Bacterial Translocation: Intestinal Epithelial Permeability

  • C. L. Wells
  • S. L. Erlandsen
Part of the Update in Intensive Care and Emergency Medicine book series (UICM, volume 26)

Abstract

In its broadest terms, intestinal bacterial translocation can be defined as the passage of bacteria (both live and dead) and bacterial products (such as exotoxins, endotoxins, and cell wall fragments) from the intestinal lumen to otherwise sterile extraintestinal sites. Investigators studying immune mechanisms at mucosal surfaces have long recognized that epithelial uptake and processing of intestinal antigens is a complex process, needed not only to establish the immune status of the host, but to continually regulate the immune response (both inductive and suppressive) to intestinal antigens [1]. The transmigration of intestinal bacteria was initially viewed with skepticism by many physicians; however, in recent years, the existence of bacterial translocation (BT) has become generally accepted among clinicians, although the clinical significance of this process remains a subject of debate.

Keywords

Ischemia Bacillus Dexamethasone Glucocorticoid Pseudomonas 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bland PW, Kambarage DM (1991) Antigen handling by the epithelium and lamina propria macrophages. In: MacDermott RP, Elson CO (eds) Gastroenterology Clinics of North America, WB Saunders, Philadelphia, pp 577–596Google Scholar
  2. 2.
    Carter L (1994) Bacterial translocation: Nursing implications in the care of patients with neutropenia. Oncology Nursing Forum 21: 857–865PubMedGoogle Scholar
  3. 3.
    Emori TG, Gaynes RP (1993) An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev 6: 428–444PubMedGoogle Scholar
  4. 4.
    Centers for Disease Control (1992) Public health focus: Surveillance, prevention, and control of nosocomial infections. Morbidity and Mortality Weekly Reports 41: 783–787Google Scholar
  5. 5.
    Tancrede CH, Andremont AO (1985) Bacterial translocation and gram-negative bacteremia in patients with hematological malignancies. J Infect Dis 152: 99–103PubMedCrossRefGoogle Scholar
  6. 6.
    Wells CL, Podzorski RP, Peterson PK, Ramsay NK, Simmons RL, Rhame FS (1984) Incidence of trimethoprim-sulfamethoxazole resistant enterobacteriaceae among transplant recipients. J Infect Dis 150:699–706PubMedCrossRefGoogle Scholar
  7. 7.
    Wells CL, Juni BA, Cameron SB, Mason KR, Ferrieri P, Rhame FR (1995) Stool carriage, clinical isolation, and mortality during an outbreak of vancomycin-resistant enterococcal infections in hospitalized medical/surgical patients. Clin Infect Dis 21: 45–50PubMedCrossRefGoogle Scholar
  8. 8.
    Ford EG, Baisden CE, Matteson ML, Picone AL (1991) Sepsis after coronary bypass grafting: Evidence for loss of the gut mucosal barrier. Ann Thorac Surg 52: 514–517PubMedCrossRefGoogle Scholar
  9. 9.
    Schlag G, Redl H, Hallstrom S (1991) The cell in shock: The origin of multiple organ failure. Resuscitation 21: 137–180PubMedCrossRefGoogle Scholar
  10. 10.
    Tran DD, van Onselen EBH, Wensink AJF, Cuesta MA (1994) Factors related to multiple organ system failure and mortality in a surgical intensive care unit. Nephrol Dialysis Transplant 9(Suppl 4): 172–178Google Scholar
  11. 11.
    Moore FA, Moore EE, Paggetti R, et al (1991) Gut bacterial translocation via the portal vein: A clinical perspective with major torso trauma. J Trauma 31: 629–638PubMedCrossRefGoogle Scholar
  12. 12.
    Rush BF, Sori AJ, Murphy TF, Smith S, Flanagan JJ, Machiedo GW (1988) Endotoxemia and bacteremia during hemorrhagic shock. The link between trauma and sepsis? Ann Surg 207: 549–554PubMedCrossRefGoogle Scholar
  13. 13.
