Changes in gut microbiota in rats fed a high fat diet correlate with obesity-associated metabolic parameters

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Lecomte, Virginie ^a   Kaakoush, Nadeem O ^a   Maloney, Christopher A ^a   Raipuria, Mukesh ^a   Huinao, Karina D ^a   Mitchell, Hazel M ^a   Morris, Margaret J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; INSULIN; LEPTIN; PROPIONIC ACID; RNA 16S; TRIACYLGLYCEROL; BIOLOGICAL MARKER; GLUCOSE;

ACIDAMINOCOCCACEAE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DETERIORATION; FAT MASS; GLUCOSE TOLERANCE; HIGH THROUGHPUT SEQUENCING; INSULIN SENSITIVITY; INTESTINE FLORA; LACTOBACILLUS INTESTINALIS; LIPID DIET; MALE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; OBESITY; PHASCOLARCTOBACTERIUM; POPULATION ABUNDANCE; PROTEUS MIRABILIS; RAT; WEIGHT CHANGE; ANIMAL; BIODIVERSITY; BLOOD; BODY WEIGHT; DIET; ENERGY METABOLISM; METABOLISM; METAGENOME;

ACIDAMINOCOCCACEAE; BACTERIA (MICROORGANISMS); LACTOBACILLUS INTESTINALIS; PHASCOLARCTOBACTERIUM; PROTEUS MIRABILIS; RATTUS;

ANIMALS; BIODIVERSITY; BIOMARKERS; BODY WEIGHT; DIET; DIET, HIGH-FAT; ENERGY METABOLISM; GASTROINTESTINAL MICROBIOME; GLUCOSE; INSULIN; MALE; METAGENOME; OBESITY; RATS;

EID: 84930675333     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126931     Document Type: Article

References (87)

