelli R, Montero EF, Keller R, Silva MH, Goldenberg S, et al. Where is the site of bacterial translocation—small or large bowel? Transplant Proc 1996; 28: 2661.
  • 59
    MacFie J, O'Boyle C, Mitchell CJ, Buckley PM, Johnstone D, Sudworth P. Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. Gut 1999; 45: 223–228.
  • 60
    Marshall JC, Christou NV, Horn R, Meakins JL. The microbiology of multiple organ failure: The proximal gastrointestinal tract as an occult reservoir of pathogens. Arch Surg 1988; 123: 309–315.
  • 61
    Guy-Grand D, Griscelli C, Vassalli P. The mouse gut T lymphocyte, a novel type of T cell: nature, origin, and traffic in mice in normal and graft-versus-host conditions. J Exp Med 1978; 148: 1661–1677.
  • 62
    Imaoka A, Matsumoto S, Setoyama H, Okada Y, Umesaki Y. Proliferative recruitment of intestinal intraepithelial lymphocytes after microbial colonization of germ-free mice. Eur J Immunol 1996; 26: 945–948.
    Direct Link:
  • 63
    Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nature Immunol 2001; 2: 675–680.
  • 64
    Uronen-Hansson H, Allen J, Osman M, Squires G, Klein N, Callard RE. Toll-like receptor 2 (TLR2) and TLR4 are present inside human dendritic cells, associated with microtubules and the Golgi apparatus but are not detectable on the cell surface: integrity of microtubules is required for interleukin-12 production in response to internalized bacteria. Immunology 2004; 111: 173–178.
    Direct Link:
  • 65
    Manigold T, Böcker U, Hanck C, Gundt J, Traber P, Antoni C, et al. Differential expression of toll-like receptors 2 and 4 in patients with liver cirrhosis. Eur J Gastroenterol Hepatol 2003; 15: 275–282.
  • 66
    Riordan SM, Skinner N, Nagree A, McCallum H, McIver CJ, Kurtovic J, et al. Peripheral blood mononuclear cell expression of toll-like receptors and relation to cytokine levels in cirrhosis. HEPATOLOGY 2003; 37: 1154–1164.
    Direct Link:
  • 67
    Marsik C, Mayr F, Cardona F, Derhaschnig U, Wagner OF, Jilma B. Endotoxaemia modulates Toll-like receptors on leucocytes in humans. Br J Haematol 2003; 121: 653–656.
    Direct Link:
  • 68
    Mirlashari MR, Lyberg T. Expression and involvement of Toll-like receptors (TLR)2, TLR4, and CD14 in monocyte TNF-alpha production induced by lipopolysaccharides from Neisseria meningitidis. Med Sci Monit 2003; 9: BR316–BR324.
  • 69
    Albillos A, de la Hera A, Reyes E, Monserrat J, Munoz L, Nieto M, et al. Tumor necrosis factor-alpha expression by activated monocytes and altered T-cell homeostasis in ascitic alcoholic cirrhosis: amelioration with norfloxacin. J Hepatol 2004; 40: 624–631.
  • 70
    Khoruts A, Stahnke L, McClain CJ, Logan G, Allen JI. Circulating tumor necrosis factor, interleukin-1 and interleukin-6 concentrations in chronic alcoholic patients. HEPATOLOGY 1991; 13: 267–276.
    Direct Link:
  • 71
    Deviere J, Content J, Denys C, Vandenbussche P, Schandene L, Wybran J, et al. Excessive in vitro bacterial lipopolysaccharide-induced production on monokines in cirrhosis. HEPATOLOGY 1990; 11: 628–634.
    Direct Link:
  • 72
    Genesca J, Marti R, Rojo F, Campos F, Peribanez V, Gonzalez A, et al. Increased tumour necrosis factor alpha production in mesenteric lymph nodes of cirrhotic patients with ascites. Gut 2003; 52: 1054–1059.
  • 73
    Hassner A, Kletter Y, Jedvab M, Aronson M, Shibolet S. Impaired monocyte function in liver cirrhosis. Lancet 1979; 1: 329–330.
  • 74
    Rajkovic IA, Williams R. Abnormalities of neutrophil phagocytosis, intracellular killing and metabolic activity in alcoholic cirrhosis and hepatitis. HEPATOLOGY 1986; 6: 252–262.