    Van der Waaij DJM, Berghuis-de Vries JM, Lekkerkerk-van der Wees JEC (1971) Colonization resistance of the digestive tract and the spread of bacteria to the lymphatic organs in mice. J Hyg 70: 335–342CrossRefGoogle Scholar
  14. 14.
    Loirat Ph, Johanson WG, Van Saene HKF (1992) First European consensus conference in intensive care medicine: Selective decontamination of the digestive tract in intensive care and emergency medicine. Intensive Care Med 18: 182–188CrossRefGoogle Scholar
  15. 15.
    Wells CL (1993) A decade of selective decontamination of the digestive tract as prophylaxis for infections in ICU patients: What have we learned? (editorial) Clin Infect Dis 17: 1055–1057PubMedCrossRefGoogle Scholar
  16. 16.
    Boom SJ, Ramsay G (1992) Selective decontamination of the digestive tract in intensive care. Epidemiol Infect 109: 337–347PubMedCrossRefGoogle Scholar
  17. 17.
    Ambrose NS, Johnson M, Burdon DW, Keighley MRB (1984) Incidence of pathogenic bacteria from mesenteric lymph nodes and ileal serosa during Crohn’s disease surgery. Br J Surg 71: 623–625PubMedCrossRefGoogle Scholar
  18. 18.
    Laffineur G, Lescut D, Vincent P, Quandalle P, Wurtz A, Colombel JF (1992) Bacterial translocation in Crohn’s disease. Gastroenterol Clin Biol 16: 777–781PubMedGoogle Scholar
  19. 19.
    Vincent P, Colombel JF, Lescut D, et al (1988) Bacterial translocation in patients with colorectal cancer. J Infect Dis 158: 1395–1396PubMedCrossRefGoogle Scholar
  20. 20.
    Deitch EA (1989) Simple intestinal obstruction causes bacterial translocation in man. Arch Surg 124: 699–701PubMedCrossRefGoogle Scholar
  21. 21.
    Peitzman AB, Odekwu AO, Ochoa J, Smith A (1991) Bacterial translocation in trauma patients. J Trauma 31: 1083–1087PubMedGoogle Scholar
  22. 22.
    Koha M, Brismar B, Wikstrom B, Ewrth S, Nord CE (1992) Bacterial colonization and translocation in colorectal carcinoma. Med Microbiol Lett 1: 168–176Google Scholar
  23. 23.
    Sedman PC, Macfie J, Sagar P, et al (1994) The prevalence of gut translocation in humans. Gastroenterol 107: 643–649CrossRefGoogle Scholar
  24. 24.
    Brathwaite CEM, Ross SE, Nagele R, Mure AJ, O’Malley KF, Garcia-Perez FA (1993) Bacterial translocation occurs in humans after traumatic injury: Evidence using immunofluorescence. J Trauma 34: 586–590PubMedCrossRefGoogle Scholar
  25. 25.
    Reed LL, Martin M, Manglano R, Newson B, Kocka F, Barrett J (1994) Bacterial translocation following abdominal trauma in humans. Circ Shock 42: 1–6PubMedGoogle Scholar
  26. 26.
    van Goor H, Rosman C, Ground J, Kooi K, Wubbels GH, Bleichrodt RP (1994) Translocation of bacteria and endotoxin in organ donors. Arch Surg 129: 1063–1066PubMedCrossRefGoogle Scholar
  27. 27.
    Wells CL, Jechorek RP, Erlandsen SL (1990) Evidence for the translocation of Enterococcus faecalis across the mouse intestinal tract. J Infect Dis 162: 82–90PubMedCrossRefGoogle Scholar
  28. 28.
    Mainous MR, Tso P, Berg RD, Deitch EA (1991) Studies of the route, magnitude, and time course of bacterial translocation in a model of systemic inflammation. Arch Surg 126: 33–37PubMedCrossRefGoogle Scholar
  29. 29.
    Madara JL (1990) Pathobiology of the intestinal epithelial barrier. Am J Pathol 137: 1273–1281PubMedGoogle Scholar
  30. 30.
