Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases

Manoj Kumar, Ravinder Nagpal, Rajesh Kumar, R Hemalatha, Vinod Verma, Ashok Kumar, Chaitali Chakraborty, Birbal Singh, Francesco Marotta, Shalini Jain, Hariom Yadav, Manoj Kumar, Ravinder Nagpal, Rajesh Kumar, R Hemalatha, Vinod Verma, Ashok Kumar, Chaitali Chakraborty, Birbal Singh, Francesco Marotta, Shalini Jain, Hariom Yadav

Abstract

Cardiovascular diseases are one of the major causes of deaths in adults in the western world. Elevated levels of certain blood lipids have been reported to be the principal cause of cardiovascular disease and other disabilities in developed countries. Several animal and clinical trials have shown a positive association between cholesterol levels and the risks of coronary heart disease. Current dietary strategies for the prevention of cardiovascular disease advocate adherence to low-fat/low-saturated-fat diets. Although there is no doubt that, in experimental conditions, low-fat diets offer an effective means of reducing blood cholesterol concentrations on a population basis, these appear to be less effective, largely due to poor compliance, attributed to low palatability and acceptability of these diets to the consumers. Due to the low consumer compliance, attempts have been made to identify other dietary components that can reduce blood cholesterol levels. Supplementation of diet with fermented dairy products or lactic acid bacteria containing dairy products has shown the potential to reduce serum cholesterol levels. Various approaches have been used to alleviate this issue, including the use of probiotics, especially Bifidobacterium spp. and Lactobacillus spp.. Probiotics, the living microorganisms that confer health benefits on the host when administered in adequate amounts, have received much attention on their proclaimed health benefits which include improvement in lactose intolerance, increase in natural resistance to infectious disease in gastrointestinal tract, suppression of cancer, antidiabetic, reduction in serum cholesterol level, and improved digestion. In addition, there are numerous reports on cholesterol removal ability of probiotics and their hypocholesterolemic effects. Several possible mechanisms for cholesterol removal by probiotics are assimilation of cholesterol by growing cells, binding of cholesterol to cellular surface, incorporation of cholesterol into the cellular membrane, deconjugation of bile via bile salt hydrolase, coprecipitation of cholesterol with deconjugated bile, binding action of bile by fibre, and production of short-chain fatty acids by oligosaccharides. The present paper reviews the mechanisms of action of anti-cholesterolemic potential of probiotic microorganisms and probiotic food products, with the aim of lowering the risks of cardiovascular and coronary heart diseases.

Figures

Figure 1
Figure 1
Cholesterol as the precursor for the synthesis of new bile acids and the hypocholesterolemic role of bile salt hydrolase (BSH).
Figure 2
Figure 2
Role of probiotics' metabolites as epigenetic approach to control high cholesterol and colon cancer.

References

    1. Aloğlu H, Öner Z. Assimilation of cholesterol in broth, cream, and butter by probiotic bacteria. European Journal of Lipid Science and Technology. 2006;108(9):709–713.
    1. WHO. Cardiovascular Disease. Fact sheet no. 317, WHO, Geneva, Switzerland, 2009, .
    1. Yusuf PS, Hawken S, Ôunpuu S, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet. 2004;364(9438):937–952.
    1. WHO. Report of a Joint WHO/FAO Expert Consultation. Geneva, Switzerland: 2003. Diet, Nutrition and Prevention of Chronic Diseases.
    1. Dunn-Emke S, Weidner G, Ornish D. Benefits of a low-fat plant-based diet. Obesity Research. 2001;9(11):p. 731.
    1. Bliznakov EG. Lipid-lowering drugs (statins), cholesterol, and coenzyme Q10. The Baycol case—a modern Pandora’s box. Biomedicine and Pharmacotherapy. 2002;56(1):56–59.
    1. De Smet I, De Boever P, Verstraete W. Cholesterol lowering in pigs through enhanced bacterial bile salt hydrolase activity. British Journal of Nutrition. 1998;79(2):185–194.
    1. De Smet I, Van Hoorde L, Vande Woestyne M, Christiaens H, Verstraete W. Significance of bile salt hydrolytic activities of lactobacilli. Journal of Applied Bacteriology. 1995;79(3):292–301.
