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Bifidobacterium bifidum TMC3115 Can Characteristically Influence Glucose and Lipid Profile and Intestinal Microbiota in the Middle-Aged and Elderly

  • Ke Wang
  • Xiaohong Yu
  • Yi Li
  • Yun Guo
  • Lin Ge
  • Fangfang Pu
  • Xinying Ma
  • Wenjing Cui
  • Francesco Marrota
  • Fang He
  • Ming Li
Article

Abstract

Bifidobacterium bifidum TMC3115 strain (TMC3115) was orally administrated to 47 subjects with mild hyperglycaemia and dyslipidaemia aged 45 to 75 years for 3 weeks. Blood samples were collected before and after intervention for profiling plasma total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol and triglyceride concentrations, as well as fasting blood glucose. Before and 3 and 4 weeks after intervention, the faecal samples were collected to analyse faecal microbiota using the sequencing of 16S rRNA genes with a next-generation sequencer. TMC3115 significantly decreased plasma TC and LDL-C levels of the tested subjects after intervention (P < 0.05). The frequencies of defaecation and faecal odour after the intervention and 1 week later were significantly better than at pre-intervention, respectively. TMC3115 administration increased Firmicutes, Bacteroides and Actinobacteria and decreases in Proteobacteria and Fusobacteria. There were significant increases in the proportions of Dorea and Lachnospira after the intervention (P < 0.05). TMC3115 also increased the level of Firmicutes and decreased that of Bacteroidetes 1 week after the intervention (P < 0.05). Serum triglycerides correlated negatively with the proportions of Bacteroidetes (R = − 0.21, P = 0.047) and Bacteroides (R = − 0.23, P = 0.029), while the relative abundance of Dialister of Firmicutes correlated negatively and significantly with the serum LDL-C (R = − 0.24, P = 0.022) and TC levels (R = − 0.22, P = 0.030). These results indicate that TMC3115 might exhibit beneficial effects on the serum cholesterol metabolism of subjects with dyslipidaemia through modulation of their intestinal microbiota. Trial registration: ChiCTR-OOC-16010271

Keywords

Probiotic supplementation Intestinal microflora Hyperglycaemia Dyslipidaemia 

Notes

Acknowledgements

We thank all the participants for agreeing to join this study. We are grateful to Hebei Yiran Biotechnology Co. Ltd. for providing Bifidobacterium bifidum TMC3115 and funding. We are indebted to the staffs at health service centre of Huayang community.

Compliance with Ethical Standards

The study was conducted in accordance with the guidelines of the Declaration of Helsinki and approved by the Ethical Committee of West China School of Public Health on 11 November 2016. Informed consent was obtained from all patients included in the study.