    Alexander JW, Boyce ST, Babcock GF, et al (1990) The process of microbial translocation. Surgery 212: 496–512Google Scholar
  31. 31.
    Cole GT, Seshan KR, Pope LM, Vancey RJ (1988) Morphological analysis of gastrointestinal tract invasion by Candida albicans in the infant mouse. J Med Vet My col 26: 173–185CrossRefGoogle Scholar
  32. 32.
    Wells CL, Erlandsen SL (1991) Localization of translocating Escherichia coli, Proteus mirabilis, and Enterococcus faecalis within cecal and colonic tissue of monoassociated mice. Infect Immun 59: 4693–4697PubMedGoogle Scholar
  33. 33.
    Wells CL, Jechorek RP, Erlandsen SL (1990) Evidence for the translocation of Enterococcus faecalis across the mouse intestinal tract. J Infect Dis 162: 82–90PubMedCrossRefGoogle Scholar
  34. 34.
    Falkow S, Isberg RR, Portnoy DA (1992) The interaction of bacteria with mammalian cells. Annu Rev Cell Biol 8: 333–363PubMedCrossRefGoogle Scholar
  35. 35.
    Brandtzaeg P (1989) Overview of the mucosal immune system. Curr Topics Microbiol Immunol 146: 13–25Google Scholar
  36. 36.
    Neutra M, Louvard D (1989) Differentiation of intestinal epithelial cells in vitro. In: Satir BH (ed) Functional epithelial cells in culture. Alan R Liss, New York, pp 363–398Google Scholar
  37. 37.
    Wells CL, Jechorek RP, Olmsted SB, Erlandsen SL (1993) Effect of LPS on epithelial integrity and bacterial uptake in the polarized human enterocyte-like cell line Caco-2. Circ Shock 40: 276–288PubMedGoogle Scholar
  38. 38.
    Wells CL, Jechorek RP, Olmsted SB, Erlandsen SL (1994) Bacterial translocation in cultured enterocytes: Magnitude, specificity, and electron microscopic observations of endocytosis. Shock 1: 443–451PubMedCrossRefGoogle Scholar
  39. 39.
    Olmsted SB, Dunny GM, Erlandsen SL, Wells CL (1994) A plasmid-encoded surface protein on Enterocoecus faecalis augments its internalisation by cultured intestinal epithelial cells. J Infect Dis 170:1549–1556PubMedCrossRefGoogle Scholar
  40. 40.
    Griffin FM Jr, Griffin JA, Silverstein SC (1975) Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane. J Exp Med 142: 1263–1282PubMedCrossRefGoogle Scholar
  41. 41.
    Wells CL, van de Westerlo EMA, Jechorek RP, Erlandsen SL (1995) Exposure of the lateral enterocyte membrane by dissociation of calcium-dependent junctional complex augments endocytosis of enteric bacteria. Shock 4: 204–210PubMedCrossRefGoogle Scholar
  42. 42.
    Wells CL, van de Westerlo EMA, Jechorek RP, Felds BA, Wilkins TD, Erlandsen SL (1996) Bactervides fragilis enterotoxin modulates epithelial permeability and bacterial internalization by HT-29 enterocytes. Gastroenterol (In press)Google Scholar
  43. 43.
    Armitage WJ, Juss BK, Easty DL (1994) Response of epithelial (MDCK) cell junctions to calcium removal and osmotic stress is influenced by temperature. Cryobiology 31: 453–460PubMedCrossRefGoogle Scholar
  44. 44.
    Howarth AG, Singer KL, Stevenson BR (1994) Analysis of the distribution and phosphorylation state of ZO-1 in MDCK and non-epithelial cells. J Membrane Biol 137:261–270CrossRefGoogle Scholar
  45. 45.
    Citi S (1992) Protein kinase inhibitors prevent junction dissociation induced by low extracellular calcium in MDCK epithelial cells. J Cell Biol 117: 169–178PubMedCrossRefGoogle Scholar
  46. 46.
