The perspective on cholesterol-lowering mechanisms of probiotics

Molecular Nutrition and Food Research

Volumn 59, Issue 1, 2015, Pages 94-105

  Ishimwe, Nestor ^a,b   Daliri, Eric B ^a   Lee, Byong H ^a,c   Fang, Fang ^a   Du, Guocheng ^a  

^a JIANGNAN UNIVERSITY   (China)

^b UNIVERSITY OF RWANDA   (Rwanda)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Cardiovasculardiseases; Hypocholesterolemiceffect; Prebiotics; Probiotics; Sepsis

Indexed keywords

ANIMALIA;

BILE ACID; CHOLESTEROL; PROBIOTIC AGENT; SYNBIOTIC AGENT;

ANIMAL; BLOOD; HUMAN; METABOLISM; PRODUCT SAFETY; RANDOMIZED CONTROLLED TRIAL (TOPIC);

ANIMALS; BILE ACIDS AND SALTS; CHOLESTEROL; CONSUMER PRODUCT SAFETY; HUMANS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SYNBIOTICS;

EID: 84921032830     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400548     Document Type: Review

References (116)

1. Upadhyay, N., Moudgal, V., Probiotics: a review. J. Clin. Outcomes Manage. 2012, 19, 76-84.
2. CDC. Vital signs: prevalence, treatment, and control of high levels of low-density lipoprotein cholesterol. United States, 1999-2002 and 2005-2008. MMWR Morb. Mortal. Wkly. Rep. 2011, 60, 109-114.
3. Wassel, J. J., Prebiotics, probiotics and synbiotics: functional foods. 2006, 1-6. Available from: http://static.abbottnutrition.com/cms-prod/anhi.org/img/Prebiotics_Probiotics_Synbiotics_Functional_Foods.pdf.
4. Hsu, K. C., Liao, W. J., Chung, C. Y., Hsieh, P. C. et al., Xylo-oligosaccharides and fructo-oligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J. Nutr. 2004, 134, 1523-1528.
5. Li, J. X., Piao, S. X., Kim, W. S., Liu, P. et al., Effects of chito-oligosaccharide supplementation on performance, nutrient digestibility, and serum composition in broiler chickens. Poultry Sci. 2007, 86, 1107-1114.
6. Chen, H., Liu, J. L., Zhu, J. J., Xu, B. et al., Effect of soybean oligosaccharides on blood lipid, glucose levels and antioxidant enzymes activity in high fat rats. Food Chem. 2010, 119, 1633-1636.
7. Panesar, P. S., Kumari, S., Panesar, R., Biotechnological approaches for the production of prebiotics and their potential applications. Crit. Rev. Biotechnol. 2013, 33, 345-364.
8. Ooi, L. G., Liong, M. T., Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int. J. Mol. Sci. 2010, 11, 2499-2522.
9. Duggan, C., Gannon, J., Walker, W. A., Protective nutrients and functional foods for the gastrointestinal tract. Am. J. Clin. Nutr. 2002, 75, 789-808.
10. de Roos, N. M., Katan, M. B., Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: a review of papers published between 1988 and 1998. Am. J. Clin. Nutr. 2000, 71, 405-411.
11. DiRienzo, D. B., Effect of probiotics on biomarkers of cardiovascular disease: implications for heart-healthy diets. Nutr. Rev. 2014, 72, 18-29.
12. Martín, R., Miquel, S., Ulmer, J., Kechaou, N. et al., Role of commensal and probiotic bacteria inhuman health: a focus on inflammatory bowel disease. Microb. Cell Fact. 2013, 12, 71.
13. Whelan, K., Myers, C. E., Safety of probiotics in patients receiving nutritional support: a systematic review of case reports, randomized controlled trials, and nonrandomized trials. Am. J. Clin. Nutr. 2010, 91, 687-703.