    1. Sanders TAB. Food production and food safety. British Medical Journal. 1999;318(7199):1689–1693.
    1. Nagpal R, Yadav H, Puniya AK, Singh K, Jain S, Marotta F. Potential of probiotics and prebiotics for synbiotic functional dairy foods. International Journal of Probiotics and Prebiotics. 2007;2:75–84.
    1. Kumar M, Behare PV, Mohania D, Arora S, Kaur A, Nagpal R. Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. European Journal of Clinical Nutrition. 2008;62(5):584–593.
    1. Bengmark S, Ahrne S, Molin G, Jeppsson B. Intestinal colonizing lactobacilli. Journal of Nutrition. 1998;14(8):585–594.
    1. Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. American Journal of Physiology. 1999;276(4):G941–G950.
    1. Yadav H, Jain S, Sinha PR. Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition. 2007;23(1):62–68.
    1. Yadav H, Jain S, Sinha PR. Formation of oligosaccharides in skim milk fermented with mixed dahi cultures, Lactococcus lactis ssp diacetylactis and probiotic strains of lactobacilli. Journal of Dairy Research. 2007;74(2):154–159.
    1. Kumar M, Mohania D, Poddar D, et al. A probiotic fermented milk prepared by mixed culture reduces pathogen shedding and alleviates disease signs in rats challenged with pathogens. International Journal of Probiotics and Prebiotics. 2009;4(3):211–217.
    1. Kumar M, Kumar A, Nagpal R, et al. Cancer-preventing attributes of probiotics: An update. International Journal of Food Sciences and Nutrition. 2010;61(5):473–496.
    1. Kumar M, Verma V, Nagpal R, et al. Anticarcinogenic effect of probiotic fermented milk and Chlorophyllin on aflatoxin-B1 induced liver carcinogenesis in rats. British Journal of Nutrition. 2012;107:1006–1016.
    1. Kumar M, Verma V, Nagpal R, et al. Effect of probiotic fermented milk and chlorophyllin on gene expressions and genotoxicity during AFB1-induced hepatocellular carcinoma. Gene. 2011;490(1-2):54–59.
    1. Niedzielin K, Kordecki H, Birkenfeld B. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. European Journal of Gastroenterology and Hepatology. 2001;13(10):1143–1147.
    1. Sanders TAB. Food production and food safety. British Medical Journal. 1999;318(7199):1689–1693.
    1. Nagpal R, Behare PV, Kumar M, et al. Milk, milk products and disease free health: an updated overview. Critical Reviews in Food Science and Nutrition. 2011;52(4):1549–7852.
    1. Pereira DIA, Gibson GR. Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Critical Reviews in Biochemistry and Molecular Biology. 2002;37(4):259–281.
    1. Klaver FAM, Van der Meer R. The assumed assimilation of cholesterol by lactobacilli and Bifidobacterium bifidum is due to their bile salt-deconjugating activity. Applied and Environmental Microbiology. 1993;59(4):1120–1124.
    1. Tahri K, Grill JP, Schneider F. Bifidobacteria strain behavior toward cholesterol: Coprecipitation with bile salts and assimilation. Current Microbiology. 1996;33(3):187–193.
    1. Tahri K, Grill JP, Schneider F. Involvement of trihydroxyconjugated bile salts in cholesterol assimilation by bifidobacteria. Current Microbiology. 1997;34(2):79–84.
    1. Usman HA. Bile tolerance, taurocholate deconjugation, and binding of cholesterol by Lactobacillus gasseri strains. Journal of Dairy Science. 1999;82(2):243–248.
    1. De Smet I, van Hoorde L, De Saeyer N, Vande Woestyne M, Verstraete W. 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. 1994;7(6):315–329.
    1. De Rodas BZ, Gilliland SE, Maxwell CV. Hypocholesterolemic action of Lactobacillus acidophilus ATCC 43121 and calcium in swine with hypercholesterolemia induced by diet. Journal of Dairy Science. 1996;79(12):2121–2128.
    1. Reynier MO, Montet JC, Gerolami A. Comparative effects of cholic, chenodeoxycholic, and ursodeoxycholic acids on micellar solubilization and intestinal absorption of cholesterol. Journal of Lipid Research. 1981;22(3):467–473.
    1. Gilliland SE, Nelson CR, Maxwell C. Assimilation of cholesterol by Lactobacillus acidophilus . Applied and Environmental Microbiology. 1985;49(2):377–381.