    Bhat M, Toledo-Velasquez D, Wang L, Malanga CJ, Ma JK, Rojanasakul Y (1993) Regulation of tight junction permeability by calcium mediators and cell cytoskeleton in rabbit tracheal epithelium. Pharmaceutical Res 10: 991–997CrossRefGoogle Scholar
  47. 47.
    Somosy Z, Kovacs J, Siklos L, Koteies GJ (1993) Morphological and histochemical changes in intercellular junctional complexes in epithelial cells of mouse small intestine upon X-irra-diation: Changes of ruthenium red permeability and calcium content. Scanning Microscopy 7: 961–971PubMedGoogle Scholar
  48. 48.
    Moncrief JS, Obiso R Jr, Barroso LA, et al (1995) The enterotoxin of Bacteroides fragilis is a metalloprotease. Infect Immun 63: 175–181PubMedGoogle Scholar
  49. 49.
    Mounier J, Vasselon T, Hellio R, Lesourd M, Sansonetti PJ (1992) Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect Immun 60: 237–248PubMedGoogle Scholar
  50. 50.
    Edmiston CE, Condon RE (1991) Bacterial translocation. Surg Gyn Obstetrics 173: 73–83Google Scholar
  51. 51.
    Van Leeuwen PA, Boermeester MA, Houdijk AP, et al (1994) Clinical significance of translocation. Gut 35: S28–S34PubMedCrossRefGoogle Scholar
  52. 52.
    Ryan CM, Bailey SH, Carter EA, Schoenfeld DA, Tompkins RG (1994) Additive effects of thermal injury and infection on gut permeability. Arch Surg 129: 325–328PubMedCrossRefGoogle Scholar
  53. 53.
    Berthiaume F, Ezzell RM, Toner M, Yarmush ML, Tompkins RG (1994) Transport of fluorescent dextrans across the rat ileum after cutaneous thermal injury. Crit Care Med 22: 455–464PubMedCrossRefGoogle Scholar
  54. 54.
    Horton JW (1994) Bacterial translocation after burn injury: The contribution of ischemia and permeability changes. Shock 1: 286–290PubMedCrossRefGoogle Scholar
  55. 55.
    Messick WJ, Koruda M, Meyer A, Zimmerman K (1994) Differential changes in intestinal permeability following burn injury. J Trauma 36: 306–311PubMedCrossRefGoogle Scholar
  56. 56.
    Rhodes RS, Karnovsky MJ (1971) Loss of macromolecular barrier function associated with surgical trauma to the intestine. Lab Invest 25: 220–229PubMedGoogle Scholar
  57. 57.
    Ziegler TR, Smith RJ, O’Dwyer ST, Demling RH, Wilmore DW (1988) Increased intestinal permeability associated with infection in burn patients. Arch Surg 123: 1313–1319PubMedCrossRefGoogle Scholar
  58. 58.
    Deitch EA (1990) Intestinal permeability is increased in burn patients shortly after injury. Surg 107: 411–416Google Scholar
  59. 59.
    Ryan CM, Yarmush ML, Burke JF, Tompkins (1992) Increased gut permeability early after burns correlates with the extent of burn injury. Crit Care Med 20: 1508–1512PubMedCrossRefGoogle Scholar
  60. 60.
    Pape HC, Dweger A, Regel G, et al (1994) Increased gut permeability after multiple trauma. Br J Surg 81: 850–852PubMedCrossRefGoogle Scholar
  61. 61.
    Langkamp-Henken B, Donovan TB, Pate LM, Maull CD, Kudsk KA (1995) Increased intestinal permeability following blunt and penetrating trauma. Crit Care Med 23: 660–664PubMedCrossRefGoogle Scholar
  62. 62.
    Wang XD, Parsson H, Andersson R, Soltesz V, Johansson K, Bengmark S (1994) Bacterial translocation, intestinal ultrastructure and cell membrane permeability early after major liver resection in the rat. Br J Surg 81: 579–584PubMedCrossRefGoogle Scholar
  63. 63.
