Bile acid malabsorption in inflammatory bowel disease

Inflammatory Bowel Diseases

Volumn 21, Issue 2, 2015, Pages 476-483

  Vítek, Libor ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Bile acid malabsorption; Bile acids; Crohn's disease; Inflammatory bowel disease; Ulcerative colitis

Indexed keywords

BILE ACID; FARNESOID X RECEPTOR; G PROTEIN COUPLED BILE ACID RECEPTOR 1; G PROTEIN COUPLED RECEPTOR; LIPID; PREGNANE X RECEPTOR; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

BACTERIAL OVERGROWTH; BILE ACID MALABSORPTION; BILE ACID METABOLISM; CHOLELITHIASIS; CROHN DISEASE; DIARRHEA; DIGESTION; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE MOTILITY; INTESTINE MUCOSA PERMEABILITY; LABORATORY DEVICE; MALABSORPTION; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SECRETION (PROCESS); SIGNAL TRANSDUCTION; UROLITHIASIS; COMPLICATION; INFLAMMATORY BOWEL DISEASES; METABOLISM; PATHOLOGY; PROGNOSIS; STEATORRHEA;

BILE ACIDS AND SALTS; DIARRHEA; HUMANS; INFLAMMATORY BOWEL DISEASES; PROGNOSIS; STEATORRHEA;

EID: 84927738000     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000193     Document Type: Review

References (92)