    1. Du Toit M, Franz CMAP, Dicks LMT, et al. Characterisation and selection of probiotic lactobacilli for a preliminary minipig feeding trial and their effect on serum cholesterol levels, faeces pH and faeces moisture content. International Journal of Food Microbiology. 1998;40(1-2):93–104.
    1. Walker DK, Gilliland SE. Relationship among bile tolerance, bile salt deconjugation, and assimilation of cholesterol by Lactobacillus acidophilus . Journal of Dairy Science. 1993;76(4):956–961.
    1. Rojas M, Ascencio F, Conway PL. Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Applied and Environmental Microbiology. 2002;68(5):2330–2336.
    1. Reid G, Bruce AW, Fraser N, Heinemann C, Owen J, Henning B. Oral probiotics can resolve urogenital infections. FEMS Immunology and Medical Microbiology. 2001;30(1):49–52.
    1. Gusils C, González SN, Oliver G. Some probiotic properties of chicken lactobacilli. Canadian Journal of Microbiology. 1999;45(12):981–987.
    1. Heinemann C, van Hylckama Vlieg JET, Janssen DB, Busscher HJ, van der Mei HC, Reid G. Purification and characterization of a surface-binding protein from Lactobacillus fermentum RC-14 that inhibits adhesion of Enterococcus faecalis 1131. FEMS Microbiology Letters. 2000;190(1):177–180.
    1. Tanaka H, Doesburg K, Iwasaki T, Mierau I. Screening of lactic acid bacteria for bile salt hydrolase activity. Journal of Dairy Science. 1999;82(12):2530–2535.
    1. Tanaka H, Hashiba H, Kok J, Mierau I. Bile salt hydrolase of Bifidobacterium longum—biochemical and genetic characterization. Applied and Environmental Microbiology. 2000;66(6):2502–2512.
    1. Grill JP, Cayuela C, Antoine JM, Schneider F. Isolation and characterization of a Lactobacillus amylovorus mutant depleted in conjugated bile salt hydrolase activity: relation between activity and bile salt resistance. Journal of Applied Microbiology. 2000;89(4):553–563.
    1. Wood BJB, Holzapfel WH. The Genera of Lactic Acid Bacteria. London, UK: Blackie Academy; 1995.
    1. Corzo G, Gilliland SE. Bile salt hydrolase activity of three strains of Lactobacillus acidophilus . Journal of Dairy Science. 1999;82(3):472–480.
    1. Corzo G, Gilliland SE. Measurement of bile salt hydrolase activity from Lactobacillus acidophilus based on disappearance of conjugated bile salts. Journal of Dairy Science. 1999;82(3):466–471.
    1. Moser SA, Savage DC. Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in lactobacilli. Applied and Environmental Microbiology. 2001;67(8):3476–3480.
    1. Mann GV, Spoerry A. Studies of a surfactant and cholesteremia in the Maasai. American Journal of Clinical Nutrition. 1974;27(5):464–469.
    1. Mann GV. A factor in yoghurt which lowers cholesterolemia in man. Arthrosclerosis. 1977;26:335–340.
    1. Lin MY, Chen TW. Reduction of Cholesterol by Lactobacillus acidophilus in Culture Broth. Journal of Food and Drug Analysis. 2000;8(2):97–102.
    1. Grunewald KK. Serum cholesterol levels in rats fed skim milk fermented by Lactobacillus acidophilus. Journal of Food Science. 1982;47:2078–2079.
    1. Taranto MP, Medici M, Perdigon G, Ruiz Holgado AP, Valdez GF. Evidence for hypocholesterolemic effect of Lactobacillus reuteri in hypercholesterolemic mice. Journal of Dairy Science. 1998;81(9):2336–2340.
    1. Xiao JZ, Kondo S, Takahashi N, et al. Effects of milk products fermented by Bifidobacterium longum on blood lipids in rats and healthy adult male volunteers. Journal of Dairy Science. 2003;86(7):2452–2461.
    1. Abd El-Gawad IA, El-Sayed EM, Hafez SA, El-Zeini HM, Saleh FA. The hypocholesterolaemic effect of milk yoghurt and soy-yoghurt containing bifidobacteria in rats fed on a cholesterol-enriched diet. International Dairy Journal. 2005;15(1):37–44.
