Interplay between bile acid metabolism and microbiota in irritable bowel syndrome

Neurogastroenterology and Motility

Volumn 28, Issue 9, 2016, Pages 1330-1340

  Dior, M ^a,b   Delagreverie H ^a   Duboc, H ^a,b   Jouet, P ^b,c   Coffin, B ^b,c   Brot, L ^a   Humbert, L ^a   Trugnan, G ^a   Seksik, P ^a,d   Sokol, H ^a,d,e   Rainteau, D ^a,d   Sabate, J M ^b,c  

^a Centre National de la Recherche Scientifique   (France)

^b HÔPITAL LOUIS MOURIER   (France)

^c HÔPITAL AMBROISE PARÉ   (France)

^d HÔPITAL SAINT ANTOINE   (France)

^e UMR1319 MICALIS   (France)

Author keywords

bile acid metabolism; irritable bowel syndrome; microbiota; neurogastroenterology

Indexed keywords

7ALPHA CHOLESTEN 3 ONE; BILE ACID; CHENODEOXYCHOLIC ACID; CHOLESTEROL DERIVATIVE; FIBROBLAST GROWTH FACTOR 19; UNCLASSIFIED DRUG;

ABDOMINAL PAIN; ADULT; AGED; ARTICLE; BACTEROIDES; BIFIDOBACTERIUM; BILE ACID BLOOD LEVEL; BILE ACID METABOLISM; CLINICAL ARTICLE; CONSTIPATION; CONTROLLED STUDY; DIARRHEA; DYSBIOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FECES MICROFLORA; FEMALE; HUMAN; IN VITRO STUDY; IRRITABLE COLON; MALE; MASS SPECTROMETRY; METAGENOMICS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

EID: 84983543551     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12829     Document Type: Article

References (46)