1. Bernstein CN. Epidemiology of inflammatory bowel disease: The shifting landscape. In: Targan SR, Shanahan F, Karp LC, eds. Inflammatory Bowel Disease. Translating Basic Science Into Clinical Practice. Singapore: Blackwell Publishing Ltd; 2010:9-15.
2. Sands BE. Crohn's disease: clinical course and complications. In: Targan SR, Shanahan F, Karp LC, eds. Inflammatory Bowel Diseases. Translating Basic Science Into Clinical Practice. Singapore: Blackwell Publishing Ltd; 2010:228-244.
3. Camilleri M. Advances in understanding of bile acid diarrhea. Expert Rev Gastroenterol Hepatol. 2014;8:49-61.
4. Wilcox C, Turner J, Green J. Systematic review: The management of chronic diarrhoea due to bile acid malabsorption. Aliment Pharmacol Ther. 2014;39:923-939.
5. Markossian S, Kreydiyyeh SI. TNF-alpha down-regulates the Na+-K+ ATPase and the Na+-K+-2Cl-cotransporter in the rat colon via PGE2. Cytokine. 2005;30:319-327.
6. Tang Y, Forsyth CB, Keshavarzian A. New molecular insights into inflammatory bowel disease-induced diarrhea. Expert Rev Gastroenterol Hepatol. 2011;5:615-625.
7. Zeissig S, Burgel N, Gunzel D, et al. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut. 2007;56:61-72.
8. Ivanov AI, Parkos CA, Nusrat A. Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol. 2010;177:512-524.
9. Reddy SN, Bazzocchi G, Chan S, et al. Colonic motility and transit in health and ulcerative colitis. Gastroenterology. 1991;101:1289-1297.
10. Castiglione F, Del Vecchio Blanco G, Rispo A, et al. Orocecal transit time and bacterial overgrowth in patients with Crohn's disease. J Clin Gastroenterol. 2000;31:63-66.
11. Tursi A, Brandimarte G, Giorgetti G, et al. Assessment of orocaecal transit time in different localization of Crohn's disease and its possible influence on clinical response to therapy. Eur J Gastroenterol Hepatol. 2003;15:69-74.
12. Fava F, Danese S. Intestinal microbiota in inflammatory bowel disease: friend of foe? World J Gastroenterol. 2011;17:557-566.
13. Nguyen GC, Kaplan GG, Harris ML, et al. A national survey of the prevalence and impact of Clostridium difficile infection among hospitalized inflammatory bowel disease patients. Am J Gastroenterol. 2008;103: 1443-1450.
14. Hofmann AF, Poley JR. Role of bile acid malabsorption in pathogenesis of diarrhea and steatorrhea in patients with ileal resection. I. Response to cholestyramine or replacement of dietary long chain triglyceride by medium chain triglyceride. Gastroenterology. 1972; 62:918-934.
15. Grabitske HA, Slavin JL. Gastrointestinal effects of low-digestible carbohydrates. Crit Rev Food Science Nutr. 2009;49:327-360.
16. Mekjian HS, Phillips SF, Hofmann AF. Colonic secretion of water and electrolytes induced by bile acids: perfusion studies in man. J Clin Invest. 1971;50:1569-1577.
17. Chadwick VS, Gaginella TS, Carlson GL, et al. Effect of molecular structure on bile acid-induced alterations in absorptive function, permeability, and morphology in the perfused rabbit colon. J Lab Clin Med. 1979;94: 661-674.
18. Binder HJ. Mechanisms of diarrhea in inflammatory bowel diseases. Ann N Y Acad Sci. 2009;1165:285-293.
19. Debongnie JC, Phillips SF. Capacity of the human colon to absorb fluid. Gastroenterology. 1978;74:698-703.
20. Aldini R, Roda A, Festi D, et al. Bile acid malabsorption and bile acid diarrhea in intestinal resection. Dig Dis Sci. 1982;27:495-502.
21. Binder HJ, Filburn C, Volpe BT. Bile salt alteration of colonic electrolyte transport role of cyclic adenosine monophosphate. Gastroenterology. 1975;68:503-508.
22. Davie RJ, Hosie KB, Grobler SP, et al. Ileal bile acid malabsorption in colonic Crohn's disease. Br J Surg. 1994;81:289-290.
23. Lenicek M, Duricova D, Komarek V, et al. Bile acid malabsorption in inflammatory bowel disease: Assessment by serum markers. Inflamm Bowel Dis. 2011;17:1322-1327.