Conflict of Interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Gu JF. (2016). Interpretation of the status of Chinese residents’ nutrition and chronic diseases (2015). Acta Nutrimenta Sinica. (06), 525–529. http://kns.cnki.net/KCMS/detail/detail.aspx?FileName=YYXX201606007&DbName=CJFQ2016
  2. 2.
    Saito I (2012) Epidemiological evidence of type 2 diabetes mellitus, metabolic syndrome, and cardiovascular disease in Japan. Circ J 76(5):1066–1073 https://www.jstage.jst.go.jp/article/circj/76/5/76_CJ-11-1519/_article CrossRefGoogle Scholar
  3. 3.
    Alberti KG, Zimmet P, Shaw J (2006) Metabolic syndrome—a new world-wide definition. A consensus statement from the International Diabetes Federation. Diabet Med 23(5):469–480.  https://doi.org/10.1111/j.1464-5491.2006.01858 CrossRefGoogle Scholar
  4. 4.
    De la Sierra A, Pintó X, Guijarro C, Miranda JL, Callejo D, Cuervo J, Subirà R, Rubio M. (2015). Prevalence, treatment, and control of hypercholesterolemia in high cardiovascular risk patients: evidences from a systematic literature review in Spain. Adv Ther, 32(10):944–961. 10.1007%2Fs12325-015-0252-yGoogle Scholar
  5. 5.
    Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK (2011) Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol 19(7):349–359 https://linkinghub.elsevier.com/retrieve/pii/S0966-842X(11)00095-3 CrossRefGoogle Scholar
  6. 6.
    Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK et al (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5(2):e9085. http://journals.plos.org/plosone/article?id.  https://doi.org/10.1371/journal.pone.0009085 CrossRefGoogle Scholar
  7. 7.
    Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267 http://science.sciencemag.org/content/336/6086/1262.long CrossRefGoogle Scholar
  8. 8.
    Saez-Lara MJ, Robles-Sanchez C, Ruiz-Ojeda FJ, Plaza-Diaz J, Gil A (2016) Effects of probiotics and synbiotics on obesity, insulin resistance syndrome, type 2 diabetes and non-alcoholic fatty liver disease: a review of human clinical trials. Int J Mol Sci 17(6). http://www.mdpi.com/1422-0067/17/6/928
  9. 9.
    Guo Z, Liu XM, Zhang QX, Shen Z, Tian FW, Zhang H, Sun ZH, Zhang HP, Chen W (2011) Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomised controlled trials. Nutr Metab Cardiovasc Dis 21(11):844–850 https://linkinghub.elsevier.com/retrieve/pii/S0939-4753(11)00103-7 CrossRefGoogle Scholar
  10. 10.
    Patel AK, Singhania RR, Pandey A, Chincholkar SB (2010) Probiotic bile salt hydrolase: current developments and perspectives. Appl Biochem Biotechnol 162(1):166–180.  https://doi.org/10.1007/s12010-009-8738-1 CrossRefGoogle Scholar
  11. 11.
    Li Z, Yang S, Lin H, Huang J, Watkins PA, Moser AB, Desimone C, Song XY, Diehl AM (2003) Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology 37(2):343–350.  https://doi.org/10.1053/jhep.2003.50048 CrossRefGoogle Scholar
  12. 12.
    Tabuchi M, Ozaki M, Tamura A, Yamada N, Ishida T, Hosoda M et al (2003) Antidiabetic effect of Lactobacillus GG in streptozotocin-induced diabetic rats. Biosci Biotechnol Biochem 67(6):1421–1424.  https://doi.org/10.1271/bbb.67.1421 CrossRefGoogle Scholar
  13. 13.
    Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50(11):2374–2383.  https://doi.org/10.1007/s00125-007-0791-0 CrossRefGoogle Scholar
  14. 14.
    St-Onge MP, Farnworth ER, Savard T, Chabot D, Mafu A, Jones PJ (2002) Kefir consumption does not alter plasma lipid levels or cholesterol fractional synthesis rates relative to milk in hyperlipidemic men: a randomized controlled trial [ISRCTN10820810]. BMC Complement Altern Med 2(1) https://www.ncbi.nlm.nih.gov/pmc/articles/PMC65674/
  15. 15.