14. Rajkumar, H., Mahmood, N., Kumar, M., Varikuti, S. R. et al., Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized, controlled trial. Mediators Inflamm. 2014, 2014, 348959.
15. Lewis, S. J., Burmeister, S., A double-blind placebo-controlled study of the effects of Lactobacillus acidophilus on plasma lipids. Eur. J. Clin. Nutr. 2005, 59, 776-780.
16. Greany, K. A., Bonorden, M. J., Hamilton-Reeves, J. M., McMullen, M. et al., Probiotic capsules do not lower plasma lipids in young women and men. Eur. J. Clin. Nutr. 2008, 62, 232-237.
17. Anderson, J. W., Gilliland, S. E., Effect of fermented milk yogurt containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J. Am. Coll. Nutr. 1999, 18, 43-50.
18. Ooi, L. G., Ahmad, R., Yuen, K. H., Liong, M. T., Lactobacillus gasseri [corrected] CHO-220 and inulin reduced plasma total cholesterol and low-density lipoprotein cholesterol via alteration of lipid transporters. J. Dairy Sci. 2010, 93, 5048-5058.
19. Sadrzadeh-Yeganeh, H., Elmadfa, I., Djazayery, A., Mahmoud, J. et al., The effects of probiotic and conventional yoghurt on lipid profile in women. Br. J. Nutr. 2010, 103, 1778-1783.
20. Asemi, Z., Samimi, M., Tabasi, Z., Talebian, P. et al., Effect of daily consumption of probiotic yoghurt on lipid profiles in pregnant women: a randomized controlled clinical trial. J. Matern. Fetal. Neonatal Med. 2012, 25, 1552-1556.
21. Lin, S. Y., Ayres, J. W., Winkler, W. J., Sandine, E. W., Lactobacillus effects on cholesterol: in vitro and in vivo results. J. Dairy Sci. 1989, 72, 2885-2899.
22. Kiessling, G., Schneider, J., Jahreis, G., Long-term consumption of fermented dairy products over 6 months increases HDL cholesterol. Eur. J. Clin. Nutr. 2002, 56, 843-849.
23. Agerholm-Larsen, L., Raben, A., Haulrik, N., Hansen, A. S. et al., Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur. J. Clin. Nutr. 2000, 54, 288-297.
24. Jones, M. L., Martoni, C. J., Prakash, S., Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. Eur. J. Clin. Nutr. 2012, 66, 1234-1241.
25. Usinger, L., Reimer, C., Ibsen, H., Fermented milk for hypertension. Cochrane Database Syst. Rev. 2012, 18, 52.
26. Kawase, M., Hashimoto, H., Hosoda, M., Morita, H. et al., Effect of administration of fermented milk containing whey protein concentrate to rats and healthy men on serum lipids and blood pressure. J. Dairy Sci. 2000, 83, 255-263.
27. Madani, G., Mirlohi, M., Hassanzadeh, A., How much in vitro cholesterol reducing activity of lactobacilli predicts their in vivo cholesterol function? Int. J. Prev. Med. 2013, 4, 404-413.
28. Bukowska, H., Pieczul-Mróz J., Jastrzębska, M., Chelstowski, K. et al., Decrease in fibrinogen and LDL-cholesterol levels upon supplementation of diet with Lactobacillus plantarum in subjects with moderately elevated cholesterol. Atherosclerosis 1998, 137, 437-438.
29. Wang, Y., Xu, N., Xi, A., Ahmed, Z. et al., Effects of Lactobacillus plantarum MA2 isolated from Tibet kefir on lipid metabolism and intestinal microflora of rats fed on high-cholesterol diet. Appl. Microbiol. Biotechnol. 2009, 84, 341-347.
30. Shin, H. S., Shin, Y. P., Lee, D. K., Kim, S. A. et al., Hypocholesterolemic effect of sonication-killed Bifidobacterium longum isolated from healthy adult Koreans in high cholesterol fed rats. Arch. Pharm. Res. 2010, 33, 1425-1431.
