Increasing ursodeoxycholic acid in the enterohepatic circulation of pigs through the administration of living bacteria

British Journal of Nutrition

Volumn 93, Issue 4, 2005, Pages 457-469

  Lepercq, Pascale ^a   Hermier, Dominique ^b   David, Olivier ^c   Michelin, Rachel ^a   Gibard, Clotilde ^a   Beguet, Fabienne ^a   Relano, Purification ^d   Cayuela, Chantal ^d   Juste, Catherine ^a  

^a CEMAGREF   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UR341 National Agronomical Research Institute (INRA)   (France)

^d Danone Vitapole   (France)

Author keywords

Bile acids; Blood lipids; Probiotics; Ursodeoxycholic acid

Indexed keywords

BILE ACID; BILE SALT; CHENODEOXYCHOLIC ACID; CHOLESTEROL; LIPOPROTEIN; LITHOCHOLIC ACID; URSODEOXYCHOLIC ACID; ISOMERASE; PROBIOTIC AGENT;

ANIMAL EXPERIMENT; ARTICLE; BACTERIUM; BIFIDOBACTERIUM ANIMALIS; CLOSTRIDIUM; CONTROLLED STUDY; ENTEROHEPATIC CIRCULATION; FECES ANALYSIS; HYDROLYSIS; IN VITRO STUDY; LIPID BLOOD LEVEL; NONHUMAN; PORTAL VEIN; SWINE; ANIMAL; ANIMAL MODEL; BIFIDOBACTERIUM; BIOAVAILABILITY; BLOOD; HYPERCHOLESTEROLEMIA; MALE; METABOLISM; MICROBIOLOGY; ORAL DRUG ADMINISTRATION; STOMACH;

ANIMALIA; BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM ANIMALIS; CLOSTRIDIUM; CLOSTRIDIUM SARDINIENSE; SUS SCROFA;

ADMINISTRATION, ORAL; ANIMALS; BACTERIA; BIFIDOBACTERIUM; BIOLOGICAL AVAILABILITY; CHENODEOXYCHOLIC ACID; CLOSTRIDIUM; ENTEROHEPATIC CIRCULATION; HYPERCHOLESTEROLEMIA; MALE; MODELS, ANIMAL; PROBIOTICS; RACEMASES AND EPIMERASES; STOMACH; SWINE; URSODEOXYCHOLIC ACID;

EID: 23044434946     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1079/BJN20041386     Document Type: Article

References (69)