    Morris TH, Sorensen SH, Turkington J, Batt RM (1994) Diarrhoea and increased intestinal permeability in laboratory beagles associated with proximal small intestinal bacterial overgrowth. Lab Animals 28: 313–319CrossRefGoogle Scholar
  64. 64.
    Heribert DJ, Zhong R, Wang P (1989) Intestinal permeability with hemorrhagic shock, surgical trauma, and endotoxemia. Surg Forum 40: 93–95Google Scholar
  65. 65.
    Roumen RM, van der Vliet JA, Wevers RA, Goris JA (1993) Intestinal permeability is increased after major vascular surgery. J Vascular Surg 17: 734–737CrossRefGoogle Scholar
  66. 66.
    Deitch EA, Morrison J, Berg RD, Specian RD (1990) Effect of hemorrhagic shock on bacterial translocation, intestinal morphology, and intestinal permeability in conventional and antibiotic-decontaminated rats. Crit Care Med 18: 529–536PubMedCrossRefGoogle Scholar
  67. 67.
    Roumen RM, Hendriks T, Wevers RA, Goris JA (1993) Intestinal permeability after severe trauma and hemorrhagic shock is increased without relation to septic complications. Arch Surg 128: 453–457PubMedCrossRefGoogle Scholar
  68. 68.
    Horton JW, Walker PB (1993) Oxygen radicals, lipid peroxidation, and permeability changes after intestinal ischemia and reperfusion. J Appl Physiol 74: 1515–1520PubMedGoogle Scholar
  69. 69.
    Vaughn WG, Horton JW, Walker PB (1992) Allopurinol prevents intestinal permeability changes after ischemia-reperfusion injury. J Pedr Surg 27: 968–972CrossRefGoogle Scholar
  70. 70.
    Mion F, Cuber JC, Minaire Y, Chayvialle JA (1994) Short-term effects of indomethacin on rat small intestinal permeability. Role of eicosanoids and platelet activating factor. Gut 35: 490–495PubMedCrossRefGoogle Scholar
  71. 71.
    Yamada T, Deitch E, Specian RD, Perry MA, Sartor RB, Grisham MB (1993) Mechanisms of acute and chronic intestinal inflammation induced by indomethacin. Inflammation 17: 641–662PubMedCrossRefGoogle Scholar
  72. 72.
    Davies GR, Wilkie ME, Prampton DS (1993) Effects of metronidazole and misoprostol on indomethacin-induced changes in intestinal permeability. Dig Dis Sci 38:417–425PubMedCrossRefGoogle Scholar
  73. 73.
    Salzman AL, Wang H, Wollert PS, et al (1994) Endotoxin-induced ileal mucosal hyperpermeability in pigs: Role of tissue acidosis. Am J Physiol 266: G633–G646PubMedGoogle Scholar
  74. 74.
    Xu D, Qi L, Guillory D, Cruz N, Berg R, Deitch EA (1993) Mechanisms of endotoxin-induced intestinal injury in a hyperdynamic model of sepsis. J Trauma 34: 676–682PubMedCrossRefGoogle Scholar
  75. 75.
    Walker RI, Porvaznik MJ (1978) Disruption of the permeability barrier (zonula occludens) between intestinal epithelial cells by lethal doses of endotoxin. Infect Immun 21: 655–658PubMedGoogle Scholar
  76. 76.
    Fink MP, Antonsson JB, Wang H, Rothschild HR (1991) Increased intestinal permeability in endotoxic pigs. Arch Surg 126: 211–218PubMedCrossRefGoogle Scholar
  77. 77.
    Fink MP, Kaups KL, Wang HL, Rothschild HR (1991) Maintenance of superior mesenteric arterial perfusion prevents increased intestinal permeability in endotoxic pigs. Surg 110: 154–160Google Scholar
  78. 78.