    Direct Link:
  • 75
    Trevisani F, Castelli E, Foschi FG, Parazza M, Loggi E, Bertelli M, et al. Impaired tuftsin activity in cirrhosis: relationship with splenic function and clinical outcome. Gut 2002; 50: 707–712.
  • 76
    Bailey RJ, Cullens H, Woolf IL, Williams R. Metabolic inhibition of polymorphnuclear leucocytes in fulminant liver failure. Lancet 1976; i: 1162–1163.
  • 77
    Finlayson ND, Krohn K, Fauconnet MH, Anderson KE. Significance of serum complement levels in chronic liver disease. Gastroenterology 1972; 63: 653–659.
  • 78
    Ekdahl KN, Lööf L, Nyberg A, Nilsson UR, Nilsson B. Defective Fc receptor-mediated clearance in patients with primary biliary cirrhosis. Gastroenterology 1991; 101: 1076–1082.
  • 79
    Runyon BA, Morrissey RL, Hoefs JC, Wyle FA. Opsioinic activity of human ascitic fluid: a potentially important mechanism against spontaneous bacterial peritonitis. HEPATOLOGY 1985; 5: 634–637.
    Direct Link:
  • 80
    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.
  • 81
    Homann C, Varming K, Hogasen K, Mollnes TE, Graudal N, Thomsen AC, et al. Acquired C3 deficiency in patients with alcoholic cirrhosis predisposes to infection and increased mortality. Gut 1997; 40: 544–549.
  • 82
    Gomez F, Ruiz P, Schreiber AD. Impaired function of macrophage Fc gamma receptors and bacterial infection in alcoholic cirrhosis. N Engl J Med 1994; 331: 1122–1128.
  • 83
    Kaliniski P, Hilkens CM, Wierenga EA, Kapsenberg ML. T cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today 1999; 20: 561–567.
  • 84
    Gautreaux MD, Deitch EA, Berg RD. T lymphocytes in host defense against bacterial translocation from the gastrointestinal tract. Infect Immun 1994; 62: 2874–2884.
  • 85
    MacPherson A, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000; 288: 2222–2226.
  • 86
    Saitoh O, Sugi K, Kojima K, Matsumoto H, Nakagawa K, Kayazawa M, et al. Increased prevalence of intestinal inflammation in patients with liver cirrhosis. World J Gastroenterol 1999; 5: 391–396.
  • 87
    Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004; 303: 1662–1665.
  • 88
    Berg RD, Wommack E, Deitch EA. Immunosuppression and intestinal bacterial overgrowth synergistically promote bacterial translocation. Arch Surg 1988; 123: 1359–1364.
  • 89
    Choudhry MA, Fazal N, Goto M, Gamelli RL, Sayeed MM. Gut-associated lymphoid T cell suppression enhances bacterial translocation in alcohol and burn injury. Am J Physiol Gastrointest Liver Physiol 2002; 282: G937–G947.
  • 90
    Shimizu T, Tani T, Hanasawa K, Endo Y, Kodama M. The role of bacterial translocation on neutrophil activation during hemorrhagic shock in rats. Shock 2001; 16: 59–63.
  • 91
    Kalff JC, Schwarz NT, Walgenbach KJ, Schraut WH, Bauer AJ. Leukocytes of the intestinal muscularis: their phenotype and isolation. J Leukoc Biol 1998; 63: 683–691.
  • 92
    Clayburgh DR, Shen L, Turner JR. A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 2004; 84: 282–291.
  • 93
    Nagral AS, Joshi AS, Bhatia SJ, Abraham P, Mistry FP, Vora IM. Congestive jejunopathy in portal hypertension. Gut 1993; 34: 694–697.
  • 94
    Mainous MR, Tso P, Berg RD, Deitch EA. Studies of the route, magnitude, and time course of bacterial translocation in a model of systemic inflammation. Arch Surg 1991; 126: 33–37.
  • 95
    Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001; 411: 599–603.
  • 96
    Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001; 411: 603–606.
  • 97
    Holler E, Rogler G, Herfarth H, Brenmoehl J, Wild PJ, Hahn J, et al. Both donor and recipient NOD2/CARD15 mutations associate with transplant-related mortality and GvHD following allogeneic stem cell transplantation. Blood 2004; 104: 889–894.
  • 98
    Inohara N, Ogura Y, Fontalba A. Host recognition of bacterial muramyl dipeptide mediated through NOD2: implications for Crohn′s disease. J Biol Chem 2003; 278: 5509–5512.