31. McNaught, E. C., Woodcock, P. N., Anderson, D. G. A., MacFie, J., A prospective randomised trial of probiotics in critically ill patients. Clin. Nutr. 2005, 24, 211-219.
32. Naruszewicz, M., Johansson, M. L., Zapolska- Downar, D., Bukowska, H., Effect of Lactobacillus plantarum 299v on cardiovascular disease risk factors in smokers. Am. J. Clin. Nutr. 2002, 76, 1249-1255.
33. Trautvetter, U., Ditscheid, B., Kiehntopf, M., Jahreis, G., A combination of calcium phosphate and probiotics beneficially influences intestinal lactobacilli and cholesterol metabolism in humans. Clin. Nutr. 2012, 31, 230-237.
34. Fabian, E., Elmadfa, I., Influence of daily consumption of probiotic and conventional yoghurt on the plasma lipid profile in young healthy women. Ann. Nutr. Metab. 2006, 50, 387-393.
35. Lee, H. Y., Park, J. H., Seok, S. H., Baek, M. W. et al., Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim. Biophys. Acta 2006, 1761, 736-744.
36. Hatakka, K., Mutanen, M., Holma, R., Saxelin, M. et al., Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp shermanii JS administered in capsules is ineffective in lowering serum lipids. J. Am. Coll. Nutr. 2008, 27, 441-447.
37. Rossi, E. A., Vendramini R. C., Carlos, I. Z., de Oliveira, M. G. et al., Effect of a new fermented soy milk product on serum lipid levels in normocholesterolemic adult men. Arch. Latinoam. Nutr. 2003, 53, 47-51.
38. Cheik, N. C., Rossi, E. A., Guerra, R. L., Tenorio, N. M. et al., Effects of a ferment soy product on the adipocyte area reduction and dyslipidemia control in hypercholesterolemic adult male rats. Lipids Health Dis. 2008, 7, 50.
39. Mohan, J. C., Preliminary observations on effect of Lactobacillus sporogenes on serum lipid levels in hypercholesterolemic patients. Indian J. Med. Res. 1990, 92, 431-432.
40. Simons, L. A., Amansec, S. G., Conway, P., Effect of Lactobacillus fermentum on serum lipids in subjects with elevated serum cholesterol. Nutr. Metab. Cardiovasc. Dis. 2006, 16, 531-535.
41. Songisepp, E., Kals, J., Kullisaar, T., Mandar, R. et al., Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr. J. 2005, 4, 22.
42. Pan, D. D., Zeng, X. Q., Yan, Y. T., Characterisation of Lactobacillus fermentum SM-7 isolated from koumiss, a potential probiotic bacterium with cholesterol-lowering effects. J. Sci. Food. Agric. 2011, 91, 512-518.
43. Usman, Hosono, A., Effect of administration of Lactobacillus gasseri on serum lipids and fecal steroids in hypercholesterolemic rats. J. Dairy Sci. 2000, 83, 1705-1711.
44. Guardamagna, O., Amaretti, A., Puddu, P. E., Raimondi, S. et al., Bifidobacteria supplementation: effects on plasma lipid profiles in dyslipidemic children. Nutrition 2014, 30, 831-836.
45. Xiao, J. Z., Kondo, S., Takahashi, N., Miyaji, K. et al., Effects of milk products fermented by Bifidobacterium longum on blood lipids in rats and healthy adult male volunteers. J. Dairy Sci. 2003, 86, 2452-2461.
46. Bordoni, A., Amaretti, A., Leonardi, A., Boschetti, E. et al., Cholesterol-lowering probiotics: in vitro selection and in vivo testing of Bifidobacteria. Appl. Microbiol. Biotechnol. 2013, 97, 8273-8281.