1. World Health Organisation. World Health Statistic 2013. Geneva: WHO. 2013.Available: http://www.who.int/gho/publications/world-health-statistics/2013/en/
2. Everard A, Cani PD. Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol. 2013; 27: 73-83. doi: 10.1016/j.bpg.2013.03.007 PMID: 23768554
3. Robles Alonso V, Guarner F. Linking the gut microbiota to human health. Br J Nutr. 2013; 109 Suppl 2: S21-6. doi: 10.1017/S0007114512005235 PMID: 23360877
4. Plummer JL, Ossowicz CJ, Whibley C, Ilsley AH, Hall PD. Influence of intestinal flora on the development of fibrosis and cirrhosis in a rat model. J Gastroenterol Hepatol. 2000; 15: 1307-11. PMID: 11129226
5. The Human Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486: 207-14. doi: 10.1038/nature11234 PMID: 22699609
6. Brooks SP, McAllister M, Sandoz M, Kalmokoff ML. Culture-independent phylogenetic analysis of the faecal flora of the rat. Can J Microbiol. 2003; 49: 589-601. PMID: 14663493
7. Manichanh C, Reeder J, Gibert P, Varela E, Llopis M, Antolin M, et al. Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res. 2010; 20: 1411-9. doi: 10.1101/gr.107987.110 PMID: 20736229
8. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005; 102: 11070-5. PMID: 16033867
9. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444: 1027-31. PMID: 17183312
10. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006; 444: 1022-3. PMID: 17183309
11. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond). 2008; 32: 1720-4. doi: 10.1038/ijo.2008.155 PMID: 18779823
12. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 2007; 73: 1073-8. PMID: 17189447
13. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring). 2010; 18: 190-5. doi: 10.1038/oby.2009.167 PMID: 19498350
14. Duncan SH, Louis P, Flint HJ. Cultivable bacterial diversity from the human colon. Lett Appl Microbiol. 2007; 44: 343-50. PMID: 17397470
15. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013; 500: 541-6. doi: 10.1038/nature12506 PMID: 23985870
16. Burcelin R. Regulation of metabolism: a cross talk between gut microbiota and its human host. Physiology (Bethesda). 2012; 27: 300-7. doi: 10.1152/physiol.00023.2012 PMID: 23026753
17. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012; 336: 1262-7. doi: 10.1126/science.1223813 PMID: 22674330
18. Power SE, O'Toole PW, Stanton C, Ross RP, Fitzgerald GF. Intestinal microbiota, diet and health. Br J Nutr. 2013;1-16.
19. Mujico JR, Baccan GC, Gheorghe A, Diaz LE, Marcos A. Changes in gut microbiota due to supplemented fatty acids in diet-induced obese mice. Br J Nutr. 2013; 110: 711-20. doi: 10.1017/ S0007114512005612 PMID: 23302605
20. Serino M, Luche E, Gres S, Baylac A, Berge M, Cenac C, et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012; 61: 543-53. doi: 10.1136/gutjnl-2011-301012 PMID: 22110050
21. de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol. 2010; 299: G440-8. doi: 10.1152/ajpgi.00098.2010 PMID: 20508158
22. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009; 137: 1716-24 e1-2. doi: 10.1053/j.gastro.2009.08.042 PMID: 19706296
23. Mozes S, Bujnakova D, Sefcikova Z, Kmet V. Developmental changes of gut microflora and enzyme activity in rat pups exposed to fat-rich diet. Obesity (Silver Spring). 2008; 16: 2610-5. doi: 10.1038/oby.2008.435 PMID: 18927555
24. Serino M, Chabo C, Burcelin R. Intestinal MicrobiOMICS to define health and disease in human and mice. Curr Pharm Biotechnol. 2012; 13: 746-58. PMID: 22122483
25. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol. 2008; 6: 121-31. doi: 10.1038/nrmicro1817 PMID: 18180751
26. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006; 40: 235-43. PMID: 16633129
27. Al-Lahham SH, Peppelenbosch MP, Roelofsen H, Vonk RJ, Venema K. Biological effects of propionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim Biophys Acta. 2010; 1801: 1175-83. doi: 10.1016/j.bbalip.2010.07.007 PMID: 20691280
28. Cani PD, Everard A, Duparc T. Gut microbiota, enteroendocrine functions and metabolism. Curr Opin Pharmacol. 2013; 13: 935-40. doi: 10.1016/j.coph.2013.09.008 PMID: 24075718
29. Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009; 139: 1619-25. doi: 10.3945/jn.109.104638 PMID: 19625695
30. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007; 56: 1761-72. PMID: 17456850
31. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008; 57: 1470-81. doi: 10.2337/db07-1403 PMID: 18305141
32. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, Le Chatelier E, et al. Dietary intervention impact on gut microbial gene richness. Nature. 2013; 500: 585-8. doi: 10.1038/nature12480 PMID: 23985875
33. Delzenne NM, Neyrinck AM, Cani PD. Gut microbiota and metabolic disorders: How prebiotic can work? Br J Nutr. 2013; 109 Suppl 2: S81-5. doi: 10.1017/S0007114512004047 PMID: 23360884