24. Gothe F, Beigel F, Rust C, et al. Bile acid malabsorption assessed by 7 alpha-hydroxy-4-cholesten-3-one in pediatric inflammatory bowel disease: correlation to clinical and laboratory findings. J Crohns Colitis. 2014;8:1072-1078.
25. Jung D, Fantin AC, Scheurer U, et al. Human ileal bile acid transporter gene ASBT (SLC10A2) is transactivated by the glucocorticoid receptor. Gut. 2004;53:78-84.
26. Nyhlin H, Merrick MV, Eastwood MA. Bile acid malabsorption in Crohn's disease and indications for its assessment using SeHCAT. Gut. 1994;35:90-93.
27. Fromm H, Malavolti M. Bile acid-induced diarrhoea. Clin Gastroenterol. 1986;15:567-582.
28. Johnston I, Nolan J, Pattni SS, et al. New insights into bile acid malabsorption. Curr Gastroenterol Rep. 2011;13:418-425.
29. Oelkers P, Kirby LC, Heubi JE, et al. Primary bile acid malabsorption caused by mutations in the ileal sodium-dependent bile acid transporter gene (SLC10A2). J Clin Invest. 1997;99:1880-1887.
30. Walters JR, Tasleem AM, Omer OS, et al. A new mechanism for bile acid diarrhea: defective feedback inhibition of bile acid biosynthesis. Clin Gastroenterol Hepatol. 2009;7:1189-1194.
31. Trauner M, Claudel T, Fickert P, et al. Bile acids as regulators of hepatic lipid and glucose metabolism. Dig Dis. 2010;28:220-224.
32. Hofmann AF. Chemistry and enterohepatic circulation of bile acids. Hepatology. 1984;4:4-14.
33. Zwicker BL, Agellon LB. Transport and biological activities of bile acids. Int J Biochem Cell Biol. 2013;45:1389-1398.
34. Modica S, Gadaleta RM, Moschetta A. Deciphering the nuclear bile acid receptor FXR paradigm. Nucl Receptor Signaling. 2010;8:005.
35. Duboc H, Tache Y, Hofmann AF. The bile acid TGR5 membrane receptor: from basic research to clinical application. Dig Liver Dis. 2014;4: 302-312.
36. Holt JA, Luo G, Billin AN, et al. Definition of a novel growth factordependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev. 2003;17:1581-1591.
37. Chiang JY. Bile acids: regulation of synthesis. J Lipid Res. 2009;50: 1955-1966.
38. Alemi F, Poole DP, Chiu J, et al. The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice. Gastroenterology. 2013;144:145-154.
39. Rana SV, Sharma S, Malik A, et al. Small intestinal bacterial overgrowth and orocecal transit time in patients of inflammatory bowel disease. Dig Dis Sci. 2013;58:2594-2598.
40. Lorenzo-Zuniga V, Bartoli R, Planas R, et al. Oral bile acids reduce bacterial overgrowth, bacterial translocation, and endotoxemia in cirrhotic rats. Hepatology. 2003;37:551-557.
41. Chadwick VS, Modha K, Dowling RH. Mechanism for hyperoxaluria in patients with ileal dysfunction. N Engl J Med. 1973;289:172-176.
42. Vitek L, Carey MC. Enterohepatic cycling of bilirubin as a cause of 'black' pigment gallstones in adult life. Eur J Clin Invest. 2003;33: 799-810.
43. Ao M, Sarathy J, Domingue J, et al. Chenodeoxycholic acid stimulates Cl (-) secretion via cAMP signaling and increases cystic fibrosis transmembrane conductance regulator phosphorylation in T84 cells. Am J Physiol Cell Physiol. 2013;305:447-456.
44. Hofmann AF, Hagey LR. Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell Mol Life Sci. 2008;65:2461-2483.
45. Angelini G, Cavallini G, Bovo P, et al. Pancreatic function in chronic inflammatory bowel disease. Int J Pancreatol. 1988;3:185-193.
46. Cipriani S, Mencarelli A, Chini MG, et al. The bile acid receptor GPBAR- 1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. PLoS One. 2011;6:25637.
47. Raimondi F, Santoro P, Barone MV, et al. Bile acids modulate tight junction structure and barrier function of Caco-2 monolayers via EGFR activation. Am J Physiol Gastrointest Liver Physiol. 2008;294:906-913.
48. Fasano A, Budillon G, Guandalini S, et al. Bile acids reversible effects on small intestinal permeability. An in vitro study in the rabbit. Dig Dis Sci. 1990;35:801-808.
49. Zeissig S, Bergann T, Fromm A, et al. Altered ENaC expression leads to impaired sodium absorption in the noninflamed intestine in Crohn's disease. Gastroenterology. 2008;134:1436-1447.
