Intestinal hypoperfusion contributes to gut barrier failure in severe acute pancreatitis

Journal of Gastrointestinal Surgery

Volumn 7, Issue 1, 2003, Pages 26-36

  Rahman, Sakhawat H ^a   Ammori, Basil J ^a   Holmfield, John ^a   Larvin, Michael ^b   McMahon, Michael J ^a   Sarr, M G ^c   Duncan, M D ^c   Mattews, J B ^c   Hodin, Richard A ^c  

^a LEEDS GENERAL INFIRMARY   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c NONE

Author keywords

Acute pancreatitis; IFABP; Ischemia reperfusion; Permeability

Indexed keywords

C REACTIVE PROTEIN; ENDOTOXIN; ENDOTOXIN ANTIBODY; FATTY ACID BINDING PROTEIN; IMMUNOGLOBULIN M ANTIBODY; MACROGOL; BIOLOGICAL MARKER; CARRIER PROTEIN; CORE ENDOTOXIN; DIAGNOSTIC AGENT; FABP7 PROTEIN, HUMAN; FATTY ACID; IMMUNOGLOBULIN M; MACROGOL DERIVATIVE; TUMOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ACUTE PANCREATITIS; AGED; ARTICLE; CHILD; CONTROLLED STUDY; DISEASE SEVERITY; ENDOTOXEMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; INTESTINE MUCOSA PERMEABILITY; INTESTINE PERFUSION; KIDNEY TUBULE EXCRETION; MAJOR CLINICAL STUDY; MALE; MOLECULAR PROBE; PROTEIN SECRETION; PROTEIN URINE LEVEL; SCORING SYSTEM; STATISTICAL SIGNIFICANCE; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; ACUTE DISEASE; ADULT; BLOOD; IMMUNOLOGY; INTESTINE; ISCHEMIA; METABOLISM; MIDDLE AGED; MULTIPLE ORGAN FAILURE; PANCREATITIS; PATHOPHYSIOLOGY; PERMEABILITY; URINE; VASCULARIZATION;

ACUTE DISEASE; ADULT; AGED; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CARRIER PROTEINS; ENDOTOXINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; FEMALE; HUMANS; IMMUNOGLOBULIN M; INTESTINES; ISCHEMIA; MALE; MIDDLE AGED; MULTIPLE ORGAN FAILURE; NEOPLASM PROTEINS; PANCREATITIS; PERMEABILITY; POLYETHYLENE GLYCOLS; TUMOR SUPPRESSOR PROTEINS;

EID: 0037263857     PISSN: 1091255X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1091-255X(02)00090-2     Document Type: Article

References (100)

