Mechanisms responsible for the hypocholesterolaemic effect of regular consumption of probiotics

Nutrition Research Reviews

Volumn 30, Issue 1, 2017, Pages 36-49

  Reis, S A ^a   Conceicao L L ^a   Rosa, D D ^a   Siqueira, N P ^a   Peluzio, M C G ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

CVD; Dyslipidaemias; Lipid metabolism; Probiotics

Indexed keywords

BILE SALT; COPROSTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MEMBRANE PROTEIN; MESSENGER RNA; NIEMANN PICK C1 LIKE 1 PROTEIN; PROBIOTIC AGENT; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN RECEPTOR; BILE ACID; CHOLESTANOL; CHOLESTEROL; HYPOCHOLESTEROLEMIC AGENT;

BACTERIAL STRAIN; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM LONGUM; BODY FAT; CELL MEMBRANE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; DRUG ACTIVITY; ENZYME INHIBITION; EUBACTERIUM; EUBACTERIUM COPROSTANOLIGENES; HUMAN; HYPOCHOLESTEROLEMIC ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INTESTINE ABSORPTION; INTESTINE CELL; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; LIMIT OF QUANTITATION; LIPID METABOLISM; NONHUMAN; PRECIPITATION; REVIEW; WESTERN DIET; ANIMAL; BACTERIUM; BIOSYNTHESIS; CARDIOVASCULAR DISEASE; DYSLIPIDEMIA; INTESTINE; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTICHOLESTEREMIC AGENTS; BACTERIA; BILE ACIDS AND SALTS; CARDIOVASCULAR DISEASES; CELL MEMBRANE; CHEMICAL PRECIPITATION; CHOLESTANOL; CHOLESTEROL; DYSLIPIDEMIAS; HUMANS; INTESTINAL ABSORPTION; INTESTINES; LIPID METABOLISM; PROBIOTICS;

EID: 85006782938     PISSN: 09544224     EISSN: 14752700     Source Type: Journal    
DOI: 10.1017/S0954422416000226     Document Type: Review

References (93)

