Clinical application of probiotics in type 2 diabetes mellitus: A randomized, double-blind, placebo-controlled study

Clinical Nutrition

Volumn 36, Issue 1, 2017, Pages 85-92

  Tonucci, Livia Bordalo ^a   Olbrich dos Santos, Karina Maria ^b   Licursi de Oliveira, Leandro ^c   Rocha Ribeiro, Sonia Machado ^c   Duarte Martino, Hercia Stampini ^c  

^a INTA College   (Brazil)

^b EMBRAPA CERRADOS   (Brazil)

^c FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

Gut microbiota; Inflammation; Probiotics; SCFA; Stress oxidative; Type 2 diabetes

Indexed keywords

ACETIC ACID; FRUCTOSAMINE; HEMOGLOBIN A1C; INTERLEUKIN 10; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PLACEBO; PROBIOTIC AGENT; RESISTIN; SHORT CHAIN FATTY ACID; TUMOR NECROSIS FACTOR; BIOLOGICAL MARKER; CHOLESTEROL; CYTOKINE; GLYCOSYLATED HEMOGLOBIN; TRIACYLGLYCEROL; VOLATILE FATTY ACID;

ADULT; ARTICLE; BIFIDOBACTERIUM ANIMALIS; BLOOD SAMPLING; BODY COMPOSITION; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; DIET THERAPY; DOUBLE BLIND PROCEDURE; FECES ANALYSIS; FEMALE; FERMENTED MILK PRODUCT; FOLLOW UP; GLYCEMIC CONTROL; HUMAN; INFLAMMATION; LACTOBACILLUS ACIDOPHILUS; LIPID ANALYSIS; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL; TREATMENT DURATION; ANTHROPOMETRY; BLOOD; CHEMISTRY; FECES; GLUCOSE BLOOD LEVEL; METABOLISM; MICROBIOLOGY; MIDDLE AGED; TREATMENT OUTCOME;

ACETIC ACID; ADULT; ANTHROPOMETRY; BIFIDOBACTERIUM ANIMALIS; BIOMARKERS; BLOOD GLUCOSE; CHOLESTEROL; CULTURED MILK PRODUCTS; CYTOKINES; DIABETES MELLITUS, TYPE 2; DOUBLE-BLIND METHOD; FATTY ACIDS, VOLATILE; FECES; FEMALE; FOLLOW-UP STUDIES; GLYCATED HEMOGLOBIN A; HUMANS; LACTOBACILLUS ACIDOPHILUS; MALE; MIDDLE AGED; OXIDATIVE STRESS; PROBIOTICS; TREATMENT OUTCOME; TRIGLYCERIDES;

EID: 84951734603     PISSN: 02615614     EISSN: 15321983     Source Type: Journal    
DOI: 10.1016/j.clnu.2015.11.011     Document Type: Article

References (46)