1. Bradley E.L. III, Allen K. A prospective longitudinal study of observation versus surgical intervention in the management of necrotizing pancreatitis. Am J Surg. 161:1991;19-24.
2. Forsmark C.E., Toskes P.P. Acute pancreatitis. Medical management. Crit Care Clin. 11:1995;295-309.
3. Larvin M., McMahon M.J. Apache-II score for assessment and monitoring of acute pancreatitis. Lancet. 22:1989;201-205.
4. Mann D.V., Hershman M.J., Hittinger R., Glazer G. Multicentre audit of death in acute pancreatitis. Br J Surg. 81:1994;890-893.
5. Renner I.G., Savage W.T. III, Pantoja J.L., Renner V.J. Death due to acute pancreatitis. A prospective analysis of 405 autopsy cases Dig Dis Sci. 30:1985;1005-1018.
6. Buggy B.P., Nostrant T.T. Lethal pancreatitis. Am J Gastroenterol. 78:1983;810-814.
7. Beger H.G., Bittner R., Block S., Büchler M. Bacterial contamination of pancreatic necrosis - A prospective clinical study. Gastroenterology. 91:1986;433-438.
8. Gerzof S.A., Banks P.A., Robbins A.H.et al. Early diagnosis of pancreatic infection by computed tomography-guided aspiration. Gastroenterology. 93:1987;1315-1320.
9. Bassi C., Falconi M., Girelli R.et al. Microbiological findings in severe pancreatitis. Surg Res Commun. 5:1989;1-4.
10. Bradley E.L. III A clinically based classification system for acute pancreatitis. Arch Surg. 128:1993;586-590.
11. Büchler M., Malfertheiner P., Friess H.et al. Human pancreatic tissue concentration of bactericidal antibiotics. Gastroenterology. 103:1992;1902-1908.
12. Fedorak I.J., Ko T.C., Djuricin G.et al. Secondary pancreatic infections. Are they distinct clinical entities? Surgery. 112:1992;824-831. -.
13. Malangoni M.A., Shallcross J.C., Seiler J.G.et al. Factors contributing to fatal outcome after treatment of pancreatic abscess. Ann Surg. 203:1986;605-613.
14. Bassi C., Vesentini S., Nifosi F.et al. Pancreatic abscess and other pus-harboring collections related to pancreatitis. A review of 108 cases World J Surg. 14:1990;505-512.
15. Lumsden A., Bradley E.L. III Secondary pancreatic infection. Surg Gynecol Obstet. 170:1990;459-467.
16. Swank G.M., Deitch E.A. Role of the gut in multiple organ failure. Bacterial translocation and permeability changes World J Surg. 20:1996;411-417.
17. Weinstein L., Swartz M.N. Pathogenic properties of invading micro-organisms. Sodeman W.A. Jr., Sodeman W.A. Pathologic Physiology. Mechanisms of Disease:1974;466-468 Saunders, Philadelphia.
18. Connor J., Fine J., Kusano K.et al. Potentiation by endotoxin of responses associated with increases in calcium conductance. Proc Natl Acad Sci USA. 70:1973;3301-3304.
19. Foulis A.K., Murray W.R., Galloway D.et al. Endotoxemia and complement activation in acute pancreatitis in man. Gut. 23:1982;656-661.
20. Exley A.R., Leese T., Holliday M.P.et al. Endotoxaemia and serum tumour necrosis factor as prognostic markers in severe acute pancreatitis. Gut. 33:1992;1126-1128.
21. Liehr H., Grun M., Seeling R., Seeling H.-P. Endotoxinamie bei akuter Pankreatitis. Leber Magen Darm. 10:1980;259-264.
22. Wang X.D., Wang Q., Andersson R., Ihse I. Alterations in intestinal function in acute pancreatitis in an experimental model. Br J Surg. 83:1996;1537-1543.
23. Ryan C.M., Schmidt J., Lewandrowski K.et al. Gut macromolecular permeability in pancreatitis correlates with severity of disease in rats. Gastroenterology. 104:1993;890-895.
24. Ammori B.J., Leeder P.C., King R.F.et al. Early increase in intestinal permeability in patients with severe acute pancreatitis. Correlation with endotoxemia, organ failure, and mortality J Gastrointest Surg. 3:1999;252-262.
25. Runkel N.S., Moody F.G., Smith G.S.et al. The role of the gut in the development of sepsis in acute pancreatitis. J Surg Res. 51:1991;18-23.
26. Gianotti L., Munda R., Alexander J.W. Pancreatitis-induced microbial translocation. A study of the mechanisms Res Surg. 4:1992;87-91.
27. Deitch E.A. Multiple organ failure. Pathophysiology and potential future therapy. Ann Surg. 216:1992;117-134.
28. Marshall J.C., Christou N.V., Meakins J.L. The gastrointestinal tract. The 'undrained abscess' of multiple organ failure. Ann Surg. 218:1993;111-119.