50. Raimondi F, Crivaro V, Capasso L, et al. Unconjugated bilirubin modulates the intestinal epithelial barrier function in a human-derived in vitro model. Pediatr Res. 2006;60:30-33.
51. Armstrong DN, Krenz HK, Modlin IM, et al. Bile salt inhibition of motility in the isolated perfused rabbit terminal ileum. Gut. 1993;34:483-488.
52. Penagini R, Misiewicz JJ, Frost PG. Effect of jejunal infusion of bile acids on small bowel transit and fasting jejunal motility in man. Gut. 1988;29: 789-794.
53. Snape WJ Jr, Shiff S, Cohen S. Effect of deoxycholic acid on colonic motility in the rabbit. Am J Physiol. 1980;238:321-325.
54. Kidd M, Modlin IM, Gustafsson BI, et al. Luminal regulation of normal and neoplastic human EC cell serotonin release is mediated by bile salts, amines, tastants, and olfactants. Am J Physiol Gastrointest Liver Physiol. 2008;295:260-272.
55. Grider JR, Piland BE. The peristaltic reflex induced by short-chain fatty acids is mediated by sequential release of 5-HT and neuronal CGRP but not BDNF. Am J Physiol Gastrointest Liver Physiol. 2007;292: G429-G437.
56. Hofmann AF, Mysels KJ. Bile acid solubility and precipitation in vitro and in vivo: The role of conjugation, pH, and Ca2+ ions. J Lipid Res. 1992; 33:617-626.
57. Inagaki T, Moschetta A, Lee YK, et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc Natl Acad Sci USA. 2006;103:3920-3925.
58. Hueppelshaeuser R, von Unruh GE, Habbig S, et al. Enteric hyperoxaluria, recurrent urolithiasis, and systemic oxalosis in patients with Crohn's disease. Pediatr Nephrol. 2012;27:1103-1109.
59. Vitek L, Carey MC. New pathophysiological concepts underlying pathogenesis of pigment gallstones. Clin Res Hepatol Gastroenterol. 2012;36: 122-129.
60. Miettinen TA. Relationship between faecal bile acids, absorption of fat and vitamin B 12, and serum lipids in patients with ileal resections. Eur J Clin Invest. 1971;1:452-460.
61. Vijayvargiya P, Camilleri M, Shin A, et al. Methods for diagnosis of bile acid malabsorption in clinical practice. Clin Gastroenterol Hepatol. 2013; 11:1232-1239.
62. Farkkila MA, Kairemo KJ, Taavitsainen MJ, et al. Plasma lathosterol as a screening test for bile acid malabsorption due to ileal resection: correlation with 75SeHCAT test and faecal bile acid excretion. Clin Sci (Lond). 1996;90:315-319.
63. Peters AM, Walters JR. Recycling rate of bile acids in the enterohepatic recirculation as a major determinant of whole body 75SeHCAT retention. Eur J Nucl Med Mol Imaging. 2013;40:1618-1621.
64. Kovar J, Lenicek V, Zimolova M, et al. Regulation of diurnal variation of cholesterol 7alpha-hydroxylase (CYP7A1) activity in healthy subjects. Physiol Res. 2009;59:233-238.
65. Lenicek M, Juklova M, Zelenka J, et al. Improved HPLC analysis of serum 7alpha-hydroxycholest-4-en-3-one, a marker of bile acid malabsorption. Clin Chem. 2008;54:1087-1088.
66. Pattni SS, Brydon WG, Dew T, et al. Fibroblast growth factor 19 in patients with bile acid diarrhoea: A prospective comparison of FGF19 serum assay and SeHCAT retention. Aliment Pharmacol Ther. 2013;38:967-976.
67. Pattni SS, Brydon WG, Dew T, et al. Fibroblast growth factor 19 and 7 alpha-Hydroxy-4-Cholesten-3-one in the diagnosis of patients with possible bile acid diarrhea. Clin Transl Gastroenterol. 2012;3:18.
68. Moschetta A. Role of intestinal nuclear bile acid receptor FXR in the gut-liver axis. In: Keppler D, Stiehl A, Trauner M, eds. Bile Acid Biology and Therapeutic Actions. Cornwall, United Kingdom: Springer; 2009:135-142.
69. van Mil SW. Anti-inflammatory actions of FXR. In: Häussinger D, Trauner M, eds. XII International Bile Acid Meeting-Hepatic and Extrahepatic Targets of Bile Acid Signaling. Basel, Switzerland: Falk Foundation; 2012:66-71.
70. Gadaleta RM, Van Erpecum KJ, Oldenburg B, et al. Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease. Gut. 2011;60:463-472.