1. IDF, International Diabetes Federation, (eds.) IDF diabetes atlas, 6th ed., 2013.
2. Kershaw, E.E., Flier, J.S., Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89 (2004), 2548–2556.
3. Rani, A.J., Mythili, S.V., Study on total antioxidant status in relation to oxidative stress in type 2 diabetes mellitus. J Clin Diagn Res 8 (2014), 108–110.
4. Muoio, D.M., Newgard, C.B., Molecular and metabolic mechanisms of insulin resistance and [beta]-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9 (2008), 193–205.
5. Hsieh, F.-C., Lee, C.-L., Chai, C.-Y., Chen, W.-T., Lu, Y.-C., Wu, C.-S., Oral administration of Lactobacillus reuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutr Metab, 10, 2013, 35.
6. Wang, S., Zhu, H., Lu, C., Kang, Z., Luo, Y., Feng, L., et al. Fermented milk supplemented with probiotics and prebiotics can effectively alter the intestinal microbiota and immunity of host animals. J Dairy Sci 95 (2012), 4813–4822.
7. Larsen, N., Vogensen, F.K., van den Berg, F.W.J., Nielsen, D.S., Andreasen, A.S., Pedersen, B.K., et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One, 5, 2010, e9085.
8. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
9. Karlsson, F.H., Tremaroli, V., Nookaew, I., Bergstrom, G., Behre, C.J., Fagerberg, B., et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498 (2013), 99–103.
10. Cani, P.D., Amar, J., Iglesias, M.A., Poggi, M., Knauf, C., Bastelica, D., et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 (2007), 1761–1772.
11. Cani, P.D., Lecourt, E., Dewulf, E.M., Sohet, F.M., Pachikian, B.D., Naslain, D., et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr 90 (2009), 1236–1243.
12. Psichas, A., Sleeth, M.L., Murphy, K.G., Brooks, L., Bewick, G.A., Hanyaloglu, A.C., et al. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int J Obes 39:3 (2014), 424–429.
13. Maynard, C.L., Elson, C.O., Hatton, R.D., Weaver, C.T., Reciprocal interactions of the intestinal microbiota and immune system. Nature 489 (2012), 231–241.
14. Cani, P., Neyrinck, A., Fava, F., Knauf, C., Burcelin, R., Tuohy, K., et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50 (2007), 2374–2383.
15. ADA, American diabetes association. Standards of medical care in diabetes—2014. Diabetes Care 37 (2014), S14–S80.
16. Mazloom, Z., Yousefinejad, A., Dabbaghmanesh, M.H., 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 (2013), 38–43.
17. Buriti, F.C.A., Freitas, S.C., Egito, A.S., dos Santos KMO, Effects of tropical fruit pulps and partially hydrolysed galactomannan from Caesalpinia pulcherrima seeds on the dietary fibre content, probiotic viability, texture and sensory features of goat dairy beverages. LWT Food Sci Technol 59 (2014), 196–203.
18. Peryam, D.R., Pilgrim, F.J., Hedonic scale method of measuring food preferences. Food Technol 11:Suppl. (1957), 9–14.
19. Geloneze, B., Repetto, E.M., Geloneze, S.R., Tambascia, M.A., Ermetice, M.N., The threshold value for insulin resistance (HOMA-IR) in an admixtured population IR in the Brazilian metabolic syndrome study. Diabetes Res Clin Pract 72 (2006), 219–220.
20. Vignali, D.A.A., Multiplexed particle-based flow cytometric assays. J Immunol Methods 243 (2000), 243–255.
21. Smiricky-Tjardes, M.R., Grieshop, C.M., Flickinger, E.A., Bauer, L.L., Fahey, G.C., Dietary galactooligosaccharides affect ileal and total-tract nutrient digestibility, ileal and fecal bacterial concentrations, and ileal fermentative characteristics of growing pigs. J Animal Sci 81 (2003), 2535–2545.
22. Gravitz, L., Microbiome: the critters within. Nature 485 (2012), 12–13.
23. 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 67 (2003), 1421–1424.
24. Yadav, H., Jain, S., Sinha, P., Antidiabetic effect of probiotic dahi containing lactobacillus acidophilus ans lactobacillus case I in high fructose fed rats. Nutr 23 (2007), 62–68.
25. Kang, J.-H., Yun, S.-I., Park, M.-H., Park, J.-H., Jeong, S.-Y., Park, H.-O., Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PLoS One, 8, 2013, e54617.