29. Meakins J.L., Marshall J.C. The gastrointestinal tract. The "motor" of multiple organ failure Arch Surg. 121:1986;197.
30. Border J.R., Hassett J., LaDuca J.et al. Gut origin septic states in blunt trauma (ISS = 40) in the ICU. Ann Surg. 206:1987;427-448.
31. Kivilaakso E., Valtonen V.V., Malkamaki M.et al. Endotoxaemia and acute pancreatitis. Correlation between the severity of the disease and the anti-enterobacterial common antigen antibody titre Gut. 25:1984;1065-1070.
32. Windsor J.A., Fearon K.C.H., Ross J.A.et al. The role of serum endotoxin and antiendotoxin core antibody levels in predicting the development of multiple organ failure in acute pancreatitis. Br J Surg. 80:1993;1042-1046.
33. Tarpila E., Nystrom P.-O., Franzen L., Ihse I. Bacterial translocation during acute pancreatitis in rats. Eur J Surg. 159:1993;109-113.
34. Warshaw A.L. Inflammatory masses following acute pancreatitis. Surg Clin North Am. 54:1974;620-637.
35. Webster M.W., Pasculle A.W., Myerowitz R.L.et al. Postinduction bacteremia in experimental acute pancreatitis. Am J Surg. 138:1979;418-420.
36. Byrne J.J., Joison J. Bacterial regurgitation in experimental pancreatitis. Am J Surg. 107:1964;317-320.
37. Keynes W.M. A nonpancreatic source of the proteolytic enzyme amidase and bacteriology in experimental acute pancreatitis. Ann Surg. 191:1980;187-199.
38. Carrico C.J., Meakins J.L., Marshall J.C., Fry D., Maier R.V. Multiple-organ-failure syndrome. Arch Surg. 121:1986;196-208.
39. Morris S.E., Navaratnam N., Townsend C.M., Herndon D.N. Decreased mesenteric blood flow independently promotes bacterial translocation in chronically instrumented sheep. Surg Forum. 40:1989;88-90.
40. Navaratnam N.S., Morris C., Townsend C.et al. Bacterial translocation and selective mesenteric artery perfusion with nitroprusside in an ovine model. Int J Radiat Oncol Biol Phys. 21:1989;240. [abstr].
41. Tokyay R., Zeigler S.T., Traber D.L.et al. Postburn gastrointestinal vasoconstriction increases bacterial and endotoxin translocation. J Appl Physiol. 74:1993;1521-1527.
42. Redan J.A., Rush B.F., Lysz T.W.et al. Organ distribution of gut-derived bacteria caused by bowel manipulation ischemia. Am J Surg. 159:1990;85-89.
43. Sori A.J., Rush B.F., Lysz T.W., Smith S., Machiedo G.W. The gut as a source of sepsis after hemorrhagic shock. Am J Surg. 155:1988;187-192.
44. Baker J.W., Deitch E.A., Berg R.D., Specian R.D. Hemorrhagic shock induces bacterial translocation from the gut. J Trauma. 28:1988;896-906.
45. Horton J.W., Walker P.B. Oxygen radicals, lipid peroxidation, and permeability changes after intestinal ischemia and reperfusion. J Appl Physiol. 74:1993;1515-1520.
46. Kubes P. Ischemia-reperfusion in feline small intestine. A role for nitric oxide Am J Physiol. 264:1993;G143-G149.
47. Deitch E.A., Berg R. Bacterial translocation from the gut. A mechanism of infection J Burn Care Rehabil. 8:1987;475-482.
48. Tancrede C.H., Andremont A.O. Bacterial translocation, and gram-negative bacteremia in patients with hematological malignancies. J Infect Dis. 152:1985;99-103.
49. Berg R.D. Bacterial translocation from the gastrointestinal tracts of mice receiving immunosuppressive chemotherapeutic agents. Curr Microbiol. 8:1983;285-292.
50. Owens W.E., Berg R.D. Bacterial translocation from the gastrointestinal tract of athymic (nu/nu) mice. Infect Immun. 27:1982;461-467.
51. Maddaus M.A., Wells C.L., Platt J.L.et al. Effect of T cell modulation on the translocation of the bacteria from the gut and mesenteric lymph nodes. Ann Surg. 207:1988;387-398.
52. Deitch E.A., Maejima K., Berg R. Effect of oral antibiotics and bacterial overgrowth on the translocation of the GI tract microflora in burned rats. J Trauma. 25:1985;385-392.
53. Steffen E.K., Berg R.D. Relationship between cecal population levels and indigenous bacteria and translocation to the mesenteric lymph nodes. Infect Immun. 39:1983;1252-1259.
54. Berg R.D., Owen W.E. Inhibition of translocation of viable Escherichia coli from the gastrointestinal tract of mice by bacterial antagonism. Infect Immun. 25:1979;820-827.
