Pathophysiology of increased intestinal permeability in obstructive jaundice

World Journal of Gastroenterology

Volumn 13, Issue 48, 2007, Pages 6458-6464

  Assimakopoulos, Stelios F ^a   Scopa, Chrisoula D ^a   Vagianos, Constantine E ^b  

^a UNIVERSITY OF PATRAS   (Greece)

^b GENERAL HOSPITAL OF NIKEA   (Greece)

Author keywords

Apoptosis; Bacterial translocation; Claudin 4; Endotoxemia; Intestinal barrier; Intestinal permeability; Obstructive jaundice; Occludin; Oxidative stress; Tight junctions

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GLUTATHIONE DISULFIDE; IMMUNOGLOBULIN A; INTERLEUKIN 1; INTERLEUKIN 6; NITRIC OXIDE; OXYGEN RADICAL; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; BILE; CELL PROLIFERATION; ENDOTOXEMIA; HUMAN; IMMUNE SYSTEM; INTESTINE CELL; INTESTINE MUCOSA PERMEABILITY; MORBIDITY; MORTALITY; NONHUMAN; OBSTRUCTIVE JAUNDICE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERMEABILITY BARRIER; POSTOPERATIVE CARE; PREOPERATIVE EVALUATION; REVIEW; TIGHT JUNCTION;

EID: 38349070557     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.13.6458     Document Type: Review

References (66)