    Yang YX, Zhang HM. (2016). A brief introduction to Chinese residents’ dietary guidelines (2016). Acta Nutrimenta Sinica. (03):209–217. http://kns.cnki.net/KCMS/detail/detail.aspx?FileName=YYXX201603003&DbName=CJFQ2016
  16. 16.
    Zhu JR, Gao RL, Zhao SP, Lu GP, Zhao D, Li JJ. (2016). Guidelines for the prevention and treatment of dyslipidemia in Chinese adults (revised edition in 2016). Chinese Circulation Journal (10):937–953. http://kns.cnki.net/KCMS/detail/detail.aspx?FileName=ZGXH201610002&DbName=CJFQ2016
  17. 17.
    Wang SJ, Zhu H, Lu C, He F, Feng LL, Luo YK. (2011). Effect of yogurt drink containing bifidobacterium lactis LB-1 on intestinal health of adult women. Food Research and Development. (09), 193–196. http://kns.cnki.net/KCMS/detail/detail.aspx?FileName=SPYK201109061&DbName=CJFQ2011
  18. 18.
    Ren D, Gong S, Shu J, Zhu J, Rong F, Zhang Z, Wang D, Gao L, Qu T, Liu H, Chen P (2017) Mixed Lactobacillus plantarum strains inhibit Staphylococcus aureus induced inflammation and ameliorate intestinal microflora in mice. Biomed Res Int 2017:7476467 https://www.hindawi.com/journals/bmri/2017/7476467/ Google Scholar
  19. 19.
    Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10(1):57–59 https://www.nature.com/articles/nmeth.2276 CrossRefGoogle Scholar
  20. 20.
    McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217. http://journals.plos.org/plosone/article?id.  https://doi.org/10.1371/journal.pone.0061217 CrossRefGoogle Scholar
  21. 21.
    Bordoni A, Amaretti A, Leonardi A, Boschetti E, Danesi F, Matteuzzi D, Roncaglia L, Raimondi S, Rossi M (2013) Cholesterol-lowering probiotics: in vitro selection and in vivo testing of bifidobacteria. Appl Microbiol Biotechnol 97(18):8273–8281.  https://doi.org/10.1007/s00253-013-5088-2 CrossRefGoogle Scholar
  22. 22.
    Turroni F, Ventura M, Butto LF, Duranti S, O'Toole PW, Motherway MO et al (2014) Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71(2):183–203.  https://doi.org/10.1007/s00018-013-1318-0 CrossRefGoogle Scholar
  23. 23.
    Yadav H, Jain S, Sinha PR (2007) Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition 23(1):62–68 http://www.nutritionjrnl.com/article/S0899-9007(06)00329-7/fulltext CrossRefGoogle Scholar
  24. 24.
    He F, Morita H, Ouwehand AC, Hosoda M, Hiramatsu M, Kurisaki J, Isolauri E, Benno Y, Salminen S (2002) Stimulation of the secretion of pro-inflammatory cytokines by Bifidobacterium strains. Microbiol Immunol 46(11):781–785.  https://doi.org/10.1111/j.1348-0421.2002 CrossRefGoogle Scholar
  25. 25.
    Harata G, He F, Takahashi K, Hosono A, Kawase M, Kubota A, Hiramatsu M, Kaminogawa S (2010) Bifidobacterium suppresses IgE-mediated degranulation of rat basophilic leukemia (RBL-2H3) cells. Microbiol Immunol 54(1):54–57.  https://doi.org/10.1111/j.1348-0421.2009.00185 CrossRefGoogle Scholar
  26. 26.
    Wu ZX, Li SS, Shen X, et al. (2017). Effects on immunomodulatory of probiotics. Food Science and Technology. (01), 29–33. http://kns.cnki.net/KCMS/detail/detail.aspx?FileName=SSPJ201701010&DbName=CJFQ2017
  27. 27.
    Zanotti I, Turroni F, Piemontese A, Mancabelli L, Milani C, Viappiani A, Prevedini G, Sanchez B, Margolles A, Elviri L, Franco B, van Sinderen D, Ventura M (2015) Evidence for cholesterol-lowering activity by Bifidobacterium bifidum PRL2010 through gut microbiota modulation. Appl Microbiol Biotechnol 99(16):6813–6829.  https://doi.org/10.1007/s00253-015-6564-7 CrossRefGoogle Scholar
  28. 28.
    Turroni F, Duranti S, Bottacini F, Guglielmetti S, Van Sinderen D, Ventura M (2014) Bifidobacterium bifidum as an example of a specialized human gut commensal. Front Microbiol 5(437).  https://doi.org/10.3389/fmicb.2014.00437/full
  29. 29.
    Ling N, Zhao SL, Qi SH, He F. (2015). Bifidobacterium TMC3115 can inhibit fat cells of discrepancy and its application, CN104630096A. http://dbpub.cnki.net/grid2008/dbpub/detail.aspx?filename=CN104630096A&dbname=