    1. Kumar R, Grover S, Batish VK. Hypocholesterolaemic effect of dietary inclusion of two putative probiotic bile salt hydrolase-producing Lactobacillus plantarum strains in Sprague-Dawley rats. British Journal of Nutrition. 2010:1–12.
    1. Lin SY, Ayres JW, Winkler W, Sandine WE. Lactobacillus effects on cholesterol: in vitro and in vivo results. Journal of Dairy Science. 1989;72(11):2885–2899.
    1. Mohan JC, Arora R, Khalilullah M. Preliminary observations on effect of Lactobacillus sporogenes on serum lipid levels in hypercholesterolemic patients. Indian Journal of Medical Research Section B. 1990;92:431–432.
    1. Gilliland FD, Mahler R, Hunt WC, Davis SM. Preventive health care among rural American Indians in New Mexico. Preventive Medicine. 1999;28(2):194–202.
    1. Klein A, Friedrich U, Vogelsang H, Jahreis G. Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. European Journal of Clinical Nutrition. 2008;62(5):584–593.
    1. Jones ML, Martoni CJ, Parent M, Prakash S. Cholesterol-lowering efficacy of a microencapsulated bile salt hydrolase-active Lactobacillus reuteri NCIMB 30242 yoghurt formulation in hypercholesterolaemic adults. British Journal of Nutrition. 2011;9:1–9.
    1. Carey MC, Duane WC. Enterohepatic circulation. In: Arias IM, Boyer N, Fausto N, Jackoby WB, Schachter DA, Shafritz DA, editors. The Liver: Biology and Pathobiology. New York, NY, USA: Raven Press, Ltd.; 1994. pp. 719–738.
    1. Hofmann AF. Bile acids. In: Arias IM, Boyer JL, Fausto N, Jackoby WB, Schachter DA, Shafritz DA, editors. The Liver: Biology and Pathobiology. New York, NY, USA: Raven Press; 1994. pp. 677–718.
    1. Begley M, Gahan CGM, Hill C. The interaction between bacteria and bile. FEMS Microbiology Reviews. 2005;29(4):625–651.
    1. Begley M, Sleator RD, Gahan CGM, Hill C. Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes . Infection and Immunity. 2005;73(2):894–904.
    1. Vlahcevic ZR, Heuman DM, Hylemon PB. Physiology and pathophysiology of enterohepatic circulation of bile acids. In: Zakim D, Boyer T, editors. Hepatology: A Textbook of Liver Disease. 3rd edition. Philadelphia, Pa, USA: Saunders; 1996. pp. 376–417.
    1. Bortolini O, Medici A, Poli S. Biotransformations on steroid nucleus of bile acids. Steroids. 1997;62(8-9):564–577.
    1. Batta AK, Salen G, Arora R, Shefer S, Batta M, Person A. Side chain conjugation prevents bacterial 7-dehydroxylation of bile acids. Journal of Biological Chemistry. 1990;265(19):10925–10928.
    1. Elkins CA, Moser SA, Savage DC. Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonii 100-100 and other Lactobacillus species. Microbiology. 2001;147(12):3403–3412.
    1. Franz CMAP, Specht I, Haberer P, Holzapfel WH. Bile salt hydrolase activity of enterococci isolated from food: screening and quantitative determination. Journal of Food Protection. 2001;64(5):725–729.
    1. Edgell DR, Belfort M, Shub DA. Barriers to intron promiscuity in bacteria. Journal of Bacteriology. 2000;182(19):5281–5289.
    1. McAuliffe O, Cano RJ, Klaenhammer TR. Genetic analysis of two bile salt hydrolase activities in Lactobacillus acidophilus NCFM. Applied and Environmental Microbiology. 2005;71(8):4925–4929.
    1. Huijghebaert SM, Mertens JA, Eyssen HJ. Isolation of a bile salt sulfatase producing Clostridium strain from rat intestinal microflora. Applied and Environmental Microbiology. 1982;43(1):185–192.
    1. Van Eldere J, Celis P, De Pauw G, Lesaffre E, Eyssen H. Tauroconjugation of cholic acid stimulates 7α-dehydroxylation by fecal bacteria. Applied and Environmental Microbiology. 1996;62(2):656–661.