1. Greig JD, Krukowski ZH, Matheson NA. Surgical morbidity and mortality in one hundred and twenty-nine patients with obstructive jaundice. Br J Surg 1988; 75: 216-219
2. Pain JA, Cahill CJ, Bailey ME. Perioperative complications in obstructive jaundice: therapeutic considerations. Br J Surg 1985; 72: 942-945
3. Sewnath ME, Karsten TM, Prins MH, Rauws EJ, Obertop H, Gouma DJ. A meta-analysis on the efficacy of preoperative biliary drainage for tumors causing obstructive jaundice. Ann Surg 2002; 236: 17-27
4. van der Gaag NA, de Castro SM, Rauws EA, Bruno MJ, van Eijck CH, Kuipers EJ, Gerritsen JJ, Rutten JP, Greve JW, Hesselink EJ, Klinkenbijl JH, Rinkes IH, Boerma D, Bonsing BA, van Laarhoven CJ, Kubben FJ, van der Harst E, Sosef MN, Bosscha K, de Hingh IH, Th de Wit L, van Delden OM, Busch OR, van Gulik TM, Bossuyt PM, Gouma DJ. Preoperative biliary drainage for periampullary tumors causing obstructive jaundice; DRainage vs. (direct) OPeration (DROP-trial). BMC Surg 2007; 7: 3
5. Parks RW, Halliday MI, McCrory DC, Erwin P, Smye M, Diamond T, Rowlands BJ. Host immune responses and intestinal permeability in patients with jaundice. Br J Surg 2003; 90: 239-245
6. Scott-Conner CE, Grogan JB. The pathophysiology of biliary obstruction and its effect on phagocytic and immune function. J Surg Res 1994; 57: 316-336
7. 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
8. Clements WD, Erwin P, McCaigue MD, Halliday I, Barclay GR, Rowlands BJ. Conclusive evidence of endotoxaemia in biliary obstruction. Gut 1998; 42: 293-299
9. Deitch EA, Sittig K, Li M, Berg R, Specian RD. Obstructive jaundice promotes bacterial translocation from the gut. Am J Surg 1990; 159: 79-84
10. Scopa CD, Koureleas S, Tsamandas AC, Spiliopoulou I, Alexandrides T, Filos KS, Vagianos CE. Beneficial effects of growth hormone and insulin-like growth factor I on intestinal bacterial translocation, endotoxemia, and apoptosis in experimentally jaundiced rats. J Am Coll Surg 2000; 190: 423-431
11. Sano T, Ajiki T, Takeyama Y, Kuroda Y. Internal biliary drainage improves decreased number of gut mucosal T lymphocytes and MAdCAM-1 expression in jaundiced rats. Surgery 2004; 136: 693-699
12. Ogawa A, Tagawa T, Nishimura H, Yajima T, Abe T, Arai T, Taniguchi M, Takeda K, Akira S, Nimura Y, Yoshikai Y. Toll-like receptors 2 and 4 are differentially involved in Fas dependent apoptosis in Peyer's patch and the liver at an early stage after bile duct ligation in mice. Gut 2006; 55: 105-113
13. Arai T, Yoshikai Y, Kamiya J, Nagino M, Uesaka K, Yuasa N, Oda K, Sano T, Nimura Y. Bilirubin impairs bactericidal activity of neutrophils through an antioxidant mechanism in vitro. J Surg Res 2001; 96: 107-113
14. Brown WR, Kloppel TM. The liver and IgA: immunological, cell biological and clinical implications. Hepatology 1989; 9: 763-784
15. Kloppel TM, Hoops TC, Gaskin D, Le M. Uncoupling of the secretory pathways for IgA and secretory component by cholestasis. Am J Physiol 1987; 253: G232-G240
16. 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
17. Binder HJ, Filburn B, Floch M. Bile acid inhibition of intestinal anaerobic organisms. Am J Clin Nutr 1975; 28: 119-125
18. Floch MH, Gershengoren W, Elliott S, Spiro HM. Bile acid inhibition of the intestinal microflora - a function for simple bile adds? Gastroenterology 1971; 61: 228-233
19. Ding JW, Andersson R, Soltesz V, Willen R, Bengmark S. The role of bile and bile acids in bacterial translocation in obstructive jaundice in rats. Eur Surg Res 1993; 25: 11-19
20. Ding JW, Anderssson F. Soltesz VL, Parsson H, Johansson K, Wang W, Bengmark S. Inhibition of bacberial translocation in obstructive jaundice by muramyl tripeptide phosphatidylethanolamine in the rat. J Hepatol 1994; 20: 720-728
21. Assimakopoulos SF, Vagianos CE, Patsoukis N, Georgiou C, Nikolopoulou V, Scopa CD. Evidence for intestinal oxidative stress in obstructive jaundice-induced gut barrier dysfunction in rats. Acta Physiol Scand 2004; 180: 177-185
22. Bron PA, Marco M, Hoffer SM, Van Mullekom E, de Vos WM, Kleerebezem M. Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. J Bacteriol 2004; 186: 7829-7835