47. Cenesiz, S., Yaman, H., Ozcan, A., Kart, A. et al., Effects of kefir as a probiotic on serum cholesterol, total lipid, aspartate amino transferase and alanine amino transferase activities in broiler chicks. Med. Weter. 2008, 64, 168-170.
48. Hlivak, P., Odraska, J., Ferencik, M., Ebringer, L. et al., One-year application of probiotic strain Enterococcus faecium M-74 decreases serum cholesterol levels. Bratisl. Lek. Listy 2005, 106, 67-72.
49. Pato, U., Surono, S. I., Koesnandar, Hosono, A., Hypocholesterolemic effect of indigenous dadih lactic acid bacteria by deconjugation of bile salts. Asian-Australas. J. Anim. Sci. 2004, 17, 1741-1745.
50. Baek, Y. J., Lee, B. H., Probiotics and prebiotics as bioactive components in dairy products. in: Park, Y. W. (Ed.), Bioactive Components in Milk and Dairy Products, Wiley-Blackwell, New York 2009, p. 440.
51. Yusuf, P., Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004, 364, 937-952.
52. Heidenreich, P. A., Trogdon, J. G., Khavjou, O. A., Javed, B. et al., Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association. Circulation 2011, 123, 933-944.
53. Scarborough, P., Bhatnagar, P., Wickramasinghe, K., Smolina, K. et al., University of Oxford, Department of Public Health 2010. Available from: "http://www.stroke.org.uk/sites/default/files/R11%20Stroke%20statistics%20-%20large%20print.doc"
54. Leal, J., Luengo-Fernandez, R., Gray, A., European Heart Network, Brussels, European Society of Cardiology, Sophia Antipolis 2012. Available from: http://www.escardio.org/about/documents/eu-cardiovascular-disease-statistics-2012.pdf
55. Homayouni, A., Payahoo, L., Azizi, A., Effect of probiotics on lipids profile: a review. Am. J. Food technol. 2012, 7, 251-265.
56. Tanaka, H., Hashiba, H., Kok, J., Mierau, I., Bile salt hydrolase of Bifidobacterium longum-biochemical and genetic characterization. Appl. Environ. Microbiol. 2000, 66, 2502-2512.
57. Jolanda, L. M., Bongers, R. S., Vos, W. M. D., Kleerebezem, M., Functional analysis of four bile salt hydrolase and penicillin acylase family members in Lactobacillus plantarum WCFS1. Appl. Environ. Microbiol. 2008, 74, 4719-4726.
58. Ren, J., Sun, K., Wu, Z., Yao, J., Guo, B., All 4 bile salt hydrolase proteins are responsible for the hydrolysis activity in Lactobacillus plantarum ST-III. J. Food Sci. 2011, 76, M622-628.
59. Gu, X., Luo, X., Wang, C., Ma, D. et al., Cloning and analysis of bile salt hydrolase genes from Lactobacillus plantarum CGMCC No. 8198. Biotechnol. Lett. 2014, 36, 975-983.
60. Kim, G. B., Miyamoto, C. M., Meighen, E. A., Lee, B. H., Cloning and characterization of the bile salt hydrolase genes (bsh) from Bifidobacterium bifidum strains. Appl. Environ. Microbiol. 2004, 70, 5603-5612.
61. Chae, J. P., Valeriano, V. D., Kim, G. B., Kang, D. K., Molecular cloning, characterization and comparison of bile salt hydrolases from Lactobacillus johnsonii PF01. J. Appl. Microbiol. 2013, 114, 121-133.
62. Kim, G. B., Brochet, M., Lee, B. H., Cloning and characterization of a bile salt hydrolase (bsh) from Bifidobacterium adolescentis. Biotechnol. Lett. 2005, 27, 817-822.
63. Montalto, M., D'Onofrio, F., Gallo, A., Cazzato, A., Gasbarrini, G., Intestinal microbiota and its functions. Dig. Liver Dis. 2009, 3, 30-34.
64. Kim, G. B., Yi, S. H., Lee, B. H., Purification and characterization of three different types of bile salt hydrolases from Bifidobacterium strains. J. Dairy Sci. 2004, 87, 258-266.