34. Hernell O, West CE. Clinical effects of probiotics: scientific evidence from a paediatric perspective. British Journal of Nutrition. 2013; 109: S70-S75.
35. Andreotti R, Perez de Leon AA, Dowd SE, Guerrero FD, Bendele KG, Scoles GA. Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol. 2011; 11: 6. doi: 10.1186/1471-2180-11-6 PMID: 21211038
36. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun. 2010; 78: 1509-19. doi: 10.1128/IAI.00862-09 PMID: 20145094
37. Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe. 2010; 16: 444-53. doi: 10.1016/j.anaerobe.2010.06.008 PMID: 20603222
38. Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol. 2011; 76: 301-10. doi: 10.1111/j.1574-6941.2011.01058.x PMID: 21261668
39. Gontcharova V, Youn E, Wolcott RD, Hollister EB, Gentry TJ, Dowd SE. Black Box Chimera Check (B2C2): a Windows-Based Software for Batch Depletion of Chimeras from Bacterial 16S rRNA Gene Datasets. Open Microbiol J. 2010; 4: 47-52. doi: 10.2174/1874285801004010047 PMID: 21339894
40. Capone KA, Dowd SE, Stamatas GN, Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011; 131: 2026-32. doi: 10.1038/jid.2011.168 PMID: 21697884
41. Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis. 2008; 5: 459-72. doi: 10.1089/fpd.2008.0107 PMID: 18713063
42. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 2008; 8: 125. doi: 10.1186/1471-2180-8-125 PMID: 18652685
43. Dowd SE, Delton Hanson J, Rees E, Wolcott RD, Zischau AM, Sun Y, et al. Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care. 2011; 20: 40-7. PMID: 21278640
44. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460-1. doi: 10.1093/bioinformatics/btq461 PMID: 20709691
45. Eren AM, Zozaya M, Taylor CM, Dowd SE, Martin DH, Ferris MJ. Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS One. 2011; 6: e26732. doi: 10.1371/journal.pone.0026732 PMID: 22046340
46. Swanson KS, Dowd SE, Suchodolski JS, Middelbos IS, Vester BM, Barry KA, et al. Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. ISME J. 2011; 5: 639-49. doi: 10.1038/ismej.2010.162 PMID: 20962874
47. Dowd SE, Zaragoza J, Rodriguez JR, Oliver MJ, Payton PR. Windows. NET Network Distributed Basic Local Alignment Search Toolkit (W.ND-BLAST). BMC Bioinformatics. 2005; 6: 93. PMID: 15819992
48. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009; 37: D141-5. doi: 10.1093/nar/gkn879 PMID: 19004872
49. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecology. 2001; 26: 32-46.
50. Clarke KR. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology. 1993; 18: 117-143.
51. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009; 457: 480-4. doi: 10.1038/nature07540 PMID: 19043404
52. Sefcikova Z, Kmet V, Bujnakova D, Racek L, Mozes S. Development of gut microflora in obese and lean rats. Folia Microbiol (Praha). 2010; 55: 373-5. doi: 10.1007/s12223-010-0061-2 PMID: 20680574
53. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010; 5: e9085. doi: 10.1371/journal.pone.0009085 PMID: 20140211
54. Davis JJ, Xia F, Overbeek RA, Olsen GJ. Genomes of the class Erysipelotrichia clarify the firmicute origin of the class Mollicutes. Int J Syst Evol Microbiol. 2013; 63: 2727-41. doi: 10.1099/ijs.0.048983-0 PMID: 23606477
55. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008; 3: 213-23. doi: 10.1016/j. chom.2008.02.015 PMID: 18407065
56. Tomas J, Langella P, Cherbuy C. The intestinal microbiota in the rat model: major breakthroughs from new technologies. Anim Health Res Rev. 2012; 13: 54-63. doi: 10.1017/S1466252312000072 PMID: 22853927
57. Joly F, Mayeur C, Bruneau A, Noordine ML, Meylheuc T, Langella P, et al. Drastic changes in fecal and mucosa-associated microbiota in adult patients with short bowel syndrome. Biochimie. 2010; 92: 753-61. doi: 10.1016/j.biochi.2010.02.015 PMID: 20172013
58. Dalby AB, Frank DN, St Amand AL, Bendele AM, Pace NR. Culture-independent analysis of indomethacin-induced alterations in the rat gastrointestinal microbiota. Appl Environ Microbiol. 2006; 72: 6707-15. PMID: 17021222
59. Zhao X, Liu XW, Xie N, Wang XH, Cui Y, Yang JW, et al. Lactobacillus species shift in distal esophagus of high-fat-diet-fed rats. World J Gastroenterol. 2011; 17: 3151-7. doi: 10.3748/wjg.v17.i26.3151 PMID: 21912459
60. Santacruz A, Marcos A, Warnberg J, Marti A, Martin-Matillas M, Campoy C, et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring). 2009; 17: 1906-15. doi: 10.1038/oby.2009.112 PMID: 19390523
61. Tanida M, Shen J, Maeda K, Horii Y, Yamano T, Fukushima Y, et al. High-fat diet-induced obesity is attenuated by probiotic strain Lactobacillus paracasei ST11 (NCC2461) in rats. Obesity Research & Clinical Practice. 2008; 2: 159-169.
62. Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, et al. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr. 2010; 64: 636-43. doi: 10.1038/ejcn.2010.19 PMID: 20216555
63. Zhang C, Li S, Yang L, Huang P, Li W, Wang S, et al. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat Commun. 2013; 4: 2163. doi: 10.1038/ncomms3163 PMID: 23860099
64. Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog. 2012; 53: 100-8. doi: 10.1016/j.micpath.2012.05.007 PMID: 22634320
65. Drissi F, Merhej V, Angelakis E, El Kaoutari A, Carriere F, Henrissat B, et al. Comparative genomics analysis of Lactobacillus species associated with weight gain or weight protection. Nutr Diabetes. 2014; 4: e109. doi: 10.1038/nutd.2014.6 PMID: 24567124
66. Fleissner CK, Huebel N, Abd El-Bary MM, Loh G, Klaus S, Blaut M. Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr. 2010; 104: 919-29. doi: 10.1017/S0007114510001303 PMID: 20441670
67. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One. 2012; 7: e39743. doi: 10.1371/journal.pone.0039743 PMID: 22761885
68. Kim KA, Gu W, Lee IA, Joh EH, Kim DH. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One. 2012; 7: e47713. doi: 10.1371/journal.pone.0047713 PMID: 23091640
69. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007; 2: 204. PMID: 18030708
70. Vael C, Verhulst SL, Nelen V, Goossens H, Desager KN. Intestinal microflora and body mass index during the first three years of life: an observational study. Gut Pathog. 2011; 3: 8. doi: 10.1186/1757-4749-3-8 PMID: 21605455
71. Armbruster CE, Mobley HL. Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat Rev Microbiol. 2012; 10: 743-54. doi: 10.1038/nrmicro2890 PMID: 23042564
72. Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe. 2010; 8: 292-300. doi: 10.1016/j.chom.2010.08.004 PMID: 20833380
73. Newkirk MM, Zbar A, Baron M, Manges AR. Distinct bacterial colonization patterns of Escherichia coli subtypes associate with rheumatoid factor status in early inflammatory arthritis. Rheumatology (Oxford). 2010; 49: 1311-6. doi: 10.1093/rheumatology/keq088 PMID: 20360042
74. Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004; 91: 915-23. PMID: 15182395
75. Watanabe Y, Nagai F, Morotomi M. Characterization of Phascolarctobacterium succinatutens sp. nov., an asaccharolytic, succinate-utilizing bacterium isolated from human feces. Appl Environ Microbiol. 2011; 78: 511-8. doi: 10.1128/AEM.06035-11 PMID: 22081579
76. Johnson JL, Moore WEC, Moore LVH. Bacteroides-Caccae Sp-Nov, Bacteroides-Merdae Sp-Nov, and Bacteroides-Stercoris Sp-Nov Isolated from Human Feces. International Journal of Systematic Bacteriology. 1986; 36: 499-501.
77. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011; 13: 517-26. doi: 10.1016/j.cmet.2011.02.018 PMID: 21531334
78. Vinolo MA, Ferguson GJ, Kulkarni S, Damoulakis G, Anderson K, Bohlooly YM, et al. SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor. PLoS One. 2011; 6: e21205. doi: 10.1371/journal.pone.0021205 PMID: 21698257
79. Vinolo MA, Rodrigues HG, Nachbar RT, Curi R. Regulation of inflammation by short chain fatty acids. Nutrients. 2011; 3: 858-76. doi: 10.3390/nu3100858 PMID: 22254083
80. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL, et al. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology. 2008; 149: 4519-26. doi: 10.1210/en.2008-0059 PMID: 18499755
81. Bjursell M, Admyre T, Goransson M, Marley AE, Smith DM, Oscarsson J, et al. Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. Am J Physiol Endocrinol Metab. 2011; 300: E211-20. doi: 10.1152/ajpendo.00229.2010 PMID: 20959533
82. Tabuchi M, Ozaki M, Tamura A, Yamada N, Ishida T, Hosoda M, et al. Antidiabetic effect of Lactobacillus GG in streptozotocin-induced diabetic rats. Biosci Biotechnol Biochem. 2003; 67: 1421-4. PMID: 12843677
83. 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: 62-8. PMID: 17084593
84. Xie N, Cui Y, Yin YN, Zhao X, Yang JW, Wang ZG, et al. Effects of two Lactobacillus strains on lipid metabolism and intestinal microflora in rats fed a high-cholesterol diet. BMC Complement Altern Med. 2011; 11: 53. doi: 10.1186/1472-6882-11-53 PMID: 21722398
85. Naito E, Yoshida Y, Makino K, Kounoshi Y, Kunihiro S, Takahashi R, et al. Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. J Appl Microbiol. 2011; 110: 650-7. doi: 10.1111/j.1365-2672.2010.04922.x PMID: 21281408
86. Kootte RS, Vrieze A, Holleman F, Dallinga-Thie GM, Zoetendal EG, de Vos WM, et al. The therapeutic potential of manipulating gut microbiota in obesity and type 2 diabetes mellitus. Diabetes Obes Metab. 2012; 14: 112-20. doi: 10.1111/j.1463-1326.2011.01483.x PMID: 21812894
87. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009; 58: 1509-17. doi: 10.2337/db08-1637 PMID: 19366864