1. Choung RS, Locke GR 3rd. Epidemiology of IBS. Gastroenterol Clin North Am 2011; 40: 1–10.
2. Ducrotte P. [Irritable bowel syndrome: from the gut to the brain-gut]. Gastroenterol Clin Biol 2009; 33: 703–12.
3. Camilleri M, Katzka DA. Irritable bowel syndrome: methods, mechanisms, and pathophysiology. Genetic epidemiology and pharmacogenetics in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2012; 302: G1075–84.
4. Mayer EA, Naliboff BD, Craig AD. Neuroimaging of the brain-gut axis: from basic understanding to treatment of functional GI disorders. Gastroenterology 2006; 131: 1925–42.
5. Azpiroz F, Bouin M, Camilleri M, Mayer EA, Poitras P, Serra J, Spiller RC. Mechanisms of hypersensitivity in IBS and functional disorders. Neurogastroenterol Motil 2007; 19 (1 Suppl.): 62–88.
6. Ringel Y, Ringel-Kulka T. The intestinal microbiota and irritable bowel syndrome. J Clin Gastroenterol 2015; 49 (Suppl. 1): S56–9.
7. Kassinen A, Krogius-Kurikka L, Makivuokko H, Rinttila T, Paulin L, Corander J, Malinen E, Apajalahti J et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 2007; 133: 24–33.
8. Krogius-Kurikka L, Lyra A, Malinen E, Aarnikunnas J, Tuimala J, Paulin L, Corander J, Malinen E et al. Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers. BMC Gastroenterol 2009; 9: 95.
9. Malinen E, Rinttila T, Kajander K, Matto J, Kassinen A, Krogius L, Saarela M, Korpela R et al. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 2005; 100: 373–82.
10. Rajilic-Stojanovic M, Biagi E, Heilig HG, Kajander K, Kekkonen RA, Tims S, de Vos WM. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 2011; 141: 1792–801.
11. Bennet SM, Ohman L, Simren M. Gut microbiota as potential orchestrators of irritable bowel syndrome. Gut Liv 2015; 9: 318–31.
12. Bajor A, Tornblom H, Rudling M, Ung KA, Simren M. Increased colonic bile acid exposure: a relevant factor for symptoms and treatment in IBS. Gut 2015; 64: 84–92.
13. Shin A, Camilleri M, Vijayvargiya P, Busciglio I, Burton D, Ryks M, Rhoten D, Lueke A et al. Bowel functions, fecal unconjugated primary and secondary bile acids, and colonic transit in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 2013; 11: 1270–5 e1.
14. Wedlake L, A'Hern R, Russell D, Thomas K, Walters JR, Andreyev HJ. Systematic review: the prevalence of idiopathic bile acid malabsorption as diagnosed by SeHCAT scanning in patients with diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther 2009; 30: 707–17.
15. Bajor A, Gillberg PG, Abrahamsson H. Bile acids: short and long term effects in the intestine. Scand J Gastroenterol 2010; 45: 645–64.
16. Gerard P. Metabolism of cholesterol and bile acids by the gut microbiota. Pathogens 2013; 3: 14–24.
17. Jarocki P, Podlesny M, Glibowski P, Targonski Z. A new insight into the physiological role of bile salt hydrolase among intestinal bacteria from the genus bifidobacterium. PLoS ONE 2014; 9: e114379.
18. Ridlon JM, Kang DJ, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res 2006; 47: 241–59.
19. Duboc H, Rainteau D, Rajca S, Humbert L, Farabos D, Maubert M, Grondin V, Jouet P et al. Increase in fecal primary bile acids and dysbiosis in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil 2012; 24: 513–20, e246-7.
20. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterology 2006; 130: 1480–91.
21. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 2008; 105: 16731–6.
22. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009; 15: 1183–9.
23. Furet JP, Firmesse O, Gourmelon M, Bridonneau C, Tap J, Mondot S, Doré J, Corthier G. Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol Ecol 2009; 68: 351–62.
24. Camilleri M, Nadeau A, Tremaine WJ, Lamsam J, Burton D, Odunsi S, Sweetser S, Singh R. Measurement of serum 7alpha-hydroxy-4-cholesten-3-one (or 7alphaC4), a surrogate test for bile acid malabsorption in health, ileal disease and irritable bowel syndrome using liquid chromatography-tandem mass spectrometry. Neurogastroenterol Motil 2009; 21: 734–e43.
25. Humbert L, Maubert MA, Wolf C, Duboc H, Mahe M, Farabos D, Seksik P, Mallet JM et al. Bile acid profiling in human biological samples: comparison of extraction procedures and application to normal and cholestatic patients. J Chromatogr B Analyt Technol Biomed Life Sci 2012; 899: 135–45.
26. Duboc H, Rajca S, Rainteau D, Benarous D, Maubert MA, Quervain E, Thomas G, Barbu V et al. Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 2013; 62: 531–9.