  30. 30.
    Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V, Akbarian-Moghari A (2011) Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J Dairy Sci 94(7):3288–3294 http://linkinghub.elsevier.com/retrieve/pii/S0022-0302(11)00321-3 CrossRefGoogle Scholar
  31. 31.
    Rajkumar H, Mahmood N, Kumar M, Varikuti SR, Challa HR, Myakala SP (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. Mediat Inflamm 2014:348959 https://www.hindawi.com/journals/mi/2014/348959/ CrossRefGoogle Scholar
  32. 32.
    Nabavi S, Rafraf M, Somi MH, Homayouni-Rad A, Asghari-Jafarabadi M (2014) Effects of probiotic yogurt consumption on metabolic factors in individuals with nonalcoholic fatty liver disease. J Dairy Sci 97(12):7386–7393 https://linkinghub.elsevier.com/retrieve/pii/S0022-0302(14)00701-2 CrossRefGoogle Scholar
  33. 33.
    Sun J, Buys N (2015) Effects of probiotics consumption on lowering lipids and CVD risk factors: a systematic review and meta-analysis of randomized controlled trials. Ann Med 47(6):430–440.  https://doi.org/10.3109/07853890.2015.1071872?journalCode=iann20 CrossRefGoogle Scholar
  34. 34.
    Erejuwa OO, Sulaiman SA, Ab WM (2014) Modulation of gut microbiota in the management of metabolic disorders: the prospects and challenges. Int J Mol Sci 15(3):4158–4188 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3975390/ CrossRefGoogle Scholar
  35. 35.
    Ataie-Jafari A, Larijani B, Alavi MH, Tahbaz F (2009) Cholesterol-lowering effect of probiotic yogurt in comparison with ordinary yogurt in mildly to moderately hypercholesterolemic subjects. Ann Nutr Metab 54(1):22–27 https://www.karger.com/Article/Abstract/203284 CrossRefGoogle Scholar
  36. 36.
    Mazloom Z, Yousefinejad A, Dabbaghmanesh MH (2013) Effect of probiotics on lipid profile, glycemic control, insulin action, oxidative stress, and inflammatory markers in patients with type 2 diabetes: a clinical trial. Iran J Med Sci 38(1):38–43 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3642943/ Google Scholar
  37. 37.
    Oner O, Aslim B, Aydas SB (2014) Mechanisms of cholesterol-lowering effects of lactobacilli and bifidobacteria strains as potential probiotics with their bsh gene analysis. J Mol Microbiol Biotechnol 24(1):12–18 https://www.karger.com/Article/Abstract/354316 CrossRefGoogle Scholar
  38. 38.
    Kumar M, Nagpal R, Kumar R, Hemalatha R, Verma V, Kumar A, Chakraborty C, Singh B, Marotta F, Jain S, Yadav H (2012) Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diabetes Res 2012:902917 https://www.hindawi.com/journals/jdr/2012/902917/ CrossRefGoogle Scholar
  39. 39.
    Guardamagna O, Amaretti A, Puddu PE, Raimondi S, Abello F, Cagliero P, Rossi M (2014) Bifidobacteria supplementation: effects on plasma lipid profiles in dyslipidemic children. Nutrition 30(7–8):831–836 https://linkinghub.elsevier.com/retrieve/pii/S0899-9007(14)00080-X CrossRefGoogle Scholar
  40. 40.
    Pavlovic N, Stankov K, Mikov M (2012) Probiotics—interactions with bile acids and impact on cholesterol metabolism. Appl Biochem Biotechnol 168(7):1880–1895.  https://doi.org/10.1007/s12010-012-9904-4 CrossRefGoogle Scholar
  41. 41.
    Sadrzadeh-Yeganeh H, Elmadfa I, Djazayery A, Jalali M, Heshmat R, Chamary M (2010) The effects of probiotic and conventional yoghurt on lipid profile in women. Br J Nutr 103(12):1778–1783 https://www.cambridge.org/core/journals/british-journal-of-nutrition/article/effects-of-probiotic-and-conventional-yoghurt-on-lipid-profile-in-women/777D9C758EE0528E57405C3B0EFCFEC1 CrossRefGoogle Scholar
  42. 42.