1. Agerholm-Larsen L, Raben A, Haulrik N, Hansen AS, Manders M & Astrup A (2000) Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur J Clin Nutr 54, 288-297.
2. Aldini R, Roda A, Montagnani M, Cerrè C, Pellicciari R & Roda E (1996) Relationship between structure and intestinal absorption of bile acids with a steroid or side-chain modification. Steroids 61, 590-597.
3. Bachrach WH & Hofmann AF (1982) Ursodeoxycholic acid treatment of cholesterol cholelithiasis Part II. Dig Dis Sci 27, 833-856.
4. Baijal PK, Fitzpatrick DW & Bird RP (1998) Comparative effects of secondary bile acids, deoxycholic and lithocholic acids, on aberrant crypt foci growth in the postinitiation phases of colon carcinogenesis. Nutr Cancer 31, 81-89.
5. Baron SF, Franklund CV & Hylemon PB (1991) Cloning, sequencing, and expression of the gene coding for bile acid 7α-hydroxysteroid dehydrogenase from Eubacterium sp. strain VPI 12708. J Bacteriol 173, 4558-4569.
6. Batta AK, Salen G, Holubec H, Brasitus TA, Alberts D & Earnest DL (1998) Enrichment of the more hydrophilic bile acid ursodeoxycholic acid in the fecal water-soluble fraction after feeding to rats with colon polyps. Cancer Res 58, 1684-1687.
7. Bennett MJ, McKnight SL & Coleman JP (2003) Cloning and characterization of the NAD-dependent 7α-hydroxysteroid dehydrogenase from Bacteroides fragilis. Curr Microbiol 47, 475-484.
8. Brown I, Warhurst M, Arcot J, Playne M, Illman RJ & Topping DL (1997) Fecal numbers of bifidobacteria are higher in pigs fed Bifidobacterium longum with a high amylose cornstarch than with a low amylose cornstarch. J Nutr 127, 1822-1827.
9. Chen RM, Wu JJ, Lee SC, Huang AH & Wu HM (1999) Increase of intestinal Bifidobacterium and suppression of coliform bacteria with short-term yogurt ingestion. J Dairy Sci 82, 2308-2314.
10. Coleman JP, Hudson LL & Adams MJ (1994) Characterization and regulation of the NADP-linked 7α-hydroxysteroid dehydrogenase gene from Clostridium sordellii. J Bacteriol 176, 4865-4874.
11. Colombo C, Setchell KD, Podda M, Crosignani A, Roda A, Curcio L, Ronchi M & Giunta A (1990) Effects of ursodeoxycholic acid therapy for liver disease associated with cystic fibrosis. J Pediatr 117, 482-489.
12. Combes B, Carithers RL Jr, Maddrey WC, Lin D, McDonald MF, Wheeler DE, Eigenbrodt EH, Munoz SJ, Rubin R & Garcia-Tsao G (1995) A randomized, double-blind, placebo-controlled trial of ursodeoxycholic acid in primary biliary cirrhosis. Hepatology 22, 759-766.
13. Crosignani A, Setchell KD, Invernizzi P, Larghi A, Rodrigues CM & Podda M (1996) Clinical pharmacokinetics of therapeutic bile acids. Clin Pharmacokinet 30, 333-358.
14. De Rodas BZ, Gilliland SE & Maxwell CV (1996) Hypocholesterolemic action of Lactobacillus acidophilus ATCC 43121 and calcium in swine with hypercholesterolemia induced by diet. J Dairy Sci 79, 2121-2128.
15. De Smet I, De Boever P & Verstraete W (1998) Cholesterol lowering in pigs through enhanced bacterial bile salt hydrolase activity. Br J Nutr 79, 185-194.
16. Drouault S & Corthier G (2001) Health effects of lactic acid bacteria ingested in fermented milk. Vet Res 32, 101-117.
17. Drouault S, Anba J & Corthier G (2002) Streptococcus thermophilus is able to produce a β-galactosidase active during its transit in the digestive tract of germ-free mice. Appl Environ Microbiol 68, 938-941.
18. Earnest DL, Holubec H, Wali RK, Jolley CS, Bissonette M, Bhattacharyya AK, Roy H, Khare S & Brasitus TA (1994) Chemoprevention of azoxymethane-induced colonic carcinogenesis by supplemented dietary ursodeoxycholic acid. Cancer Res 54, 5071-5074.
19. Ellis E, Axelson M, Abrahamsson A, Eggertsen G, Thorne A, Nowak G, Ericzon BG, Bjorkhem I & Einarsson C (2003) Feedback regulation of bile acid synthesis in primary human hepatocytes: evidence that CDCA is the strongest inhibitor. Hepatology 38, 930-938.
20. Fedorowski T, Salen G, Tint GS & Mosbach E (1979) Transformation of chenodeoxycholic acid and ursodeoxycholic acid by human intestinal bacteria. Gastroenterology 77, 1068-1073.
21. Ferezou J, Riottot M, Serougne C, et al. (1997) Hypocholesterolemic action of β-cyclodextrin and its effects on cholesterol metabolism in pigs fed a cholesterol-enriched diet. J Lipid Res 38, 86-100.
22. Fischer S, Neubrand M & Paumgartner G (1993) Biotransformation of orally administered ursodeoxycholic acid in man as observed in gall-bladder bile, serum and urine. Eur J Clin Invest 23, 28-36.
23. Fossati P & Prencipe L (1982) Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin Chem 28, 2077-2080.