  • 99
    Chamaillard M, Girardin SE, Viala J, Philpott DJ. Nods, Nalps and Naip: intracellular regulators of bacterial-induced inflammation. Cell Microbiol 2003; 5: 581–592.
    Direct Link:
  • 100
    Wiest R, Groszmann RJ. The paradox of nitric oxide in cirrhosis and portal hypertension: too much, not enough. HEPATOLOGY 2001; 35: 478–491.
    Direct Link:
  • 101
    Obermeier F, Gross V, Scholmerich J, Falk W. Interleukin-1 production by mouse macrophages is regulated in a feedback fashion by nitric oxide. J Leukoc Biol 1999; 66: 829–836.
  • 102
    Wallace JL, Miller MJ. Nitric oxide in mucosal defense: a little goes a long way. Gastroenterology 2000; 119: 512–520.
  • 103
    Shiloh MU, MacMicking JD, Nicholson S. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 1999; 10: 29–38.
  • 104
    Morales-Ruiz M, Jimenez W, Ros J, Sole M, Leivas A, Bosch-Marce M, et al. Nitric oxide production by peritoneal macrophages of cirrhotic rats: a host response against bacterial peritonitis. Gastroenterology 1997; 112: 2056–2064.
  • 105
    Jimenez W, Ros J, Morales-Ruiz M, Navasa M, Sole M, Colmenero J, et al. Nitric oxide production and inducible nitric oxide synthase expression in peritoneal macrophages of cirrhotic patients. HEPATOLOGY 1999; 30: 670–676.
    Direct Link:
  • 106
    Garcia-Tsao G, Angulo P, Garcia JC, Groszmann R, Cadelina G. The diagnostic and predictive value of ascites nitric oxide levels in patients with spontaneous bacterial peritonitis. HEPATOLOGY 1998; 28: 17–21.
    Direct Link:
  • 107
    Alican I, Kubes P. A critical role for nitric oxide in intestinal barrier function and dysfunction. Am J Physiol 1996; 270: G225–G237.
  • 108
    Fernandez-Ruiz V, Gonzalez A, Lopez-Moratalla N. Effect of nitric oxide in the differentiation of human monocytes to dendritic cells. Immunol Lett 2004; 93: 87–95.
  • 109
    Kubes P. Nitric oxide modulates epithelial permeability in the feline small intestine. Am J Physiol 1992; 262: G1138–G1142.
  • 110
    Payne D, Kubes P. Nitric oxide donors reduce the rise in reperfusion-induced intestinal mucosal permeability. Am J Physiol 1993; 265: G189–G195.
  • 111
    Hutcheson IR, Whittle BJ, Boughton-Smith NK. Role of nitric oxide in maintaining vascular integrity in endotoxin-induced acute intestinal damage in the rat. Br J Pharmacol 1990; 101: 815–820.
  • 112
    Lopez-Belmonte J, Whittle BJ, Moncada S. The actions of nitric oxide donors in the prevention or induction of injury to the rat gastric mucosa. Br J Pharmacol 1993; 108: 73–78.
  • 113
    Tepperman BL, Brown JF, Whittle BJ. Nitric oxide synthase induction and intestinal epithelial cell viability in rats. Am J Physiol 1993; 265: G214–G218.
  • 114
    Forsythe RM, Xu DZ, Lu Q, Deitch EA. Lipopolysaccharide-induced enterocyte-derived nitric oxide induces intestinal monolayer permeability in an autocrine fashion. Shock 2002; 17: 180–184.
  • 115
    Salzman AL, Menconi MJ, Unno N, Ezzell RM, Casey DM, Gonzalez PK, et al. Nitric oxide dilates tight junctions and depletes ATP in cultured Caco-2BBe intestinal epithelial monolayers. Am J Physiol 1995; 268: G361–G373.
  • 116
    Unno N, Wang H, Menconi MJ, Tytgat SH, Larkin V, Smith M, et al. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology 1997; 113: 1246–1257.
  • 117
    Chen LW, Hsu CM, Wang JS, Chen JS, Chen SC. Specific inhibition of iNOS decreases the intestinal mucosal peroxynitrite level and improves the barrier function after thermal injury. Burns 1998; 24: 699–705.
