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Cholesterol lowering in pigs through enhanced bacterial bile salt hydrolase activity

Published online by Cambridge University Press:  09 March 2007

I. De Smet ,
P. De Boever  and
W. Verstraete
I. De Smet
Affiliation:
Laboratory of Microbial Ecology, Faculty of Agricultural and Applied Biological Sciences, University Gent, Coupure Links 653, B-9000 Gent, Belgium
P. De Boever
Affiliation:
Laboratory of Microbial Ecology, Faculty of Agricultural and Applied Biological Sciences, University Gent, Coupure Links 653, B-9000 Gent, Belgium
W. Verstraete*
Affiliation:
Laboratory of Microbial Ecology, Faculty of Agricultural and Applied Biological Sciences, University Gent, Coupure Links 653, B-9000 Gent, Belgium
*
*Corresponding author:Professor W. Verstraete, fax + 32 (0)9 264 62 48, email [email protected]
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Abstract

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The effect of feeding live Lactobacillus reuteri cells containing active bile salt hydrolase (BSH) on plasma cholesterol levels was studied in pigs. During an experiment lasting 13 weeks, twenty pigs were fed on a high-fat, high-cholesterol, low-fibre diet for the first 10 weeks, and a regular pig diet for the last 3 weeks. One group of animals received, twice daily, 11·25 (SD 0·16) log10 colony forming units of the potential probiotic bacteria for 4 weeks (from week 3 until week 7). From week 8 onwards, the treated group was again fed on the same diet as the control group without additions. The total faecal Lactobacillus counts were only significantly higher in the treated pigs during the first 2 weeks of L. reuteri feeding. Based on limited data, it was suggested that the administered Lactobacillus species had caused a temporary shift within the indigenous Lactobacillus population rather than permanently colonizing the intestinal tract. The probiotic feeding brought about significant lowering (P ≤ 0·05) of total and LDL-cholesterol concentrations in the treated pigs compared with the control pigs, while no change in HDL-cholesterol concentration was observed. The data for faecal output of neutral sterols and bile salts were highly variable between the animals of each group, yet they indicated an increased output in the treated pigs. Although the blood cholesterol levels went up in both groups during the 3 weeks following the Lactobacillus administration period, significantly lower serum total and LDL-cholesterol levels were observed in the treated pigs. During the final 3 weeks of normalization to the regular diet, cholesterol concentrations significantly decreased in both animal groups and the differences in total and LDL-cholesterol concentrations between the groups largely disappeared.

Keywords

LactobacilliBile saltsSerum cholesterolPig
Type
General Nutrition
Information
British Journal of Nutrition , Volume 79 , Issue 2 , February 1998 , pp. 185 - 194
Copyright
Copyright © The Nutrition Society 1998