24. Fujiwara S, Seto Y, Kimura A & Hashiba H (2001) Intestinal transit of an orally administered streptomycin-rifampicin-resistant variant of Bifidobacterium longum SBT2928: its long-term survival and effect on the intestinal microflora and metabolism. J Appl Microbiol 90, 43-52.
25. Hayase M, Mitsui N, Tamai K, Nakamura S & Nishida S (1974) Isolation of Clostridium absonum and its cultural and biochemical properties. Infect Immun 9, 15-19.
26. Hirano S, Nakama R, Tamaki M, Masuda N & Oda H (1981) Isolation and characterization of thirteen intestinal microorganisms capable of 7α-dehydroxylating bile acids. Appl Environ Microbiol 41, 737-745.
27. Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. Methods Microbiol 3B, 117-132.
28. Invernizzi P, Setchell KD, Crosignani A, Battezzati PM, Larghi A, O'Connell NC & Podda M (1999) Differences in the metabolism and disposition of ursodeoxycholic acid and its taurine-conjugated species in patients with primary biliary cirrhosis. Hepatology 29, 320-327.
29. Juste C, Corring T & Le Coz Y (1983) Bile restitution procedures for studying bile secretion in fistulated pigs. Lab Anim Sci 33, 199-202.
30. Kenward MG & Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983-997.
31. Kozoni V, Tsioulias G, Shiff S & Rigas B (2000) The effect of lithocholic acid on proliferation and apoptosis during the early stages of colon carcinogenesis: differential effect on apoptosis in the presence of a colon carcinogen. Carcinogenesis 21, 999-1005.
32. Latta RK, Fiander H, Ross NW, Simpson C & Schneider H (1993) Toxicity of bile acids to colon cancer cell lines. Cancer Lett 16, 167-173.
33. Legrand-Defretin V, Juste C, Corring T & Rerat A (1986) Enterohepatic circulation of bile acids in pigs: diurnal pattern and effect of a reentrant biliary fistula. Am J Physiol 250, G295-G301.
34. Lepercq P, Gérard P, Béguet F, Raibaud P, Grill JP, Relano P, Cayuela C & Juste C (2004a) Epimerization of chenodeoxycholic acid to ursodeoxycholic acid by Clostridium baratii isolated from human feces. FEMS Microbiol Lett 235, 65-72.
35. Lepercq P, Gérard P, Béguet F, Grill JP, Relano P, Cayuela C & Juste C (2004b) Isolates from normal human intestinal flora but not lactic acid bacteria exhibit 7α- and 7β-hydroxysteroid dehydrogenase activities. Microbial Ecol Health Dis 16, 195-201.
36. Lepercq P, Relano P, Cayuela C & Juste C (2004c) Bifidobacterium animalis strain DN-173 010 hydrolyses bile salts in the gastrointestinal tract of pigs. Scand J Gastroenterol 39, 1266-1271.
37. Lindor KD, Lacerda MA, Jorgensen RA, DeSotel CK, Batta AK, Salen G, Dickson ER, Rossi SS & Hofmann AF (1998) Relationship between biliary and serum bile acids and response to ursodeoxycholic acid in patients with primary biliary cirrhosis. Am J Gastroenterol 93, 1498-1504.
38. Macdonald IA & Roach PD (1981) Bile salt induction of 7α- and 7β-hydroxysteroid dehydrogenases in Clostridium absonum. Biochim Biophys Acta 665, 262-269.
39. Macdonald IA, Hutchison DM & Forrest TP (1981) Formation of urso-and ursodeoxy-cholic acids from primary bile acids by Clostridium absonum. J Lipid Res 22, 458-466.
40. Marsh A, Kim DN, Lee KT, Reiner JM & Thomas WA (1972) Cholesterol turnover, synthesis, and retention in hypercholesterolemic growing swine. J Lipid Res 13, 600-615.
41. Nowak G, Ungerstedt J, Marschall H-U, Einarsson C & Ericzon B-G (2001) Pre-treatment with ursodeoxycholic acid diminishes nonoxidative glycolysis in a pig liver transplantation model. Hepatology 34, 294A.
42. Oyama K, Shiota G, Ito H, Murawaki Y & Kawasaki H (2002) Reduction of hepatocarcinogenesis by ursodeoxycholic acid in rats. Carcinogenesis 23, 885-892.
43. Pereira DI & Gibson GR (2002) Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Crit Rev Biochem Mol Biol 37, 259-281.
44. Pochart P, Marteau P, Bouhnik Y, Goderel I, Bourlioux P & Rambaud J-C (1992) Survival of bifidobacteria ingested via fermented milk during their passage through the human small intestine: an in vivo study using intestinal perfusion. Am J Clin Nutr 55, 78-80.
45. Podda M, Ghezzi C, Battezzati PM, Crosignani A, Zuin M & Roda A (1990) Effects of ursodeoxycholic acid and taurine on serum liver enzymes and bile acids in chronic hepatitis. Gastroenterology 98, 1044-1050.
46. Ponz de Leon M, Carulli N, Loria P, Iori R & Zironi F (1980) Cholesterol absorption during bile acid feeding: effect of ursodeoxycholic acid (UDCA) administration. Gastroenterology 78, 214-219.