71. Renga B, Mencarelli A, Cipriani S, et al. The bile acid sensor FXR is required for immune-regulatory activities of TLR-9 in intestinal inflammation. PLoS One. 2013;8:54472.
72. Torok HP, Glas J, Endres I, et al. Epistasis between Toll-like receptor-9 polymorphisms and variants in NOD2 and IL23R modulates susceptibility to Crohn's disease. Am J Gastroenterol. 2009;104:1723-1733.
73. Vavassori P, Mencarelli A, Renga B, et al. The bile acid receptor FXR is a modulator of intestinal innate immunity. J Immunol. 2009;183: 6251-6261.
74. Nijmeijer RM, Gadaleta RM, van Mil SW, et al. Farnesoid X receptor (FXR) activation and FXR genetic variation in inflammatory bowel disease. PLoS One. 2011;6:23745.
75. van Schaik FD, Gadaleta RM, Schaap FG, et al. Pharmacological activation of the bile acid nuclear farnesoid X receptor is feasible in patients with quiescent Crohn's colitis. PLoS One. 2012;7:49706.
76. Mroz MS, Keating N, Ward J, et al. Farnesoid X receptor agonists attenuate colonic epithelial secretory function and prevent experimental diarrhoea in vivo. Gut. 2014;63:808-817.
77. Johnston I, Nolan JD, Dew T, et al. A novel, rational approach to treating primary bile acid diarrhea: A proof of concept study of the FXR agonist obeticholic acid. Gut. 2013;62(suppl 1):217-218.
78. Cantorna MT, Mahon BD. Mounting evidence for vitamin D as an environmental factor affecting autoimmune disease prevalence. Exp Biol Med (Maywood). 2004;229:1136-1142.
79. Ooi JH, Chen J, Cantorna MT. Vitamin D regulation of immune function in the gut: why do T cells have vitamin D receptors? Mol Aspects Med. 2012;33:77-82.
80. Mayne CG, Williams CB. Induced and natural regulatory T cells in the development of inflammatory bowel disease. Inflamm Bowel Dis. 2013; 19:1772-1788.
81. Ooi JH, Li Y, Rogers CJ, et al. Vitamin D regulates the gut microbiome and protects mice from dextran sodium sulfate-induced colitis. J Nutr. 2013;143:1679-1686.
82. Makishima M, Lu TT, Xie W, et al. Vitamin D receptor as an intestinal bile acid sensor. Science. 2002;296:1313-1316.
83. Gnewuch C, Liebisch G, Langmann T, et al. Serum bile acid profiling reflects enterohepatic detoxification state and intestinal barrier function in inflammatory bowel disease. World J Gastroenterol. 2009;15: 3134-3141.
84. Glas J, Seiderer J, Fischer D, et al. Pregnane X receptor (PXR/NR1I2) gene haplotypes modulate susceptibility to inflammatory bowel disease. Inflamm Bowel Dis. 2011;17:1917-1924.
85. Iwamoto J, Saito Y, Honda A, et al. Bile acid malabsorption deactivates pregnane X receptor in patients with Crohn's disease. Inflamm Bowel Dis. 2013;19:1278-1284.
86. Cheng J, Shah YM, Gonzalez FJ. Pregnane X receptor as a target for treatment of inflammatory bowel disorders. Trends Pharmacol Sci. 2012; 33:323-330.
87. Ma X, Shah YM, Guo GL, et al. Rifaximin is a gut-specific human pregnane X receptor activator. J Pharmacol Exp Ther. 2007;322:391-398.
88. Day AS, Gearry RB. Rifaximin and Crohn's disease: A new solution to an old problem? Dig Dis Sci. 2010;55:877-879.
89. Stepanov V, Stankov K, Mikov M. The bile acid membrane receptor TGR5: A novel pharmacological target in metabolic, inflammatory and neoplastic disorders. J Recept Signal Transduct Res. 2013;33:213-223.
90. Calmus Y, Guechot J, Podevin P, et al. Differential effects of chenodeoxycholic and ursodeoxycholic acids on interleukin 1, interleukin 6 and tumor necrosis factor-alpha production by monocytes. Hepatology. 1992;16: 719-723.
91. Kawamata Y, Fujii R, Hosoya M, et al. A G protein-coupled receptor responsive to bile acids. J Biol Chem. 2003;278:9435-9440.
92. Yoneno K, Hisamatsu T, Shimamura K, et al. TGR5 signalling inhibits the production of pro-inflammatory cytokines by in vitro differentiated inflammatory and intestinal macrophages in Crohn's disease. Immunology. 2013;139:19-29.