References

Agerbæk, M, Gerdes, LU & Richelsen, B (1995) Hypocholester-olaemic effect of a new fermented milk product in healthy middle-aged men. European Journal of Clinical Nutrition 49, 346–352.Google ScholarPubMed
Allain, CC, Poon, LS, Chan, CSG, Richmond, W & Fu, PC (1974) Enzymatic determination of total serum cholesterol. Clinical Chemistry 20, 470–475.CrossRefGoogle ScholarPubMed
Aries, VC, Crowther, JS, Drasar, BS, Hill, MJ & Williams, REO (1969) Bacteria and the aetiology of cancer of the large bowel. Gut 10, 334–335.CrossRefGoogle ScholarPubMed
Armstrong, B & Doll, R (1975) Environmental factors and cancer incidence and mortality in different countries with special reference to dietary practices. International Journal of Cancer 15, 617–631.CrossRefGoogle ScholarPubMed
Black, DD & Davidson, NO (1989) Intestinal apolipoprotein synthesis and secretion in the suckling pig. Journal of Lipid Research 30, 207–218.CrossRefGoogle ScholarPubMed
Black, DD, Rohwer-Nutter, PL & Davidson, NO (1990) Intestinal apo A-IV gene expression in the piglet. Journal of Lipid Research 31, 497–505.CrossRefGoogle ScholarPubMed
Chapman, MJ (1986) Comparative analysis of mammalian plasma lipoproteins. Methods in Enzymology 128, 70–143.CrossRefGoogle ScholarPubMed
Chikai, T, Nakao, H & Uchida, K (1987) Deconjugation of bile acids by human intestinal bacteria implanted in germ-free rats. Lipids 22, 669–671.CrossRefGoogle ScholarPubMed
Cohen, BI, Raicht, FR, Deschner, EE, Takahashi, M, Sarwal, AN & Fazzini, E (1980) Effect of cholic acid feeding on N-methyl-N-nitrosourea-induced colon tumors and cell kinetics in rats. Journal of the National Cancer Institute 64, 573–578.Google ScholarPubMed
Costa, NMB, Low, AG, Walker, AF, Owen, RW & Englyst, HN (1994) Effect of baked beans (Phaseolus vulgaris) on sterol metabolism and non-starch polysaccharide output of hyperch-olesterolaemic pigs with or without an ileo-rectal anastomosis. British Journal of Nutrition 71, 871–886.CrossRefGoogle ScholarPubMed
Danielson, AD, Peo, ER, Shahani, KM, Lewis, AJ, Whalen, PJ & Amer, MA (1989) Anticholesterolemic property of Lactobacillus acidophilus yogurt fed to mature boars. Journal of Animal Science 67, 966–974.CrossRefGoogle Scholar
Dashkevicz, MP & Feighner, SD (1989) Development of a differential medium for bile salt hydrolase active Lactobacillus sp. Applied and Environmental Microbiology 55, 11–16.CrossRefGoogle Scholar
De Smet, I, Van Hoorde, L, De Saeyer, N, Vande Woestyne, M & Verstraete, W (1994) In vitro study of bile salt hydrolase (BSH) activity of BSH isogenic Lactobacillus plantarum 80 strains and estimation of cholesterol lowering through enhanced BSH activity. Microbial Ecology in Health and Disease 7, 315–329.CrossRefGoogle Scholar
Dupont, J, Oh, S-Y, O'Deen, L, McClellan, MA, Lumb, WV & Butterfield, AB (1974) Cholesterol and bile acid turnover in miniature swine. Lipids 9, 717–721.CrossRefGoogle ScholarPubMed
Fossati, P & Prencipe, L (1982) Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clinical Chemistry 28, 2077–2080.CrossRefGoogle ScholarPubMed
Friedewald, WT, Levy, RJ & Frederickson, DS (1972) Estimation of the concentration of low-density-lipoprotein cholesterol in plasma, without use of the preparative centrifuge. Clinical Chemistry 18, 499–502.CrossRefGoogle Scholar
Fukushima, M & Nakano, M (1995) The effect of a probiotic on faecal and liver lipid classes in rats. British Journal of Nutrition 73, 701–710.CrossRefGoogle ScholarPubMed
Grundy, SM (1972) Treatment of hypercholesterolaemia by interference with bile acid metabolism. Archives of Internal Medicine 130, 638–648.CrossRefGoogle ScholarPubMed
Grundy, SM, Ahrens, EH Jr & Salen, G (1972) Interruption of the enterohepatic circulation of bile acids in man: comparative effect of cholestyramine and ileal exclusion on cholesterol metabolism. Journal of Laboratory and Clinical Medicne 78, 94–121.Google Scholar
Gustafsson, BE, Gustafsson, JA & Carlstedt-Duke, B (1977) Prolonged induction of germ-free bile acid pattern in conventional rats by antibiotics. Acta Medica Scandinavica 201, 155–160.CrossRefGoogle ScholarPubMed
Hylemon, PB & Glass, TL (1983) Biotransformations of bile acids and cholesterol by the intestinal microflora. In Human Intestinal Flora in Health and Disease, pp. 79–99 [Hentges, DJ, editor]. New York: Academic Press.Google Scholar
Juste, C, Demarne, Y & Corring, T (1983) Response of bile flow, biliary lipids and bile acid pool in the pig to quantitative variations in dietary fat. Journal of Nutrition 113, 1691–1701.CrossRefGoogle ScholarPubMed