55. Berg R.D. Inhibition of Escherichia coli translocation from the gastrointestinal tract by normal cecal flora in gnotobiotic or antibiotic-decontaminated mice. Infect Immun. 29:1980;1073-1081.
56. Andersson R., Wang X.D., Ihse I. The influence of abdominal sepsis on acute pancreatitis in rats. A study on mortality, permeability, arterial pressure, and intestinal blood flow Pancreas. 11:1995;365-373.
57. Ockner R.K., Manning J.A. Fatty acid-binding protein in small intestine. J Clin Invest. 54:1974;326-338.
58. Robinson J.W., Mirkovitch V. The recovery of function and microcirculation in small intestinal loops following ischemia. Gut. 13:1972;784-789.
59. Gollin G., Marks C., Marks W.H. Intestinal fatty acid binding protein in serum and urine reflects early ischemic injury to the small bowel. Surgery. 113:1993;545-551.
60. Kanda T., Nakatomi Y., Ishikawa H.et al. Intestinal fatty-acid binding protein as a sensitive marker of intestinal ischaemia. Dig Dis Sci. 37:1992;1362-1367.
61. Knaus W.A., Zimmerman J.E., Wagner D.P.et al. APACHE-acute physiology and chronic health evaluation. A physiologically based classification system Crit Care Med. 9:1981;591-597.
62. Ryan C.M., Yarmush M.L., Tompkins R.G. Separation and quantification of polyethylene glycols 400 and 3350 from human urine by high-performance liquid chromatography. J Pharm Sci. 81:1992;350-352.
63. Barclay G.R., Scott B.B. Serological relationships between Escherichia coli and Salmonella smooth- and rough-mutant lipopolysaccharides as revealed by enzyme-linked immunosorbent assay for human immunoglobulin G antiendotoxin antibodies. Infect Immun. 55:1987;2706-2714.
64. Barclay G.R., Scott B.B., Wright I.H.et al. Changes in anti-endotoxin IgG antibody and endotoxaemia in three cases of gram-negative septic shock. Circ Shock. 29:1989;93-106.
65. Kanda T., Fujii H., Tani T.et al. Intestinal fatty-acid binding protein is a useful diagnostic marker for mesenteric infarction in humans. Gastroenterology. 110:1996;339-343.
66. Lieberman J.M., Marks W.H., Cohn S.et al. Organ failure, infection, and the systemic inflammatory response syndrome are associated with elevated levels of urinary intestinal fatty acid binding protein. Study of 100 consecutive patients in a surgical intensive care unit J Trauma Infect Crit Care. 45:1998;900-905.
67. Roitt I., Brostoff J., Male D. Immunology. 3rd ed:1993;Mosby-Year Book Europe Ltd, London.
68. Granger D.N., McCord D., Parks D.A., Halloworth M.B. Xanthine oxidase inhibitors attenuate ischemia-induced vascular permeability changes in the cat intestine. Gastroenterology. 90:1986;80-84.
69. Parks D.A., Williams T.K., Beckman J.S. Conversion of xanthine dehydrogenase to oxidase in ischemic rat intestine. A re-evaluation Am J Physiol. 54;G768-G774:1988.
70. Payne D., Kubes P. Nitric oxide donors reduce the rise in reperfusion-induced intestinal mucosal permeability. Am J Physiol. 265:1993;G189-G195.
71. Cipolle M.D., Pasqualle M.D., Ferra F.B. Secondary organ dysfunction. From clinical perspectives to molecular mediators Circ Shock. 9:1993;261-298.
72. Hotz H.G., Foitzik T., Schulzke J.D.et al. Reduced capillary blood flow is not related to increased ion permeability of the colon in acute pancreatitis. Langenbecks Arch Chir Suppl Kongressbd. 114:1997;413-415. [in German].
73. Klar E., Mall G., Messmer K.et al. Improvement of impaired pancreatic microcirculation by isovolemic hemodilution protects pancreatic morphology in acute biliary pancreatitis. Surg Gynecol Obstet. 176:1993;144-150.
74. Hunt D.R., Mildenhall P. Etiology of stricture of the colon associated with pancreatitis. Am J Dig Dis. 20:1975;941-946.
75. Russell J.C., Welch J.P., Clark D.G.et al. Colonic complications of acute pancreatitis and pancreatic abscess. Am J Surg. 146:1983;558-564.
76. Jensen K., Bradley E.L. III Mesenteric venous infarction in acute pancreatitis. Int J Pancreatol. 5:1989;213-219.
77. Buttenschoen K., Berger D., Hiki N.et al. Endotoxin and antiendotoxin antibodies in patients with acute pancreatitis. Eur J Surgery. 166:2000;459-466.