47. Poupon RE, Ouguerram K, Chrétien Y, Verneau C, Eschwège E, Magot T & Poupon R (1993) Cholesterol-lowering effect of ursodeoxycholic acid in patients with primary biliary cirrhosis. Hepatology 17, 577-582.
48. Raicht RF, Cohen BI, Sarwal A & Takahashi M (1978) Ursodeoxycholic acid. Effects on sterol metabolism in rats. Biochim Biophys Acta 531, 1-8.
49. Reynier MO, Montet JC, Gerolami A, Marteau C, Crotte C, Montet AM & Mathieu S (1981) Comparative effects of cholic, chenodeoxycholic, and ursodeoxycholic acids on micellar solubilization and intestinal absorption of cholesterol. J Lipid Res 22, 467-473.
50. Richelsen B, Kristensen K & Pedersen SB (1996) Long-term (6 months) effect of a new fermented milk product on the level of plasma lipoproteins - a placebo-controlled and double blind study. Eur J Clin Nutr 50, 811-815.
51. Richmond W (1973) Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin Chem 19, 1350-1356.
52. Riottot M, Olivier P, Huet A, Caboche J-J, Parquet M, Khallou J & Lutton C (1993) Hypolipidemic effects of β-cyclodextrin in the hamster and in the genetically hypercholesterolemic Rico rat. Lipids 28, 181-188.
53. Roberfroid MB (2000) Prebiotics and probiotics: are they functional foods? Am J Clin Nutr 71, 1682S-1687S; discussion 1688S-1690S.
54. Sarva RP, Fromm H, Carlson GL, Mendelow L & Ceryak S (1980) Intracolonic conversion in man of chenodeoxycholic acid (CDC) to ursodeoxycholic acid (UDC) with and without formation of 7-keto lithocholic acid (KLC) as an intermediate. Gastroenterology 78, 1252, Abstr.
55. Seraj MJ, Umemoto A, Kajikawa A, Mimura S, Kinouchi T, Ohnishi Y & Monden Y (1997) Effects of dietary bile acids on formation of azoxymethane-induced aberrant crypt foci in F344 rats. Cancer Lett 115, 97-103.
56. Shimizu H, Yoshii M, Seki A, Une M & Hoshita T (1992) Hypocholesterolemic effect of ursodeoxycholylcysteic acid in hamsters fed a high cholesterol diet. J Pharmacobiodyn 15, 573-580.
57. Simoni P, Cerrè C, Cipolla A, Polimeni C, Pistillo A, Ceschel G, Roda E & Roda A (1995) Bioavailability study of a new, sinking, enteric-coated ursodeoxycholic acid formulation. Pharmacol Res 31, 115-119.
58. Sutherland JD & Williams CN (1985) Bile acid induction of 7α- and 7β-hydroxysteroid dehydrogenases in Clostridium limosum. J Lipid Res 26, 344-350.
59. Takayama M, Itoh S, Nagasaki T & Tanimizu I (1977) A new enzymatic method for determination of serum choline-containing phospholipids. Clin Chim Acta 79, 93-98.
60. Taranto MP, Medici M, Perdigon G, Ruiz Holgado AP & Valdez GF (1998) Evidence for hypocholesterolemic effect of Lactobacillus reuteri in hypercholesterolemic mice. J Dairy Sci 81, 2336-2340.
61. Turley SD & Dietschy JM (1978) Re-evaluation of the 3α-hydroxysteroid dehydrogenase assay for total bile acids in bile. J Lipid Res 19, 924-928.
62. Usman HA (2001) Hypocholesterolemic effect of Lactobacillus gasseri SBT0270 in rats fed a cholesterol-enriched diet. J Dairy Res 68, 617-624.
63. van Gorkom BA, van der Meer R, Boersma-van Ek W, Termont DS, de Vries EG & Kleibeuker JH (2002) Changes in bile acid composition and effect on cytolytic activity of fecal water by ursodeoxycholic acid administration: a placebo-controlled cross-over intervention trial in healthy volunteers. Scand J Gastroenterol 37, 965-971.
64. Varnam AH & Sutherland JP (1994) Milk and Milk Products: Technology, Chemistry and Microbiology, pp. 347-380. London: Chapman & Hall.
65. Wali RK, Stoiber D, Nguyen L, Hart J, Sitrin MD, Brasitus T & Bissonnette M (2002) Ursodeoxycholic acid inhibits the initiation and postinitiation phases of azoxymethane-induced colonic tumor development. Cancer Epidemiol Biomarkers Prev 11, 1316-1321.
66. Wang X, Brown IL, Evans AJ & Conway PL (1999) The protective effects of high amylose maize (amylomaize) starch granules on the survival of Bifidobacterium spp. in the mouse intestinal tract. J Appl Microbiol 87, 631-639.
67. Woollett LA, Buckley DD, Yao L, Jones PJ, Granholm NA, Tolley EA & Heubi JE (2003) Effect of ursodeoxycholic acid on cholesterol absorption and metabolism in humans. J Lipid Res 44, 935-942.
68. Xiao JZ, Kondo S, Takahashi N, Miyaji K, Oshida K, Hiramatsu A, Iwatsuki K, Kokubo S & Hosono A (2003) Effects of milk products fermented by Bifidobacterium longum on blood lipids in rats and healthy adult male volunteers. J Dairy Sci 86, 2452-2461.
69. Yoshimoto T, Higashi H, Kanatani A, Lin XS, Nagai H, Oyama H, Kurazono K & Tsuru D (1991) Cloning and sequencing of the 7α-hydroxysteroid dehydrogenase gene from Escherichia coli HB 101 and characterization of the expressed enzyme. J Bacteriol 173, 2173-2179.