1. World Health Organization (2011) Cardiovascular Disease. Fact sheet no. 317. Geneva, Switzerland: WHO. http://www. who.int/mediacentre/factsheets/fs317/en/(accessed January 2015).
2. Guo Z, Liu XM, Zhang QX, et al. (2011) Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomized controlled trials. Nutrition, Metabolism and Cardiovascular Diseases 21, 844-850.
3. Lahti L, Salonen A, Kekkonen RA, et al. (2013) Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data. PeerJ 1, e32.
4. DiRienzo DB (2013) Effect of probiotics on biomarkers of cardiovascular disease: implications for heart-healthy diets. Nutrition Reviews 72, 18-29.
5. Food and Agriculture Organization of the United Nations/World Health Organization (2001) Probiotics in Food. Health and Nutritional Properties and Guidelines for Evaluation, FAO Food and Nutrition Paper no. 85. Rome and Geneva: Food and Agriculture Organization of the United Nations/World Health Organization.
6. Mann GV & Spoerry A (1974) Studies of a surfactant and cholesteremia in the Maasai. American Journal of Clinical Nutrition 27, 464-469.
7. Huang Y & Zheng Y (2010) The probiotic Lactobacillus acidophilus reduces cholesterol absorption through the down-regulation of Niemann-Pick C1-like 1 in Caco-2 cells. British Journal of Nutrition 103, 473-478.
8. Karlsson C, Ahrn? S, Molin G, et al. (2010) Probiotic therapy to men with incipient arteriosclerosis initiates increased bacterial diversity in colon: a randomized controlled trial. Atherosclerosis 208, 228-233.
9. Manson JE, Tosteson H, Ridker PM, et al. (1992) The primary prevention of myocardial infartion. New England Journal of Medicine 21, 1406-1416.
10. Bordoni A, Amaretti A, Leonardi A, et al. (2013) Cholesterollowering probiotics: in vitro selection and in vivo testing of bifidobacteria. Applied Microbiology and Biotechnology 97, 8273-8281.
11. Stancu CS, Sanda GM, Deleanu M, et al. (2014) Probiotics determine hypolipidemic and antioxidant effects in hyperlipidemic hamsters. Molecular Nutrition and Food Research 58, 559-568.
12. Fava F, Lovegrove JA, Gitau R, et al. (2006) The gut microbiota and lipid metabolism: implications for human health and coronary heart disease. Current Medicinal Chemistry 13, 3005-3021.
13. Zhao C & Wright KD (2010) Liver X receptor in cholesterol metabolism. Journal of Endocrinology 204, 233-240.
14. Tok E & Aslim B (2010) Cholesterol removal by some lactic acid bacteria that can be used as probiotic. Microbiology and Immunology 54, 257-264.
15. Lecerf JM & Lorgeril M (2011) Dietary cholesterol: from physiology to cardiovascular risk. British Journal of Nutrition 106, 6-14.
16. Ridlon JM, Kang DJ & Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. Journal of Lipid Research 47, 241-259.
17. G?rard P (2014) Metabolism of cholesterol and bile acids by the gut microbiota. Pathogens 3, 14-24.
18. Kumar M, Nagpal R, Kumar R, et al. (2012) Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Experimental Diabetes Research 2012, 902917.
19. Ishimwe N, Daliri EB, Lee BH, et al. (2015) The perspective on cholesterol-lowering mechanisms of probiotics. Molecular Nutrition and Food Research 59, 94-105.
20. Guo CF & Li JY (2013) Hypocholesterolaemic action of Lactobacillus casei F0822 in rats fed a cholesterolenriched diet. International Dairy Journal 32, 144-149.
21. Jones ML, Martoni CJ & Prakash S (2012) Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. European Journal of Clinical Nutrition 66, 1234-1241.
22. Jones ML, Martoni CJ, Parent M, et al. (2012) Cholesterollowering efficacy of a microencapsulated bile salt hydrolaseactive Lactobacillus reuteri NCIMB 30242 yoghurt formulation in hypercholesterolaemic adults. British Journal of Nutrition 107, 1505-1513.
23. Bi J, Fang F, Lu S, et al. (2013) New insight into the catalytic properties of bile salt hydrolase. Journal of Molecular Catalysis B: Enzymatic 96, 46-51.
24. Sridevi N, Vishwe P & Prabhune A (2009) Hypocholesteremic effect of bile salt hydrolase from Lactobacillus buchneri ATCC 4005. Food Research International 49, 516-520.
25. Miremadi F, Ayyash M, Sherkat F, et al. (2014) Cholesterol reduction mechanisms and fatty acid composition of cellular membranes of probiotic lactobacilli and bifidobacteria. Journal of Functional Foods 9, 295-305.
26. Park YH, Kim JG, Shin YW, et al. (2007) Effect of dietary inclusion of Lactobacillus acidophilus ATCC 43121 on cholesterol metabolism in rats. Journal of Microbiology and Biotechnology 17, 655-662.