23. 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
24. Parks RW, Stuart Cameron CH, Gannon CD, Pope C, Diamond T, Rowlands BJ. Changes in gastrointestinal morphology associated with obstructive jaundice. J Pathol 2000; 192: 526-532
25. Toledo A, Yamaguchi J, Wang JY, Bass BL, Turner DJ, Strauch ED. Taurodeoxycholate stimulates intestinal cell proliferation and protects against apoptotic cell death through activation of NF-kappaB. Dig Dis Sci 2004; 49: 1664-1671
26. Yamaguchi J, Toledo A, Bass BL, Celeste FA, Rao JN, Wang JY, Strauch ED. Taurodeoxycholate increases intestinal epithelial cell proliferation through c-myc expression. Surgery 2004; 135: 215-221
27. Yang R, Harada T, Li J, Uchiyama T, Han Y, Englert JA, Fink MP. Bile modulates intestinal epithelial barrier function via an extracellular signal related kinase 1/2 dependent mechanism. Intensive Care Med 2005; 31: 709-717
28. Assimakopoulos SF, Scopa CD, Charonis A, Spiliopoulou I, Georgiou C, Nikolopoulou V, Vagianos CE. Experimental obstructive jaundice disrupts intestinal mucosal barrier by altering occludin expression: beneficial effect of bombesin and neurotensin. J Am Coll Surg 2004; 198: 748-757
29. 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
30. Kimmings AN, van Deventer SJ, Obertop H, Rauws EA, Huibregtse K, Gouma DJ. Endotoxin, cytokines, and endotoxin binding proteins in obstructive jaundice and after preoperative biliary drainage. Gut 2000; 46: 725-731
31. Welsh FK, Ramsden CW, MacLennan K, Sheridan MB, Barclay GR, Guillou PJ, Reynolds JV. Increased intestinal permeability and altered mucosal immunity in cholestatic jaundice. Ann Surg 1998; 227: 205-212
32. Bailey ME. Endotoxin, bile salts and renal function in obstructive jaundice. Br J Surg 1976; 63: 774-778
33. Kuzu MA, Kale IT, Col C, Tekeli A, Tanik A, Koksoy C. Obstructive jaundice promotes bacterial translocation in humans. Hepatogastroenterology 1999; 46: 2159-2164
34. Farhadi A, Banan A, Fields J, Keshavarzian A. Intestinal barrier: an interface between health and disease. J Gastroenterol Hepatol 2003; 18: 479-497
35. Arrieta MC, Bistritz L, Meddings JB. Alterations in intestinal permeability. Gut 2006; 55: 1512-1520
36. 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
37. Sileri P, Morini S, Sica GS, Schena S, Rastellini C, Gaspari AL, Benedetti E, Cicalese L. Bacterial translocation and intestinal morphological findings in jaundiced rats. Dig Dis Sci 2002; 47: 929-934
38. Hollander D. Intestinal permeability, leaky gut, and intestinal disorders. Curr Gastroenterol Rep 1999; 1: 410-416
39. Portincasa P, Grattagliano I, Testini M, Caruso ML, Wang DQ, Moschetta A, Calamita G, Vacca M, Valentini AM, Renna G, Lissidini G, Palasciano G. Parallel intestinal and liver injury during early cholestasis in the rat: modulation by bile salts and antioxidants. Free Radic Biol Med 2007; 42: 1381-1391
40. Heiskala M, Peterson PA, Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2001; 2: 93-98
41. Tamagawa H, Takahashi I, Furuse M, Yoshitake-Kitano Y, Tsukita S, Ito T, Matsuda H, Kiyono H. Characteristics of claudin expression in follicle-associated epithelium of Peyer's patches: preferential localization of claudin-4 at the apex of the dome region. Lab Invest 2003; 83: 1045-1053
42. Assimakopoulos SF, Vagianos CE, Charonis AS, Alexandris IH, Spiliopoulou I, Thomopoulos KC, Nikolopoulou VN, Scopa CD. Experimental obstructive jaundice alters claudin-4 expression in intestinal mucosa: effect of bombesin and neurotensin. World J Gastroenterol 2006; 12: 3410-3415
43. Bemelmans MH, Gouma DJ, Greve JW, Buurman WA. Cytokines tumor necrosis factor and interleukin-6 in experimental biliary obstruction in mice. Hepatology 1992; 15: 1132-1136
44. Madara JL. Warner-Lambert/Parke-Davis Award lecture. Pathobiology of the intestinal epithelial barrier. Am J Pathol 1990; 137: 1273-1281
45. Schmitz H, Fromm M, Bentzel CJ, Scholz P, Detjen K, Mankertz J, Bode H, Epple HJ, Riecken EO, Schulzke JD. Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J Cell Sci 1999; 112: 137-146