Kandell, RL & Bernstein, C (1991) Bile salt/acid induction of DNA damage in bacterial and mammalian cells: implications for colon cancer. Nutrition and Cancer 16, 227–238.CrossRefGoogle ScholarPubMed
Kidder, DE & Manners, MJ (1978) Digestion in the Pig. Bath: Kingston Press.Google Scholar
Kim, DN, Lee, KT, Reiner, JM & Thomas, WA (1980) Increased steroid excretion in swine fed high-fat, high-cholesterol diet with soy protein. Experimental and Molecular Pathology 33, 25–35.CrossRefGoogle ScholarPubMed
Korpela, JT, Adlercreutz, H & Turunen, MJ (1988) Fecal free and conjugated bile acids and neutral sterols in vegetarians, omnivores and patients with colorectal cancer. Scandinavian Journal of Gastroenterology 23, 277–283.CrossRefGoogle ScholarPubMed
Lapré, JA, de Vries, HT, Termont, DSML, Kleibeuker, JH, de Vries, EGE & van der Meer, R (1993) Mechanisms of the protective effect of supplemental dietary calcium on cytolytic activity of fecal water. Cancer Research 53, 248–253.Google ScholarPubMed
Madsen, DC, Worstmann, BJ, Beaver, M & Chang, L (1978) Effects of aureomycin on bile acids in rats. Journal of Laboratory and Clinical Medicine 91, 605–611.Google ScholarPubMed
Marteau, P, Gerhardt, MF, Myara, A, Bouvier, E, Trivin, F & Rambaud, JC (1995) Metabolism of bile salts by alimentary bacteria during transit in the human small intestine. Microbial Ecology in Health and Disease 8, 151–157.CrossRefGoogle Scholar
Marteau, P & Rambaud, JC (1993) Potential of using lactic acid bacteria for therapy and immunomodulation in man. FEMS Microbiology Reviews 12, 207–220.CrossRefGoogle ScholarPubMed
Mashige, F, Tanaka, N, Maki, A, Kamei, S & Yamanaka, M (1981) Direct spectrophotometry of total bile acid in serum. Clinical Chemistry 27, 1352–1356.CrossRefGoogle ScholarPubMed
Miller, ER & Ullrey, DE (1987) The pig as a model for human nutrition. Annual Review of Nutrition 7, 361–365.CrossRefGoogle Scholar
Mott, GE, Moore, RW, Redmond, HE & Reiser, R (1973) Lowering of serum cholesterol by intestinal bacteria in cholesterol-fed piglets. Lipids 8, 428–431.CrossRefGoogle ScholarPubMed
Nagengast, FM, Grobben, MJ & van Munster, IP (1995) Role of bile acids in colorectal carcinogenesis. European Journal of Cancer 31, 1067–1070.CrossRefGoogle Scholar
Owen, RW, Henly, PJ, Thompson, MH & Hill, MJ (1986) Steroids and cancer: faecal bile acid screening for early detection of cancer risk. Journal of Steroid Biochemistry 24, 391–394.CrossRefGoogle ScholarPubMed
Ratcliffe, HL & Luginbühl, H (1971) The domestic pig: a model for experimental atherosclerosis. Atherosclerosis 13, 133–136.CrossRefGoogle Scholar
Scholz, K-E, Kinder, E, Hagemeister, H & Barth, CA (1985) Influence of dietary casein and soy protein isolate on intestinal cholesterol and bile acid concentration. Zeitschrift für Ernäh-rungswissenschaft 24, 158–171.CrossRefGoogle ScholarPubMed
Suckling, KE, Benson, GM, Bond, B, Gee, A, Glen, A, Haynes, C & Jackson, B (1991) Cholesterol lowering and bile acid excretion in the hamster with cholestyramine treatment. Atherosclerosis 89, 183–190.CrossRefGoogle ScholarPubMed
Tannock, GW & McConnell, MA (1994) Lactobacilli inhabiting the digestive tract of mice do not influence serum cholesterol concentrations. Microbial Ecology in Health and Disease 7, 331–334.CrossRefGoogle Scholar
Tannock, GW, Tangerman, A, Van Schaik, A & McConnell, A (1994) Deconjugation of bile acids by lactobacilli in the mouse small bowel. Applied and Environmental Microbiology 60, 3419–3420.CrossRefGoogle ScholarPubMed
Taylor, EW & Burman, NP (1964) The application of membrane filtration techniques to the bacteriological examination of water. Journal of Applied Bacteriology 27, 297–303.CrossRefGoogle Scholar
van Faassen, A, Bol, J, van Dokkum, W, Pikaar, NA, Ockhuizen, T & Hermus, RJJ (1987) Bile acids, neutral steroids and bacteria in faeces as affected by a mixed, a lacto-ovovegetarian and a vegan diet. American Journal of Clinical Nutrition 46, 962–967.CrossRefGoogle ScholarPubMed
Warnick, GR, Benderson, J & Albers, JJ (1982) Dextran sulfate-Mg2+ precipitation procedure for quantification of high-density-lipo-protein cholesterol. Clinical Chemistry 28, 1379–1388.CrossRefGoogle Scholar
Wolf, BW, Garleb, KA, Ataya, DG & Casas, IA (1995) Safety and tolerance of Lactobacillus reuteri in healthy adult male subjects. Microbial Ecology in Health and Disease 8, 41–50.CrossRefGoogle Scholar