65. Rossocha, M., Schultz-Heienbrok, R., Moeller, H. V., Coleman, J. P., Saenger, W., Conjugated bile acid hydrolase is a tetrameric N-terminal thiol hydrolase with specific recognition of its cholyl but not of its tauryl product. Biochemistry 2005, 44, 5739-5748.
66. Coleman, P. J., Hudson, L. L., Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens. Appl. Environ. Microbiol. 1995, 61, 2514-2520.
67. Elkins, C. A., Moser, S. A., Savage, D. C., Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonii 100-100 and other Lactobacillus species. Microbiology 2001, 147, 3403-3412.
68. Parvez, S., Malik, K. A., Ah Kang, S., Kim, H. Y., Probiotics and their fermented food products are beneficial for health. J. Appl. Microbiol. 2006, 100, 1171-1185.
69. Lee do, K., Jang, S., Baek, E., Kim, M.-J. et al., Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content. Lipids Health Dis. 2009, 8, 21.
70. Liong, T. M., Dunshea, R. F., Shah, P. N., 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. Br. J. Nutr. 2007, 98, 736-744.
71. Madsen, C. S., Janovitz, E., Zhang, R., Nguyen-Tran, V. et al., The Guinea pig as a preclinical model for demonstrating the efficacy and safety of statins. J. Pharmacol. Exp. Ther. 2008, 324, 576-586.
72. Sridevi, N., Vishwe, P., Prabhune, A., In vivo cholesterol reduction studies. Food Res. Intl 2009, 42, 516-520.
73. Patel, A. K., Singhania, R. R., Pandey, A., Chincholkar, S. B., Probiotic bile salt hydrolase: current developments and perspectives. Appl. Biochem. Biotechnol. 2010, 162, 166-180.
74. Guo, Z., Liu, X. M., Zhang, Q. X., Shen, Z. et al., Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomised controlled trials. Nutr. Metab. Cardiovasc. Dis. 2011, 21, 844-850.
75. Öner, O., Aslim, B., Aydas, S. B., Mechanisms of cholesterol-lowering effects of lactobacilli and bifidobacteria strains as potential probiotics with their bsh gene analysis. J. Mol. Microbiol. Biotechnol. 2014, 24, 12-18.
76. Branton, W. B., Jones, M. L., Tomaro-Duchesneau, C., Martoni, C. J., Prakash, S., In vitro characterization and safety of the probiotic strain lactobacillus reuteri cardioviva NCIMB 30242. Int. J. Probiotics Prebiotics 2010, 6, 1-12.
77. Jones, M. L., Martoni, C. J., Pietro, E. D., Simonc, R. R., Prakash, S., Evaluation of clinical safety and tolerance of a Lactobacillus reuteri NCIMB 30242 supplement capsule: a randomized control trial. Regul. Toxicol. Pharmacol. 2012, 63, 313-320.
78. Jones, M. L., Martoni, C. J., Ganopolsky, J. G., Sulemankhil, I. et al., Improvement of gastrointestinal health status in subjects consuming Lactobacillus reuteri NCIMB 30242 capsules: a post-hoc analysis of a randomized controlled trial. Exp. Opin. Biol. Ther. 2013, 13, 1643-1151.
79. Kumar, M., Nagpal, R., Kumar, R., Hemalatha, R. et al., Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp. Diabetes Res. 2012, 2012, 902-917.
80. Lye, H., Rahmat-Ali, G., Liong, M., Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. Int. Dairy J. 2010, 20, 169-175.
81. Lye, H., Rusul, G., Liong, M., Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. J. Dairy Sci. 2010, 93, 1383-1392.