    Kumar M, Rakesh S, Nagpal R, Hemalatha R, Ramakrishna A, Sudarshan V, Ramagoni R, Shujauddin M, Verma V, Kumar A, Tiwari A, Singh B, Kumar R (2013) Probiotic Lactobacillus rhamnosus GG and aloe vera gel improve lipid profiles in hypercholesterolemic rats. Nutrition 29(3):574–579 https://linkinghub.elsevier.com/retrieve/pii/S0899-9007(12)00362-0 CrossRefGoogle Scholar
  43. 43.
    Fabian E, Elmadfa I (2006) Influence of daily consumption of probiotic and conventional yoghurt on the plasma lipid profile in young healthy women. Ann Nutr Metab 50(4):387–393 https://www.karger.com/Article/Abstract/94304 CrossRefGoogle Scholar
  44. 44.
    Moroti C, Souza ML, de Rezende CM, Cavallini DC, Sivieri K (2012) Effect of the consumption of a new symbiotic shake on glycemia and cholesterol levels in elderly people with type 2 diabetes mellitus. Lipids Health Dis 11:29.  https://doi.org/10.1186/1476-511X-11-29 CrossRefGoogle Scholar
  45. 45.
    Feng LL, Wang SJ, Wang HY, et al. (2014). A study of fermented milk containing bifidobacterium LB-21on improving bowel function. Food Research and Development. (07), 111–113. http://kns.cnki.net/KCMS/detail/detail.aspx?FileName=SPYK201407031&DbName=CJFQ2014
  46. 46.
    Odamaki T, Sugahara H, Yonezawa S, Yaeshima T, Iwatsuki K, Tanabe S, Tominaga T, Togashi H, Benno Y, Xiao JZ (2012) Effect of the oral intake of yogurt containing Bifidobacterium longum BB536 on the cell numbers of enterotoxigenic Bacteroides fragilis in microbiota. Anaerobe 18(1):14–18 https://linkinghub.elsevier.com/retrieve/pii/S1075-9964(11)00206-X CrossRefGoogle Scholar
  47. 47.
    Sokol H, Jegou S, McQuitty C, Straub M, Leducq V, Landman C et al (2017) Specificities of the intestinal microbiota in patients with inflammatory bowel disease and Clostridium difficile infection. Gut Microbes:1–6.  https://doi.org/10.1080/19490976.2017.1361092?journalCode=kgmi20
  48. 48.
    Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, Possemiers S, van Holle A, François P, de Vos WM, Delzenne NM, Schrenzel J, Cani PD (2011) Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60(11):2775–2786 http://diabetes.diabetesjournals.org/content/60/11/2775.long CrossRefGoogle Scholar
  49. 49.
    Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C et al (2010) Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18(1):190–195.  https://doi.org/10.1038/oby.2009.167 CrossRefGoogle Scholar
  50. 50.
    Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1241214 http://science.sciencemag.org/content/341/6150/1241214.long CrossRefGoogle Scholar
  51. 51.
    De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A et al (2014) Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156(1–2):84–96 https://linkinghub.elsevier.com/retrieve/pii/S0092-8674(13)01550-X CrossRefGoogle Scholar
  52. 52.
    Gomes AC, Bueno AA, de Souza RG, Mota JF (2014) Gut microbiota, probiotics and diabetes. Nutr J 13:60.  https://doi.org/10.1186/1475-2891-13-60 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Ke Wang
    • 1
  • Xiaohong Yu
    • 1
  • Yi Li
    • 2
  • Yun Guo
    • 2
  • Lin Ge
    • 1
  • Fangfang Pu
    • 1
  • Xinying Ma
    • 3
  • Wenjing Cui
    • 3
  • Francesco Marrota
    • 4
  • Fang He
    • 1
    • 5
  • Ming Li
    • 1
    • 5
  1. 1.West China School of Public Health and Healthy Food Evaluation Research CenterSichuan UniversityChengduPeople’s Republic of China
  2. 2.The Health Service Center of Huayang CommunityChengduPeople’s Republic of China
  3. 3.Hebei Inatural Biotech Co. Ltd.ShijiazhuangPeople’s Republic of China
  4. 4.ReGenera R&D International for Aging Intervention and San Babila ClinicMilanItaly
  5. 5.Department of Nutrition, Food Safety and Toxicology, West China School of Public HealthSichuan UniversityChengduPeople’s Republic of China

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