26. Ejtahed, H.S., Mohtadi-Nia, J., Homayouni-Rad, A., Niafar, M., Asghari-Jafarabadi, M., Mofid, V., Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutr Burbank Los Angel Cty Calif 28 (2012), 539–543.
27. Andreasen, A.S., Larsen, N., Pedersen-Skovsgaard, T., Berg, R.M.G., Møller, K., Svendsen, K.D., et al. Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br J Nutr 104 (2010), 1831–1838.
28. Asemi, Z., Zare, Z., Shakeri, H., Sabihi, S., Esmaillzadeh, A., Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 63 (2013), 1–9.
29. Asemi, Z., Khorrami-Rad, A., Alizadeh, S.-A., Shakeri, H., Esmaillzadeh, A., Effects of synbiotic food consumption on metabolic status of diabetic patients: a double-blind randomized cross-over controlled clinical trial. Clin Nutr 33 (2014), 198–203.
30. Stephens, J.W., Khanolkar, M.P., Bain, S.C., The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis 202 (2009), 321–329.
31. Wang, X., Bao, W., Liu, J., OuYang, Y.-Y., Wang, D., Rong, S., et al. Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care 36 (2013), 166–175.
32. Tuttolomondo, A., La Placa, S., Di Raimondo, D., Bellia, C., Caruso, A., Lo Sasso, B., et al. Adiponectin, resistin and IL-6 plasma levels in subjects with diabetic foot and possible correlations with clinical variables and cardiovascular co-morbidity. Cardiovasc Diabetol, 9, 2010, 50.
33. Fasshauer, M., Paschke, R., Regulation of adipocytokines and insulin resistance. Diabetologia 46 (2003), 1594–1603.
34. Magrone, T., Jirillo, E., The interaction between gut microbiota and age-related changes in immune function and inflammation. Immun Ageing, 10, 2013, 31.
35. Matsuzaki, T., Yamazaki, R., Hashimoto, S., Yokokura, T., Antidiabetic effects of an oral administration of lactobacillus case i in a non-insulin-dependent diabetes mellitus (NIDDM) model using KK-Ay mice. Endocr J 44 (1997), 357–365.
36. Martínez-Augustin, O., Rivero-Gutiérrez, B., Mascaraque, C., Sánchez de Medina, F., Food derived bioactive peptides and intestinal barrier function. Int J Mol Sci 15 (2014), 22857–22873.
37. Marcone, S., Haughton, K., Simpson, P., Belton, O., Fitzgerald, D., Milk-derived bioactive peptides inhibit human endothelial-monocyte interactions via PPAR-gamma dependent regulation of NF-kappaB. J Inflamm, 12, 2015, 1.
38. Mohamadshahi, M., Veissi, M., Haidari, F., Shahbazian, H., Kaydani, G.A., Mohammadi, F., Effects of probiotic yogurt consumption on inflammatory biomarkers in patients with type 2 diabetes. Bioimpacts 4 (2014), 83–88.
39. Kim, S.-W., Park, K.-Y., Kim, B., Kim, E., Hyun, C.-K., Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Commun 431 (2013), 258–263.
40. De Vuyst, L., Leroy, F., Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifdobacterial competitiveness, butyrate production, and gas production. Int J Food Microbiol 149 (2011), 73–80.
41. Tonucci, L.B., Santos, K.M.O., Ferreira, C.L.L.F., Ribeiro, S.M.R., Oliveira, L.L., Martino, H.S.D., Gut microbiota and probiotics: focus on diabetes mellitus. Crit Rev Food Sci Nutr, 2015, 10.1080/10408398.2014.934438.
42. Lin, H.V., Frassetto, A., Kowalik, E.J. Jr., Nawrocki, A.R., Lu, M.M., Kosinski, J.R., et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One, 7, 2012, e35240.
43. Kasubuchi, M., Hasegawa, S., Hiramatsu, T., Ichimura, A., Kimura, I., Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 7 (2015), 2839–2849.
44. Parkar, S.G., Trower, T.M., Stevenson, D.E., Fecal microbial metabolism of polyphenols and its effects on human gut microbiota. Anaerobe 23 (2013), 12–19.
45. Ejtahed, H.S., Mohtadi-Nia, J., Homayouni-Rad, A., Niafar, M., Asghari-Jafarabadi, M., Mofid, V., 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 94 (2011), 3288–3294.
46. Mohamadshahi, M., Veissi, M., Haidari, F., Javid, A.Z., Mohammadi, F., Shirbeigi, E., Effects of probiotic yogurt consumption on lipid profile in type 2 diabetic patients: a randomized controlled clinical trial. J Res Med Sci 19 (2014), 531–536.