  • 118
    Mishima S, Xu D, Lu Q, Deitch EA. Bacterial translocation is inhibited in inducible nitric oxide synthase knockout mice after endotoxin challenge but not in a model of bacterial overgrowth. Arch Surg 1997; 132: 1190–1195.
  • 119
    Cirera I, Bauer TM, Navasa M, Vila J, Grande L, Taura P, et al. Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol 2001; 34: 32–37.
  • 120
    Such J, Frances R, Munoz C, Zapater P, Casellas JA, Cifuentes A, et al. Detection and identification of bacterial DNA in patients with cirrhosis and culture-negative, nonneutrocytic ascites. HEPATOLOGY 2002; 36: 135–141.
    Direct Link:
  • 121
    Frances R, Benlloch S, Zapater P, Gonzalez JM, Lozano B, Munoz C, et al. A sequential study of serum bacterial DNA in patients with advanced cirrhosis and ascites. HEPATOLOGY 2004; 39: 484–491.
    Direct Link:
  • 122
    Frances R, Munoz C, Zapater P, Uceda F, Gascon I, Pascual S, et al. Bacterial DNA activates cell mediated immune response and nitric oxide overproduction in peritoneal macrophages from patients with cirrhosis and ascites. Gut 2004; 53: 860–864.
  • 123
    Nikkari S, McLaughlin IJ, Dodge DE, Relman DA. Does blood of healthy subjects contain bacterial ribosomal DNA. J Clin Microbiol 2001; 39: 1956–1959.
  • 124
    Vernon SD, Shukla SK, Conradt J, Unger ER, Reeves WC. Analysis of 16S rRNA gene sequences and circulating cell-free DNA from plasma of chronic fatigue syndrome and non-fatigued subjects. BMC Microbiol 2002; 2: 39.
  • 125
    Heininger A, Binder M, Ellinger A, Pfisterer J, Botzenhart K, Unertl K, et al. Effect of comprehensive validation of the template isolation procedure on the reliability of bacteraemia detection by a 16S rRNA gene PCR. Clin Microbiol Infect 2004; 10: 452–458.
    Direct Link:
  • 126
    Gines P, Rimola A, Planas R, Vargas V, Marco F, Almela M, et al. Norfloxacin prevents spontaneous bacterial peritonitis recurrence in cirrhosis: results of a double-blind, placebo-controlled trial. HEPATOLOGY 1990; 12: 716–724.
    Direct Link:
  • 127
    Llovet JM, Bartoli R, Planas R, Vinado B, Perez J, Cabre E, et al. Selective intestinal decontamination with norfloxacin reduces bacterial translocation in ascitic cirrhotic rats exposed to hemorrhagic shock. HEPATOLOGY 1996; 23: 781–787.
    Direct Link:
  • 128
    Guarner C, Runyon BA, Heck M, Young S, Sheikh MY. Effect of long-term trimethoprim-sulfamethoxazole prophylaxis on ascites formation, bacterial translocation, spontaneous bacterial peritonitis, and survival in cirrhotic rats. Dig Dis Sci 1999; 44: 1957–1962.
  • 129
    Rabiller A, Nunes H, Lebrec D, Tazi KA, Wartski M, Dulmet E, et al. Prevention of gram-negative translocation reduces the severity of hepatopulmonary syndrome. Am J Respir Crit Care Med 2002; 166: 514–517.
  • 130
    Bauer TM, Fernandez J, Navasa M, Vila J, Rodes J. Failure of Lactobacillus spp. to prevent bacterial translocation in a rat model of experimental cirrhosis. J Hepatol 2002; 36: 501–506.
  • 131
    Runyon BA, Borzio M, Young S, Squier SU, Guarner C, Runyon MA. Effect of selective bowel decontamination with norfloxacin on spontaneous bacterial peritonitis, translocation, and survival in an animal model of cirrhosis. HEPATOLOGY 1995; 21: 1719–1724.
  • 132
    Rimola A, Bory F, Teres J, Perez-Ayuso RM, Arroyo V, Rodes J. Oral, nonabsorbable antibiotics prevent infection in cirrhotics with gastrointestinal hemorrhage. HEPATOLOGY 1985; 5: 463–467.
    Direct Link:
  • 133
    Soriano G, Guarner C, Tomas A, Villanueva C, Torras X, Gonzalez D, et al. Norfloxacin prevents bacterial infection in cirrhotics with gastrointestinal hemorrhage. Gastroenterology 1992; 103: 1267–1272.