27. Jeun J, Kim S, Cho SY, et al. (2010) Hypocholesterolemic effects of Lactobacillus plantarum KCTC3928 by increased bile acid excretion in C57BL/6 mice. Nutrition 26, 321-330.
28. Degirolamo C, Rainaldi S, Bovenga F, et al. (2014) Microbiota modification with probiotics induces hepatic bile acid synthesis via downregulation of the Fxr-Fgf15 axis in mice. Cell Reports 7, 12-18.
29. Wang CY, Wu SC, Ng CC, et al. (2009) Effect of Lactobacillusfermented adlay-based milk on lipid metabolism of hamsters fed cholesterol-enriched diet. Food Research International 43, 819-824.
30. Lye HS, Rahmat-Ali GR & Liong MT (2010) Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. International Dairy Journal 20, 169-175.
31. Ahn YT, Kim GB, Lim KS, et al. (2003) Deconjugation of bile salts by Lactobacillus acidophilus isolates. International Dairy Journal 13, 303-311.
32. Klaver FAM & Meer RVD (1993) The assumed assimilation of cholesterol by lactobacilli and Bifidobacterium bifidum is due to their bile salt-deconjugating activity. Applied and Environmental Microbiology 59, 1120-1124.
33. Kumar R, Grover S & Batish VK (2011) Hypocholesterolaemic effect of dietary inclusion of two putative probiotic bile salt hydrolase-producing Lactobacillus plantarum strains in Sprague-Dawley rats. British Journal of Nutrition 105, 561-573.
34. Tahri K, Grill JP & Schneider F (1996) Bifidobacteria strain behavior toward cholesterol: coprecipitation with bile salts and assimilation. Current Microbiology 33, 187-193.
35. Lye HS, Kuan CY, Ewe JA, et al. (2009) The improvement of hypertension by probiotics: effects on cholesterol, diabetes, renin, and phytoestrogens. International Journal of Molecular Sciences 10, 3755-3775.
36. Iranmanesh M, Ezzatpanah H & Mojgani N (2014) Antibacterial activity and cholesterol assimilation of lactic acid bacteria isolated from tradicional Iranian dairy produts. LWT-Food Science and Technology 58, 355-359.
37. Zanotti I, Turroni F, Piemontese A, et al. (2015) Evidence for cholesterol-lowering activity by Bifidobacterium bifidum PRL2010 through gut microbiota modulation. Applied Microbiology and Biotechnology 99, 6816-6829.
38. Liong MT & Shah NP (2005) Acid and bile tolerance and the cholesterol removal ability of bifidobacteria strains. Bioscience Microflora 24, 1-10.
39. Lye HS, Rusul G & Liong MT (2010) Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. Journal of Dairy Science 93, 1383-1392.
40. Lee DK, Jang S, Baek EH, et al. (2009) Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content. Lipids in Health and Disease 8, 21.
41. Park YH, Kim JG, Shin YW, et al. (2008) Effects of Lactobacillus acidophilus 43121 and a mixture of Lactobacillus casei and Bifidobacterium longum on the serum cholesterol level and fecal sterol excretion in hypercholesterolemia-induced pigs. Bioscience, Biotechnology and Biochemistry 72, 595-600.
42. Hatakka K, Holma R, El-Nezami H, et al. (2008) The influence of Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp. shermanii JS on potentially carcinogenic bacterial activity in human colon. International Journal of Food Microbiology 128, 406-410.
43. Madani G, Mirlohi M, Yahay M, et al. (2013) How much in vitro cholesterol reducing activity of lactobacilli predicts their in vivo cholesterol function? International Journal of Preventive Medicine 4, 404-413.
44. Sirilun S, Chaiyasut C, Kantachote D, et al. (2010) Characterisation of non human origin probiotic Lactobacillus plantarum with cholesterol-lowering property. African Journal of Microbiology Research 4, 994-1000.
45. Pigeon RM, Cuesta EP & Gililliand SE (2002) Binding of free bile acids by cells of yogurt starter culture bacteria. Journal of Dairy Science 85, 2705-2710.
46. Li L, Buhman KK, Hartman PA, et al. (1995) Hypocholesterolemic effect of Eubacterium coprostanoligenes ATCC 51222 in rabbits. Letters in Applied Microbiology 20, 137-140.
47. Altmann SW, Davis HR Jr, Zhu LJ, et al. (2004) Niemann-Pick C1 like 1 protein is critical for intestinal cholesterol absorption. Science 303, 1201-1204.
48. Davis HR, Zhu L, Hoos LM, et al. (2004) Niemann-Pick C1 like 1 (NPC1L1) is the intestinal phytosterol and cholesterol transporter and a key modulator of whole-body cholesterol homeostasis. Journal of Biological Chemistry 279, 33586-33592.
49. Huang Y, Wu F, Wang X, et al. (2013) Characterization of Lactobacillus plantarum Lp27 isolated from Tibetan kefir grains: a potential probiotic bacterium with cholesterollowering effects. Journal of Dairy Science 96, 2816-2825.