82. Preter, V. D., Vanhoutte, T., Huys, G., Swings, J. et al., Effects of Lactobacillus casei Shirota, Bifidobacterium breve, and oligofructose-enriched inulin on colonic nitrogen-protein metabolism in healthy humans. Am. J. Physiol. 2007, 129, G358-G368.
83. Philippe, G., Metabolism of cholesterol and bile acids by the gut microbiota. Pathogens 2014, 3, 14-24.
84. McAuliffe, O., Cano, R., Klaenhammer, R., Genetic analysis of two bile salt hydrolase activities in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 2005, 71, 4925-4929.
85. Wang, X., Wang, J., Wu, F., Sui, Y. et al., Lactobacillus plantarum strains as potential probiotic cultures with cholesterol-lowering activity. J. Dairy Sci. 2013, 96, 2746-2753.
86. Bordoni, A., Amaretti, A., Leonardi, A., Boschetti, E. et al., Cholesterol-lowering probiotics: in vitro selection and in vivo testing of bifidobacteria. Appl. Microbiol. Biotechnol. 2013, 97, 8273-8281.
87. Kimoto, H., Ohmomo, S., Okamoto, T., Cholesterol removal from media by lactococci. J. Dairy Sci. 2002, 85, 3182-3188.
88. Rabot, S., Rafter, J., Rijkers, G. T., Watzl, B., Antoine, J. M., Guidance for substantiating the evidence for beneficial effects of probiotics: impact of probiotics on digestive system metabolism. J. Nutr. 2010, 140, 677S-689S.
89. Mahrous, H., Probiotics bacteria from Egyptian infants cause cholesterol removal in media and survive in yoghurt. Food. Nutri. Sci. 2011, 2, 150-155.
90. Korecka, A., deWouters, T., Cultrone, A., Lapaque, N. et al., ANGPTL4 expression induced by butyrate and rosiglitazone in human intestinal epithelial cells utilizes independent pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304, G1025-G1037.
91. Sheril, A., Lange, K., Amolo, T., Grinstead, J. et al., Short-chain fatty acids stimulate angiopoietin-like 4 synthesis in human colon adenocarcinoma cells by activating peroxisome proliferator-activated receptor γ. Mol. Cell. Biol. 2013, 33, 1303-1316.
92. Marcil, V., Delvin, E., Garofalo, C., Levy, E., Butyrate impairs lipid transport by inhibiting microsomal triglyceride transfer trotein in caco-2 cells. J. Nutr. 2003, 133, 2180-2183.
93. Jia, L., Betters, J. L., Yu, L., Niemann-Pick C1-like 1 (NPC1L1) protein in intestinal and hepatic cholesterol transport. Annu. Rev. Physiol. 2011, 73, 239-259.
94. Wang, Y., Rogers, P., Su, C., Varga, G. et al., Regulation of cholesterologenesis by the oxysterol receptor, LXRalpha. J. Biol. Chem. 2008, 283, 26332-26339.
95. Yoon, H., Ju, J., Lee, J., Park, H. et al., The probiotic Lactobacillus rhamnosus BFE5264 and Lactobacillus plantarumNR74 promoter cholesterol efflux and suppress inflammation in THP-1 cells. J. Sci. Food Agric. 2012, 93, 781-787.
96. Gorenjak, M., Gradišnik, L., Trapecar, M., Pistello, M. et al., Improvement of lipid profile by probiotic/protective cultures: study in a non-carcinogenic small intestinal cell model. New Microbiol. 2014, 37, 51-64.
97. Jones, M. L., Tomaro-Duchesneau, C., Prakash, S., The gut microbiome, probiotics, bile acids axis, and human health. Trends Microbiol. 2014, 22, 306-308.
98. Yamanashi, Y., Tappei, T., Jun-Ichi, S., Hiroshi, S., Novel function of Niemann-Pick C1-like 1 as a negative regulator of niemann-pick C2 protein. Hepatology 2012, 55, 953-964.