    1. Tannock GW, Dashkevicz MP, Feighner SD. Lactobacilli and bile salt hydrolase in the murine intestinal tract. Applied and Environmental Microbiology. 1989;55(7):1848–1851.
    1. Gilliland SE, Speck ML. Deconjugation of bile acids by intestinal lactobacilli. Applied and Environmental Microbiology. 1977;33(1):15–18.
    1. Dambekodi PC, Gilliland SE. Incorporation of cholesterol into the cellular membrane of Bifidobacterium longum . Journal of Dairy Science. 1998;81(7):1818–1824.
    1. Taranto MP, Sesma F, Pesce De Ruiz Holgado A, De Valdez GF. Bile salts hydrolase plays a key role on cholesterol removal by Lactobacillus reuteri . Biotechnology Letters. 1997;19(9):845–847.
    1. Taranto MP, Fernandez Murga ML, Lorca G, De Valdez GF. Bile salts and cholesterol induce changes in the lipid cell membrane of Lactobacillus reuteri . Journal of Applied Microbiology. 2003;95(1):86–91.
    1. Boggs JM. Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function. Biochimica et Biophysica Acta. 1987;906(3):353–404.
    1. De Smet I, Van Hoorde L, Vande Woestyne M, Christiaens H, Verstraete W. Significance of bile salt hydrolytic activities of lactobacilli. Journal of Applied Bacteriology. 1995;79(3):292–301.
    1. Coleman JP, Hudson LL. Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens. Applied and Environmental Microbiology. 1995;61(7):2514–2520.
    1. Kim G-B, Miyamoto CM, Meighen EA, Lee BH. Cloning and characterization of the bile salt hydrolase genes (bsh) from Bifidobacterium bifidum strains. Applied and Environmental Microbiology. 2004;70(9):5603–5612.
    1. Liong MT, Shah NP. Bile salt deconjugation ability, bile salt hydrolase activity and cholesterol co-precipitation ability of lactobacilli strains. International Dairy Journal. 2005;15(4):391–398.
    1. Bateup JM, McConnell MA, Jenkinson HF, Tannock GW. Comparison of Lactobacillus strains with respect to bile salt hydrolase activity, colonization of the gastrointestinal tract, and growth rate of the murine host. Applied and Environmental Microbiology. 1995;61(3):1147–1149.
    1. Dussurget O, Cabanes D, Dehoux P, et al. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Molecular Microbiology. 2002;45(4):1095–1106.
    1. Schuster H. Improving lipid management - To titrate, combine or switch. International Journal of Clinical Practice. 2004;58(7):689–694.
    1. Taranto MP, Medici M, Perdigon G, Ruiz Holgado AP, Font de Valdez G. Effect of Lactobacillus reuteri on the prevention of hypercholesterolemia in mice. Journal of Dairy Science. 2000;83(3):401–403.
    1. Feighner SD, Dashkevicz MP. Effect of dietary carbohydrates on bacterial cholyltaurine hydrolase in poultry intestinal homogenates. Applied and Environmental Microbiology. 1988;54(2):337–342.
    1. St-Onge MP, Farnworth ER, Jones PJH. Consumption of fermented and nonfermented dairy products: Effects on cholesterol concentrations and metabolism. American Journal of Clinical Nutrition. 2000;71(3):674–681.
    1. Anderson JW, Gilliland SE. Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. Journal of the American College of Nutrition. 1999;18(1):43–50.
    1. Kaplan LA, Pesse AJ. Clinical Chemistry, Theory, Analysis, and Correlation. 3rd edition. St. Louis, Mo, USA: Mosby Company; 1996.
    1. Dessi S, Batetta B. Overview—intracellular cholesterol homeostasis: old and new players. In: Pani A, Dessi S, editors. Cell Growth and Cholesterol Esters. New York, NY, USA: Kluwer Academic/Plenum Publishers; 2003. pp. 1–12.
    1. Croft JB, Cresanta JL, Webber LS, et al. Cardiovascular risk in parents of children with extreme lipoprotein cholesterol levels: the Bogalusa Heart Study. Southern Medical Journal. 1988;81(3):341–349.
    1. Jialal I. Evolving lipoprotein risk factors: Lipoprotein(a) and oxidized low-density lipoprotein. Clinical Chemistry. 1998;44(8):1827–1832.