50. B?ckhed F (2011) Programming of host metabolism by the gut microbiota. Annals of Nutrition and Metabolism 58, 44-52.
51. Pavlovic N, Stankov K & Mikov M (2012) Probiotics-interactions with bile acids and impact on cholesterol metabolism. Applied Biochemistry and Biotechnology 168, 1880-1895.
52. Guilloteau P, Martin L, Eeckhaut V, et al. (2010) From the gut to the peripheral tissues: the multiple effects of butyrate. Nutrition Research Reviews 23, 366-384.
53. Vipperla K & O'Keefe SJ (2012) The microbiota and its metabolites in colonic mucosal health and cancer risk. Nutrition in Clinical Practice 27, 624-635.
54. Henningsson A, Bjiirck I & Nyman M (2001) Short-chain fatty acid formation at fermentation of indigestible carbohydrates. Scandinavian Journal of Nutrition 45, 165-168.
55. Wolever TMS, Spadafora PJ, Cunnane SC, et al. (1995) Propionate inhibits incorporation of colonic [1,2-13C]acetate into plasma lipids in humans. American Journal of Clinical Nutrition 61, 1241-1247.
56. Arora T, Sharma R & Frost G (2011) Propionate. Anti-obesity and satiety enhancing factor? Appetite 56, 511-515.
57. Wang Y, Xu N, Xi A, et al. (2009) Effects of Lactobacillus plantarum MA2 isolated from Tibet kefir on lipid metabolism and intestinal microflora of rats fed on high-cholesterol diet. Applied Microbiology and Biotechnology 84, 341-347.
58. St-Onge MP, Farnworth ER, Savard T, et al. (2002) Kefir consumption does not alter plasma lipid levels or cholesterol fractional synthesis rates relative to milk in hyperlipidemic men: a randomized controlled trial. BMC Complementary and Alternative Medicine 2, 1.
59. Kumar M, Nagpal R, Verma V, et al. (2012) Probiotic metabolites as epigenetic targets in the prevention of colon cancer. Nutrition Reviews 71, 23-34.
60. Aronsson L, Huang Y, Parini P, et al. (2010) Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS ONE 5, e13087.
61. Cheik NC, Rossi EA, Guerra RL, et al. (2008) Effects of a ferment soy product on the adipocyte area reduction and dyslipidemia control in hypercholesterolemic adult male rats. Lipids in Health and Disease 7, 50.
62. Moon YJ, Baik SH & Cha YS (2014) Lipid-lowering effects of Pediococcus acidilactici M76 isolated from Korean traditional makgeolli in high fat diet-induced obese mice. Nutrients 6, 1016-1028.
63. Park JE, Oh SH & Cha YS (2014) Lactobacillus plantarum LG42 isolated from gajami sik-hae decreases body and fat pad weights in diet-induced obese mice. Journal of Applied Microbiology 116, 145-156.
64. Miyoshi M, Ogawa A, Higurashi S, et al. (2014) Anti-obesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in diet-induced obese mice. European Journal of Nutrition 53, 599-606.
65. Yoshida Y, Yokoi W, Wada Y, et al. (2004) Potent hypocholesterolemic activity of the yeast Kluyveromyces marxuanus YIT 8292 in rats fed a high cholesterol diet. Bioscience, Biotechnology and Biochemistry 68, 1185-1192.
66. Yoshida Y, Yokoi W, Ohishi K, et al. (2005) Effects of the cell wall of Kluyveromyces marxuanus YIT 8292 on the plasma cholesterol and fecal sterol excretion in rats fed on a high cholesterol diet. Bioscience, Biotechnology and Biochemistry 69, 714-723.
67. Waszkiewicz-Robak B (2013) Spent brewer's yeast and ?-glucans isolated from them as diet components modifying blood lipid metabolism disturbed by an atherogenic diet. In Lipid Metabolism, chapter 12 [R Valenzuela Baez, editor]. InTech. http://www.intechopen.com/books/lipid-metabolism/spent-brewer-s-yeast-and-beta-glucans-isolated-from-them-asdiet-components-modifying-blood-lipid-me.
68. El-Arab AE, Foheid S & El-Said M (2009) Effect of yeast and botanical ?-glucan on serum lipid profile and cecum probiotic bacteria using rats fed cholesterol diet. Polish Journal of Food and Nutrition Sciences 59, 169-174.
69. Wilson TA, Barbato DA & Nicolosi RJ (2013) Glucan fiber from spent brewer's yeast reduces early atherosclerosis greater than psyllium in hypercholesterolemic Syrian golden hamsters. Food and Nutrition Sciences 4, 566-571.
70. Yoshida Y, Naito E, Ohishi K, et al. (2007) Effect of Kluyveromyces marxuanus YIT 8292 crude cell wall fraction on serum lipids in normocholesterolemic and mildly hypercholesterolemic subjects. Bioscience, Biotechnology, and Biochemistry 71, 900-905.
71. Liu H, Xie Y, Xiong L, et al. (2012) Effect and mechanism of cholesterol-lowering by Kluyveromyces from Tibetan Kefir. Advanced Materials Research 343, 1290-1298.