  • 134
    Grange JD, Roulot D, Pelletier G, Pariente EA, Denis J, Ink O, et al. Norfloxacin primary prophylaxis of bacterial infections in cirrhotic patients with ascites: a double-blind randomized trial. J Hepatol 1998; 29: 430–436.
  • 135
    Novella M, Sola R, Soriano G, Andreu M, Gana J, Ortiz J, et al. Continuous versus inpatient prophylaxis of the first episode of spontaneous bacterial peritonitis with norfloxacin. HEPATOLOGY 1997; 25: 532–536.
    Direct Link:
  • 136
    Albillos A, DelaHera A, Gonzalez M, Moya J, Calleja J, Monserrat J, et al. Increased lipopolysaccharide binding protein in cirrhotic patients with marked immune and hemodynamic derangement. HEPATOLOGY 2003; 37: 208–217.
    Direct Link:
  • 137
    Chin-Dusting JP, Rasaratnam B, Jennings G, Dudley FJ. Effect of fluorochinolone on the enhanced nitric oxide-induced peripheral vasodilation seen in cirrhosis. Ann Intern Med 1997; 127: 985–988.
  • 138
    Rasaratnam B, Kaye D, Jennings G, Dudley F, Chin-Dusting J. The effect of selective intestinal decontamination on the hyperdynamic circulatory state in cirrhosis: a randomized trial. Ann Intern Med 2003; 139: 186–193.
  • 139
    Fernandez J, Navasa M, Gomez J, Colmenero J, Vila J, Arroyo V, et al. Bacterial infections in cirrhosis: epidemiological changes with invasive procedures and norfloxacin prophylaxis. HEPATOLOGY 2002; 35: 140–148.
    Direct Link:
  • 140
    Perez-Paramo M, Munoz J, Albillos A, Freile I, Portero F, Santos M, et al. Effect of propranolol on the factors promoting bacterial translocation in cirrhotic rats with ascites. HEPATOLOGY 2000; 31: 43–48.
    Direct Link:
  • 141
    Zhang SC, Wang W, Ren WY, He BM, Zhou K, Zhu WN. Effect of cisapride on intestinal bacterial and endotoxin translocation in cirrhosis. World J Gastroenterol 2003; 9: 534–538.
  • 142
    Madrid AM, Hurtado C, Venegas M, Cumsille F, Defilippi C. Long-term treatment with cisapride and antibiotics in liver cirrhosis: effect on small intestinal motility, bacterial overgrowth, and liver function. Am J Gastroenterol 2001; 96: 1251–1255.
    Direct Link:
  • 143
    Adawi D, Ahrne S, Molin G. Effects of different probiotic strains of Lactobacillus and Bifidobacterium on bacterial translocation and liver injury in an acute liver injury model. Int J Food Microbiol 2001; 70: 213–220.
  • 144
    Wiest R, Chen F, Cadelina G, Groszmann RJ, Garcia-Tsao G. Effect of Lactobacillus-fermented diets on bacterial translocation and intestinal flora in experimental prehepatic portal hypertension. Dig Dis Sci 2003; 48: 1136–1141.
  • 145
    Rayes N, Seehofer D, Muller AR, Hansen S, Bengmark S, Neuhaus P. Influence of probiotics and fibre on the incidence of bacterial infections following major abdominal surgery - results of a prospective trial. Z Gastroenterol 2002; 40: 869–876.
  • 146
    Chiva M, Soriano G, Rochat I, Peralta C, Rochat F, Llovet T, et al. Effect of Lactobacillus johnsonii La1 and antioxidants on intestinal flora and bacterial translocation in rats with experimental cirrhosis. J Hepatol 2002; 37: 456.
  • 147
    Lorenzo-Zuniga V, Bartoli R, Planas R, Hofmann AF, Vinado B, Hagey LR, et al. Oral bile acids reduce bacterial overgrowth, bacterial translocation, and endotoxemia in cirrhotic rats. HEPATOLOGY 2003; 37: 551–557.
    Direct Link:
  • 148
    Krahenbuhl JP, Corbett M. Keeping the gut microflora at bay. Science 2004; 303: 1624–1625.
  • 149
    Brooks SG, May J, Sedman P, Tring I, Johnstone D, Mitchell CJ, et al. Translocation of enteric bacteria in humans. Br J Surg 1993; 80: 901–902.
    Direct Link:
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