46. Rao RK, Basuroy S, Rao VU, Karnaky Jr KJ, Gupta A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J 2002; 368: 471-481
47. Blikslager AT, Roberts MC. Nitric oxide and the intestinal epithelial barrier: does it protect or damage the gut? J Pediatr Gastroenterol Nutr 1997; 25: 439-440
48. Mankertz J, Tavalali S, Schmitz H, Mankertz A, Riecken EO, Fromm M, Schulzke JD. Expression from the human occludin promoter is affected by tumor necrosis factor alpha and interferon gamma. J Cell Sci 2000; 113: 2085-2090
49. Sewnath ME, Van Der Poll T, Van Noorden CJ, Ten Kate FJ, Gouma DJ. Endogenous interferon gamma protects against cholestatic liver injury in mice. Hepatology 2002; 36: 1466-1477
50. Nakajima Y, Baudry N, Duranteau J, Vicaut E. Microcirculation in intestinal villi: a comparison between hemorrhagic and endotoxin shock. Am J Respir Crit Care Med 2001; 164: 1526-1530
51. Tsukamoto T, Nigam SK. Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. Am J Physiol 1999; 276: F737-F750
52. Simonovic I, Rosenberg J, Koutsouris A, Hecht G. Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol 2000; 2: 305-315
53. Ogata Y, Nishi M, Nakayama H, Kuwahara T, Ohnishi Y, Tashiro S. Role of bile in intestinal barrier function and its inhibitory effect on bacterial translocation in obstructive jaundice in rats. J Surg Res 2003; 115: 18-23
54. Assimakopoulos SF, Scopa CD, Zervoudakis G, Mylonas PG, Georgiou C, Nikolopoulou V, Vagianos CE. Bombesin and neurotensin reduce endotoxemia, intestinal oxidative stress, and apoptosis in experimental obstructive jaundice. Ann Surg 2005; 241: 159-167
55. Margaritis VG, Filos KS, Michalaki MA, Scopa CD, Spiliopoulou I, Nikolopoulou VN, Vagianos CE. Effect of oral glutamine administration on bacterial tanslocation, endotoxemia, liver and ileal morphology, and apoptosis in rats with obstructive jaundice. World J Surg 2005; 29: 1329-1334
56. Sheen-Chen SM, Ho HT, Chen WJ, Eng HL. Obstructive jaundice alters proliferating cell nuclear antigen expression in rat small intestine. World J Surg 2003; 27: 1161-1164
57. Assimakopoulos SF, Nikolopoulou VN, Scopa CD, Vagianos CE. Beneficial effects of glutamine on intestinal barrier function in obstructive jaundice. World J Surg 2005; 29: 935-936
58. Assimakopoulos SF, Thomopoulos KC, Patsoukis N, Georgiou CD, Scopa CD, Nikolopoulou VN, Vagianos CE. Evidence for intestinal oxidative stress in patients with obstructive jaundice. Eur J Clin Invest 2006; 36: 181-187
59. Assimakopoulos SF, Maroulis I, Patsoukis N, Vagenas K, Scopa CD, Georgiou CD, Vagianos CE. Effect of antioxidant treatments on the gut-liver axis oxidative status and function in bile duct-ligated rats. World J Surg 2007; 31: 2023-2032
60. Assimakopoulos SF, Vagianos CE, Zervoudakis G, Filos KS, Georgiou C, Nikolopoulou V, Scopa CD. Gut regulatory peptides bombesin and neurotensin reduce hepatic oxidative stress and histological alterations in bile duct ligated rats. Regul Pept 2004; 120: 185-193
61. Sakaguchi S, Furusawa S, Yokota K, Sasaki K, Takayanagi M, Takayanagi Y. The enhancing effect of tumour necrosis factor-alpha on oxidative stress in endotoxemia. Pharmacol Toxicol 1996; 79: 259-265
62. Pata C, Caglikulekci M, Cinel L, Dirlik M, Colak T, Aydin S. The effects of antithrombin-III on inducible nitric oxide synthesis in experimental obstructive jaundice. An immunohistochemical study. Pharmacol Res 2002; 46: 325-331
63. Unno N, Wang H, Menconi MJ, Tytgat SH, Larkin V, Smith M, Morin MJ, Chavez A, Hodin RA, Fink MP. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology 1997; 113: 1246-1257
64. Tsuji K, Kubota Y, Yamamoto S, Yanagitani K, Amoh Y, Takaoka M, Ogura M, Kin H, Inoue K. Increased neutrophil chemotaxis in obstructive jaundice: an in vitro experiment in rats. J Gastroenterol Hepatol 1999; 14: 457-463
65. Tsai LY, Lee KT, Lu FJ. Biochemical events associated with ligation of the common bile duct in Wistar rats. J Formos Med Assoc 1997; 96: 17-22
66. Kamata H, Hirata H. Redox regulation of cellular signalling. Cell Signal 1999; 11: 1-14