78. Michie H.R., Manogue K.R., Spriggs D.et al. Detection of circulating tumor necrosis factor during endotoxemia in humans. N Engl J Med. 318:1988;1481-1486.
79. O'Dwyer S.T., Michie H.R., Ziegler T.R.et al. A single dose of endotoxin increases intestinal permeability in healthy humans. Arch Surg. 123:1988;1459-1464.
80. Walker R.I., Porvaznilk M.J. Disruption of the permeability barrier (zona occludens) between intestinal epithelial cells by lethal doses of endotoxin. Infect Immun. 21:1978;655-658.
81. Morrison D.C., Ryan J.L. Bacterial endotoxins and host immune responses. Adv Immunol. 28:1979;293-350.
82. Deitch E.A., Berg R., Specian R. Endotoxin promotes the translocation of bacteria from the gut. Arch Surg. 122:1987;185-190.
83. Curley P.J., McMahon M.J., Lancaster F.et al. Reduction in circulating levels of CD4-positive lymphocytes in acute pancreatitis. Relationship to endotoxin, interleukin 6 and disease severity Br J Surg. 80:1993;1312-1315.
84. Garcia-Sabrido J.L., Valdecantos E., Bastida E., Tellado J.M. The anergic state as a predictor of pancreatic sepsis. Zentrabl Chir. 114:1989;114-120.
85. Curley P., Nestor M., Collins K.et al. Decreased interleukin-2 production in murine acute pancreatitis. Potential for immunomodulation Gastroenterology. 110:1996;583-588.
86. Widdison A.L., Karanjia N.D., Alvarez C., Reber H.A. Reticuloendothelial function, and efficacy of levamisol for the treatment of pancreatic infection in acute necrotizing pancreatitis. Am J Surg. 163:1992;100-104.
87. Summer R.W., Kent T.H. Effects of altered propulsion on rat small intestinal flora. Gastroenterology. 59:1970;740.
88. Pederzoli P., Bassi C., Vesentini S., Campedelli A. A randomized multicenter clinical trial of antibiotic prophylaxis of septic complications in acute necrotizing pancreatitis with imipenem. Surg Gynecol Obstet. 176:1993;480-483.
89. Sainio V., Kemppaainen E., Puolakkainen P.et al. Early antibiotic treatment in acute necrotising pancreatitis. Lancet. 346:1995;663-667.
90. Isaji S., Suzuki M., Frey C.F.et al. Role of bacterial infection in diet-induced acute pancreatitis in mice. Int J Pancreatol. 11:1992;49-57.
91. Lange J.F., van Gool J., Tytgat G.N. The protective effect of a reduction in intestinal flora on mortality of acute hemorrhagic pancreatitis in the rat. Hepatogastroenterology. 34:1987;28-30.
92. Luiten E.J.T., Hop W.C.J., Lange J.F., Bruining H.A. Controlled clinical trial of selective decontamination for the treatment of severe acute pancreatitis. Ann Surg. 222:1995;57-65.
93. Foitzik T., Stufler M., Hotz H.G.et al. Glutamine stabilizes intestinal permeability and reduces pancreatic infection in acute experimental pancreatitis. J Gastrointest Surg. 1:1997;40-47.
94. Gennari R., Alexander W. Effects of hyperoxia on bacterial translocation and mortality during gut-derived sepsis. Arch Surg. 131:1996;57-62.
95. Simsek I., Mas M.R., Yasar M.et al. Inhibition of inducible nitric oxide synthase reduces bacterial translocation in a rat model of acute pancreatitis. Pancreas. 23:2002;296-301.
96. Czako I., Takacs T., Varga I.S.et al. Oxidative stress in distant organs and the effects of allopurinol during experimental acute pancreatitis. Int J Pancreatol. 27:2000;209-216.
97. Defaux J.P., Thonier F., Baroggi N.et al. Involvement of platelet-activating factor (PAF) in endotoxin- or ischaemia-induced intestinal hyperpermeability in the rat. J Lipid Mediat. 7:1993;11-21.
98. de Souza L.J., Sampietre S.N., Assis R.S.et al. Effect of PAF antagonists (BN-52021, WEB-2170, and BB-882) on bacterial translocation in acute pancreatitis. J Gastrointest Surg. 5:2001;364-370.
99. Sun Z., Wang X., Deng X.et al. Beneficial effects of lexipafant, a PAF antagonist, on gut barrier dysfunction caused by intestinal ischaemia and reperfusion in rats. Dig Surg. 17:2000;57-60.
100. Johnson C.D., Kingsnorth A.N., Imrie C.W.et al. Double blind, randomised, placebo controlled study of a platelet activating factor antagonist, lexipafant, in the treatment and prevention of organ failure in predicted severe acute pancreatitis. Gut. 48:2001;62-69.