    1. Höckerstedt A, Jauhiainen M, Tikkanen MJ. Lecithin/cholesterol acyltransferase induces estradiol esterification in high-density lipoprotein, increasing its antioxidant potential. Journal of Clinical Endocrinology and Metabolism. 2004;89(10):5088–5093.
    1. Nissen SE, Tsunoda T, Tuzcu EM, et al. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. Journal of the American Medical Association. 2003;290(17):2292–2300.
    1. Walldus G, Jungner I, Aastveit AH, Holme I, Furberg CD, Sniderman AD. The apoB/apoA-I ratio is better than the cholesterol ratios to estimate the balance between plasma proatherogenic and antiatherogenic lipoproteins and to predict coronary risk. Clinical Chemistry and Laboratory Medicine. 2004;42(12):1355–1363.
    1. De Preter V, Coopmans T, Rutgeerts P, Verbeke K. Influence of long-term administration of lactulose and Saccharomyces boulardii on the colonic generation of phenolic compounds in healthy human subjects. Journal of the American College of Nutrition. 2006;25(6):541–549.
    1. Xiong Y, Miyamoto N, Shibata K, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(4):1045–1050.
    1. De Boever P, Verstraete W. Bile salt deconjugation by Lactobacillus plantarum 80 and its implication for bacterial toxicity. Journal of Applied Microbiology. 1999;87(3):345–352.
    1. Doncheva NI, Antov GP, Softova EB, Nyagolov YP. Experimental and clinical study on the hypolipidemic and antisclerotic effect of Lactobacillus bulgaricus strain GB N 1 (48) Nutrition Research. 2002;22(4):393–403.
    1. Ahn YT, Kim GB, Lim KS, Baek YJ, Kim HU. Deconjugation of bile salts by Lactobacillus acidophilus isolates. International Dairy Journal. 2003;13(4):303–311.
    1. Noh DO, Gilliland SE. Influence of bile on cellular integrity and beta-galactosidase activity of Lactobacillus acidophilus . Journal of Dairy Science. 1993;76(5):1253–1259.
    1. Begley M, Hill C, Gahan CGM. Bile salt hydrolase activity in probiotics. Applied and Environmental Microbiology. 2006;72(3):1729–1738.
    1. Jones ML, Chen H, Ouyang W, Metz T, Prakash S. Microencapsulated genetically engineered Lactobacillus plantarum 80 (pCBH1) for bile acid deconjugation and its implication in lowering cholesterol. Journal of Biomedicine and Biotechnology. 2004;2004(1):61–69.
    1. Kimoto H, Ohmomo S, Okamoto T. Cholesterol removal from media by lactococci. Journal of Dairy Science. 2002;85(12):3182–3188.
    1. Lye HS, Rahmat-Ali GR, Liong MT. Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. International Dairy Journal. 2010;20(3):169–175.
    1. Lye HS, Rusul G, Liong MT. Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. Journal of Dairy Science. 2010;93(4):1383–1392.
    1. Chiang YR, Ismail W, Heintz D, Schaeffer C, Van Dorsselaer A, Fuchs G. Study of anoxic and oxic cholesterol metabolism by Sterolibacterium denitrificans . Journal of Bacteriology. 2008;190(3):905–914.
    1. Liong MT, Dunshea FR, Shah NP. Effects of a synbiotic containing Lactobacillus acidophilus ATCC 4962 on plasma lipid profiles and morphology of erythrocytes in hypercholesterolaemic pigs on high- and low-fat diets. British Journal of Nutrition. 2007;98(4):736–744.
    1. Arjmandi BH, Craig J, Nathani S, Reeves RD. Soluble dietary fiber and cholesterol influence in vivo hepatic and intestinal cholesterol biosynthesis in rats. Journal of Nutrition. 1992;122(7):1559–1565.
    1. Kim M, Shin HK. The water-soluble extract of chicory influences serum and liver lipid concentrations, cecal short-chain fatty acid concentrations and fecal lipid excretion in rats. Journal of Nutrition. 1998;128(10):1731–1736.
    1. Dikeman CL, Murphy MR, Fahey GC. Dietary fibers affect viscosity of solutions and simulated human gastric and small intestinal digesta. Journal of Nutrition. 2006;136(4):913–919.

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