99. Huang, Y., Zheng, Y. C., The probiotic Lactobacillus acidophilus reduces cholesterol absorption through the down-regulation of NiemannPick C1like 1 in Caco2 cells Br. J. Nutr. 2010, 103, 473-478.
100. Zhao, C., DW, K., Liver X receptor in cholesterol metabolism. J. Endocrinol. 2010, 204, 233-240.
101. Lye, H. S., Rusul, G., Liong, M. T., Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. J. Dairy Sci. 2010, 93, 1383-1392.
102. Dewulf, E., Cani, P., Claus, S., Fuentes, S. et al., Insight into the prebiotic concept: lessons from an exploratory, double-blind intervention study with inulin-type fructans in obese women. Gut 2013, 62, 1112-1121.
103. van Baarlen, P., Troosta, F., van der, M., Hooivelda, G. et al., Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc. Natl. Acad. Sci. USA 2010, 108, 4562-4569.
104. Ajouz, H., Mukherji, D., Shamseddine, A., Secondary bile acids: an underrecognized cause of colon cancer. World J. Surg. Oncol. 2014, 12, 5.
105. Lebeer, S., Ingmar, C., Vanderleyden, J., Anti-inflammatory potential of probiotics: lipoteichoic acid makes a difference. Trends Microbiol. 2012, 20, 5-10.
106. Yu, L., Overexpression of abcg5 and abcg8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. J. Clin. Invest. 2002, 11, 671-680.
107. Hanson, M., Gluckman, P., Developmental origins of noncommunicable disease: population criteria for probiotic bacteria. Am. J. Clin. Nutr. 2011, 73, 393-398.
108. Jones, M. L., Martoni, C. J., Parent, M., Prakash, S., Cholesterol-lowering efficacy of a microencapsulated bile salt hydrolase-active Lactobacillus reuteri NCIMB 30242 yoghurt formulation in hypercholesterolaemic adults. Br. J. Nutr. 2012, 107, 1505-1513.
109. Ejtahed, S. H., Mohtadi-Nia, J., Homayouni-Rad, A., Niafar, M. et al., Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J. Dairy. Sci. 2011, 94, 3288-3294.
110. Agerbaek, M., Gerdes, U. L., Richelsen, B., Hypocholesterolaemic effect of a new fermented milk product in healthy middle-aged men. Eur. J. Clin. Nutr. 1995, 49, 346-352.
111. Schaafsma G., Meuling, J. A. W., van Dokkum, W., Bouley, C., Effects of milk products, fermented by Lactobacillus acidophilus and with fructo-oligosaccharides added, on blood lipids in male volunteers. Eur. J. Clin. Nutr. 1998, 56, 436-440.
112. Ataie-Jafari, A., Larijani, B., Majd, H. A., Cholesterol-lowering effect of probiotic yogurt in comparison with ordinary yogurt in mildly to moderately hypercholesterolemic subjects. Ann. Nutr. Metab. 2009, 54, 22-27.
113. Bertolami, M. C., Faludi, A. A., Batlouni, M., Evaluation of the effects of a new fermented milk product Gaio on primary hypercholesterolemia. Eur. J. Clin. Nutr. 1999, 53, 97-101.
114. Agerholm-Larsen, L., Bell, M. L., Grunwald, G. K., Astrup A., The effect of a probiotic milk product on plasma cholesterol: a meta-analysis of short-term intervention studies. Eur. J. Clin. Nutr. 2000, 54, 856-860.
115. Boyle, R. J., Robins-Browne, R. M., Tang, M. L. K., Probiotic use in clinical practice: what are the risks? Am. J. Clin. Nutr. 2006, 83, 1256-1264.
116. Hempel, S., Newberry, S., Ruelaz, A., Wang, Z. et al., Safety of probiotics to reduce risk and prevent or treat disease. Evidence report/technology assessment no. 200. AHRQ Publication No. 11-E007. Agency for Healthcare Research and Quality, Rockville, MD 2011.