    Deitch EA, Specian RD, Berg RD (1991) Endotoxin-induced bacterial translocation and mucosal permeability: Role of xanthine oxidase, complement activation, and macrophage products. Crit Care Med 19: 785–789PubMedCrossRefGoogle Scholar
  79. 79.
    O’Dwyer ST, Michie HR, Ziegler TR, Revhaug A, Smith RJ, Wilmore DW (1988) A single dose of endotoxin increases intestinal permeability in healthy humans. Arch Surg 123: 1459–1464PubMedCrossRefGoogle Scholar
  80. 80.
    Harris CE, Griffiths RD, Freestone N, Billington D, Atherton ST, Macmillan RR (1992) Intestinal permeability in the critically ill. Intensive Care Med 18: 38–41PubMedCrossRefGoogle Scholar
  81. 81.
    Ryan CM, Schmidt J, Lewandrowski K, et al (1993) Gut macromolecular permeability in pancreatitis correlates with severity of disease in rats. Gastroenterol 105: 956–957Google Scholar
  82. 82.
    Batt RM, Hall EJ, McLean L, Simpson KW (1992) Small intestinal bacterial overgrowth and enhanced intestinal permeability in healthy beagles. Am J Vet Res 53: 1935–1940PubMedGoogle Scholar
  83. 83.
    Spaeth G, Gottwald T, Specian RD, Mainous MR, Berg RD, Deitch EA (1994) Secretory immunoglobulin A, intestinal mucin, and mucosal permeability in nutritionally-induced bacterial translocation in rats. Ann Surg 220: 798–808PubMedCrossRefGoogle Scholar
  84. 84.
    Li J, Langkamp-Henken B, Suzuki K, Stahlgren LH (1994) Glutamine prevents parenteral nutrition-induced increases in intestinal permeability. J Parent Enteral Nutr 18: 289–290CrossRefGoogle Scholar
  85. 85.
    Illig KA, Ryan CK, Hardy DJ, Rhodes J, Locke W, Sax HC (1992) Total parenteral nutritioninduced changes in gut mucosal function: Atropy alone is not the issue. Surg 112: 631–637Google Scholar
  86. 86.
    Grant D, Hurlbut D, Zhong R, et al ( 1991 ) Intestinal permeability and bacterial translocation following small bowel transplantation in the rat. Transplantation 52: 221–224PubMedCrossRefGoogle Scholar
  87. 87.
    Pantzar N, Ekstrom GM, Wang Q, Westrom BR (1994) Mechanisms of increased intestinal CrEDTA absorption during experimental colitis in the rat. Dig Dis Sci 39: 2327–2333PubMedCrossRefGoogle Scholar
  88. 88.
    Leslie KA, Behme R, Clift A, Martin S, Grant D, Duff JH (1994) Synergistic effects of tumor necrosis factor and morphine on gut barrier function. Can J Surg 37: 143–147PubMedGoogle Scholar
  89. 89.
    Spitz J, Hecht G, Taveras M, Aoys E, Alverdy J (1994) The effect of dexamethasone administration on rat intestinal permeability: The role of bacterial adherence. Gastroenterology 106: 35–41PubMedGoogle Scholar
  90. 90.
    Alverdy J, Aoys E (1991) The effect of glucocorticoid administration on bacterial translocation. Evidence for an acquired mucosal immunodeficient state. Ann Surg 214: 719–723PubMedCrossRefGoogle Scholar
  91. 91.
    Wells CL, Barton RG, Erlandsen SL, Cerra FB, Jechorek RP, Dunn D (1990) Parenteral endotoxin and intestinal function. In: Nowotny A, Spitzer JJ, Ziegler EJ (eds) Cellular and molecular aspects of endotoxin reactions. Endotoxin research series, vol 1, Elsevier, New York, pp 509–519Google Scholar
  92. 92.
    Jones WG, Minei JP, Richardson RP, et al (1990) Pathophysiologic glucocorticoid elevations promote bacterial translocation after thermal injury. Infect Immun 58: 3257–3261PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • C. L. Wells
  • S. L. Erlandsen

There are no affiliations available

Personalised recommendations