27. Sinha J, Chen F, Miloh T, Burns RC, Yu Z, Shneider BL. beta-Klotho and FGF-15/19 inhibit the apical sodium-dependent bile acid transporter in enterocytes and cholangiocytes. Am J Physiol Gastrointest Liver Physiol 2008; 295: G996–1003.
28. Walters JR, Tasleem AM, Omer OS, Brydon WG, Dew T, le Roux CW. A new mechanism for bile acid diarrhea: defective feedback inhibition of bile acid biosynthesis. Clin Gastroenterol Hepatol 2009; 7: 1189–94.
29. Odunsi-Shiyanbade ST, Camilleri M, McKinzie S, Burton D, Carlson P, Busciglio IA, Lamsam J, Singh R et al. Effects of chenodeoxycholate and a bile acid sequestrant, colesevelam, on intestinal transit and bowel function. Clin Gastroenterol Hepatol 2010; 8: 159–65.
30. Thomas LA, Veysey MJ, French G, Hylemon PB, Murphy GM, Dowling RH. Bile acid metabolism by fresh human colonic contents: a comparison of caecal versus faecal samples. Gut 2001; 49: 835–42.
31. Parkes GC, Rayment NB, Hudspith BN, Petrovska L, Lomer MC, Brostoff J, Whelan K, Sanderson JD. Distinct microbial populations exist in the mucosa-associated microbiota of sub-groups of irritable bowel syndrome. Neurogastroenterol Motil 2012; 24: 31–9.
32. Jeffery IB, O'Toole PW, Ohman L, Claesson MJ, Deane J, Quigley EM, Simrén M. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut 2012; 61: 997–1006.
33. Williams AJ, Merrick MV, Eastwood MA. Idiopathic bile acid malabsorption–a review of clinical presentation, diagnosis, and response to treatment. Gut 1991; 32: 1004–6.
34. Wong BS, Camilleri M, Carlson P, McKinzie S, Busciglio I, Bondar O, Dyer RB, Lamsam J et al. Increased bile acid biosynthesis is associated with irritable bowel syndrome with diarrhea. Clin Gastroenterol Hepatol 2012; 10: 1009–15 e3.
35. Hofmann AF. Chronic diarrhea caused by idiopathic bile acid malabsorption: an explanation at last. Expert Rev Gastroenterol Hepatol 2009; 3: 461–4.
36. Camilleri M, Busciglio I, Acosta A, Shin A, Carlson P, Burton D, Ryks M, Rhoten D et al. Effect of increased bile acid synthesis or fecal excretion in irritable bowel syndrome-diarrhea. Am J Gastroenterol 2014; 109: 1621–30.
37. Camilleri M, Acosta A, Busciglio I, Boldingh A, Dyer RB, Zinsmeister AR, Lueke A, Gray A et al. Effect of colesevelam on faecal bile acids and bowel functions in diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther 2015; 41: 438–48.
38. Oddsson E, Rask-Madsen J, Krag E. A secretory epithelium of the small intestine with increased sensitivity to bile acids in irritable bowel syndrome associated with diarrhoea. Scand J Gastroenterol 1978; 13: 408–16.
39. Rao AS, Wong BS, Camilleri M, Odunsi-Shiyanbade ST, McKinzie S, Ryks M, Burton D, Carlson P et al. Chenodeoxycholate in females with irritable bowel syndrome-constipation: a pharmacodynamic and pharmacogenetic analysis. Gastroenterology 2010; 139: 1549–58, 58 e1.
40. Hofmann AF, Loening-Baucke V, Lavine JE, Hagey LR, Steinbach JH, Packard CA, Griffin TL, Chatfield DA. Altered bile acid metabolism in childhood functional constipation: inactivation of secretory bile acids by sulfation in a subset of patients. J Pediatr Gastroenterol Nutr 2008; 47: 598–606.
41. Ferrandi EE, Bertolesi GM, Polentini F, Negri A, Riva S, Monti D. In search of sustainable chemical processes: cloning, recombinant expression, and functional characterization of the 7alpha- and 7beta-hydroxysteroid dehydrogenases from Clostridium absonum. Appl Microbiol Biotechnol 2012; 95: 1221–33.
42. Camilleri M, Shin A, Busciglio I, Carlson P, Acosta A, Bharucha AE, Burton D, Lamsam J et al. Genetic variation in GPBAR1 predisposes to quantitative changes in colonic transit and bile acid excretion. Am J Physiol Gastrointest Liver Physiol 2014; 307: G508–16.
43. Pavlovic N, Stankov K, Mikov M. Probiotics–interactions with bile acids and impact on cholesterol metabolism. Appl Biochem Biotechnol 2012; 168: 1880–95.
44. Bampton PA, Dinning PG, Kennedy ML, Lubowski DZ, Cook IJ. The proximal colonic motor response to rectal mechanical and chemical stimulation. Am J Physiol Gastrointest Liver Physiol 2002; 282: G443–9.
45. Edwards CA, Brown S, Baxter AJ, Bannister JJ, Read NW. Effect of bile acid on anorectal function in man. Gut 1989; 30: 383–6.
46. Coremans G, Tack J, Vantrappen G, Janssens J, Annese V. Is the irritable bowel really irritable? Ital J Gastroenterol 1991; 23 (8 Suppl. 1): 39–40.