72. Xie Y, Zhang H, Liu H, et al. (2015) Hypocholesterolemic effects of Kluyveromyces marxianus M3 isolated from Tibetan mushrooms on diet-induced hypercholesterolemia in rat. Brazilian Journal of Microbiology 46, 389-395.
73. Psomas EJ, Fletouris DJ, Litopoulou-Tzanetaki E, et al. (2003) Assimilation of cholesterol by yeast strains isolated from infant feces and feta cheese. Journal of Dairy Science 86, 3416-3422.
74. Girard P, Pansart Y & Verleye M (2014) Antihypercholesterolemic effect of Saccharomyces boulardii in the hamster. Pharmacology 94, 239-244.
75. Aloglu HS? , ?zer ED, ?ner Z, et al. (2015) Investigation of a probiotic yeast as a cholesterol lowering agent on rats fed on a high cholesterol enriched diet. KafKas Universitesi veteriner faKUltesi Dergisi 21, 685-689.
76. Ryan JJ, Hanes DA, Schafer MB, et al. (2015) Effect of the probiotic Saccharomyces boulardii on cholesterol and lipoprotein particles in hypercholesterolemic adults: a single-arm, open-label pilot study. Journal of Alternative and Complementary Medicine 21, 288-293.
77. Huang Y, Wang J, Cheng Y, et al. (2010) The hypocholesterolaemic effects of Lactobacillus acidophilus American Type Culture Collection 4356 in rats are mediated by the downregulation of Niemann-Pick C1-like 1. British Journal of Nutrition 104, 807-812.
78. Lee J, Kim Y, Yun HS, et al. (2010) Genetic and proteomic analysis of factors affecting serum cholesterol reduction by Lactobacillus acidophilus A4. Applied and Environmental Microbiology 76, 4829-4835.
79. Shin HS, Park SY, Lee DK, et al. (2010) Hypocholesterolemic effect of sonication-killed Bifidobacterium longum isolated from healthy adult Koreans in high cholesterol fed rats. Archives of Pharmacal Research 33, 1425-1431.
80. Xie N, Cui Y, Yin YN, et al. (2011) Effects of two Lactobacillus strains on lipid metabolism and intestinal microflora in rats fed a high-cholesterol diet. BMC Complementary and Alternative Medicine 11, 53.
81. Al-Sheraji SH, Ismail A, Manap MY, et al. (2012) Hypocholesterolaemic effect of yoghurt containing Bifidobacterium pseudocatenulatum G4 or Bifidobacterium longum BB536. Food Chemistry 135, 356-361.
82. F?k F & B?ckhed F (2012) Lactobacillus reuteri prevents dietinduced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe-/-mice. PLOS ONE 7, e46837.
83. Lindstr?m C, Holst O, Nilsson L, et al. (2012) Effects of Pediococcus parvulus 2.6 and its exopolysaccharide on plasma cholesterol levels and inflammatory markers in mice. AMB Express 2, 66.
84. Mohania D, Kansal VK, Shah D, et al. (2013) Therapeutic effect of probiotic Dahi on plasma, aortic, and hepatic lipid profile of hypercholesterolemic rats. Journal of Cardiovascular Pharmacology and Therapeutics 18, 490-497.
85. Zhang L, Zhang X, Liu C, et al. (2013) Manufacture of Cheddar cheese using probiotic Lactobacillus plantarum K25 and its cholesterol-lowering effects in a mice model. World Journal of Microbiology Biotechnology 29, 127-135.
86. Tang Z, Ma J, Zeng Z, et al. (2014) Inhibition of atherosclerotic plaque formation in ApoE-deficient mice by dietary supplementation with Lactobacillus casei. Functional Foods in Health and Disease 4, 147-158.
87. Sadrzadeh-Yeganeh H, Elmadfa I, Djazayery A, et al. (2010) The effects of probiotic and conventional yoghurt on lipid profile in women. British Journal of Nutrition 103, 1778-1783.
88. Kullisaar T, Shepetova J, Zilmer K, et al. (2011) An antioxidant probiotic reduces postprandial lipemia and oxidative stress. Central European Journal of Biology 6, 32-40.
89. Asemi Z, Samimi M, Tabasi Z, et al. (2012) Effect of daily consumption of probiotic yoghurt on lipid profiles in pregnant women: a randomized controlled clinical trial. Journal of Maternal-Fetal and Neonatal Medicine 25, 1552-1556.
90. Barreto FM, Sim?o ANC, Morimoto HK, et al. (2014) Beneficial effects of Lactobacillus plantarum on glycemia and homocysteine levels in postmenopausal women with metabolic syndrome. Nutrition 30, 939-942.
91. Guardamagna O, Amaretti A, Puddu PE, et al. (2014) Bifidobacteria supplementation: effects on plasma lipid profiles in dyslipidemic children. Nutrition 30, 831-836.
92. Mohamadshahi M, Veissi M, Haidari F, et al. (2014) Effects of probiotic yogurt consumption on lipid profile in type 2 diabetic patients: a randomized controlled clinical trial. Journal of Research in Medical Sciences 19, 531-536.
93. Rajkumar H, Mahmood N, Kumar M, et al. (2014) 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 of Inflammation 2014, 348959.