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Carbohydrates, glycemic index and diabetes mellitus

The effects of probiotic bacteria on glycaemic control in overweight men and women: a randomised controlled trial

Abstract

Background/Objectives:

Evidence from animal and in vitro models suggest a role of probiotic bacteria in improving glycaemic control and delaying the onset of type 2 diabetes. However, the evidence from controlled trials in humans is limited. The objective was to determine if the probiotic bacteria L. acidophilus La5 and B. animalis subsp lactis Bb12, supplemented in a whole food (yoghurt) or isolated (capsules) form, can improve biomarkers of glycaemic control.

Subjects/methods:

Following a 3-week washout period, 156 overweight men and women over 55 years (mean age: 67±8 years; mean body mass index (31±4 kg/m2) were randomized to a 6-week double-blinded parallel study. The four intervention groups were: (A) probiotic yoghurt plus probiotic capsules; (B) probiotic yoghurt plus placebo capsules; (C) control milk plus probiotic capsules; and (D) control milk plus placebo capsules. Outcome measurements, including fasting glucose, insulin, glycated haemoglobin and Homoeostasis Model Assessment of Insulin Resistance (HOMA-IR), were performed at baseline and week 6.

Results:

Relative to the milk-control group, probiotic yoghurt resulted in a significantly higher HOMA-IR (0.32±0.15, P=0.038), but did not have a significant effect on the other three measures of glycaemic control (P>0.05). Relative to placebo capsules, probiotic capsules resulted in a significantly higher fasting glucose (0.15±0.07 mmol/l, P=0.037), with no significant effect on the other three measures of glycaemic control (P>0.05). Further analyses did not identify other variables as contributing to these adverse findings.

Conclusions:

Data from this study does not support the hypothesis that L. acidophilus La5 and B. animalis subsp lactis Bb12, either in isolated form or as part of a whole food, benefit short-term glycaemic control. Indeed, there is weak data for an adverse effect of these strains on glucose homoeostasis.

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References

  1. Pettitt D, Lisse J, Knowler W, Bennett P . Development of retinopathy and proteinuria in relation to plasma-glucose concentrations in Pima Indians. The Lancet 1980; 316: 1050–1052.

    Article  Google Scholar 

  2. Laakso M, Kuusisto J . Epidemiological evidence for the association of hyperglycaemia and atherosclerotic vascular disease in non-insulin-dependent diabetes mellitus. Ann Med 1996; 28: 415–418.

    Article  CAS  PubMed  Google Scholar 

  3. Kuusisto J, Mykkänen L, Pyörälä K, Laakso M . NIDDM and its metabolic control predict coronary heart disease in elderly subjects. Diabetes 1994; 43: 960–967.

    Article  CAS  PubMed  Google Scholar 

  4. Stratton IM, Adler AI, Neil HAW, Matthews DR, Manley SE, Cull CA et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000; 321: 405–412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Balkau B, Shipley M, Jarrett RJ, Pyörälä K, Pyörälä M, Forhan A et al. High blood glucose concentration is a risk factor for mortality in middle-aged nondiabetic men: 20-year follow-up in the Whitehall Study, the Paris Prospective Study, and the Helsinki Policemen Study. Diabetes Care 1998; 21: 360–367.

    Article  CAS  PubMed  Google Scholar 

  6. Alberti KGMM Zimmet P, Shaw J . International Diabetes Federation: a consensus on type 2 diabetes prevention. Diabet Med 2007; 24: 451–463.

    Article  Google Scholar 

  7. Drucker DJ, Nauck MA . The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. The Lancet 368: 1696–705.

  8. Rains JL, Jain SK . Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med 2011; 50: 567–575.

    Article  CAS  PubMed  Google Scholar 

  9. Kolb H, Mandrup-Poulsen T . The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation. Diabetologia 2010; 53: 10–20.

    Article  CAS  PubMed  Google Scholar 

  10. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI . Host-bacterial mutualism in the human intestine. Science 2005; 307: 1915–1920.

    Article  PubMed  Google Scholar 

  11. Larsen N, Vogensen FK, van den Berg FWJ, 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.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Furet J-P, Kong L-C, Tap J, Poitou C, Basdevant A, Bouillot J-L et al. Differential adaptation of human gut microbiota to bariatric surgery–induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 2010; 59: 3049–3057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ding S, Chi MM, Scull BP, Rigby R, Schwerbrock NMJ, Magness S et al. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One 2010; 5: e12191.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S et al. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 2010; 328: 228–231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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: 1027–1131.

    Article  PubMed  Google Scholar 

  16. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 2004; 101: 15718–15723.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Yamanaka M, Nomura T, Kametaka M . Influence of intestinal microbes on heat production in germ-free, gnotobiotic and conventional mice. J Nutr Sci Vitaminol 1977; 23: 221.

    Article  CAS  PubMed  Google Scholar 

  18. Lye H, Kuan C, Ewe J, Fung W, Liong M . The improvement of hypertension by probiotics: effects on cholesterol, diabetes, renin, and phytoestrogens. Int J Mol Sci 2009; 10: 3755–3775.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Argentina 2001.

  20. Marteau PR, Md Vrese, Cellier CJ, Schrezenmeir J . Protection from gastrointestinal diseases with the use of probiotics. Am J Clin Nutr 2001; 73: 430S–436S.

    Article  CAS  PubMed  Google Scholar 

  21. Bertolami MC, Faludi AA, Batlouni M . Evaluation of the effects of a new fermented milk product (Gaio) on primary hypercholesterolemia. Eur J Clin Nutr 1999; 53: 97.

    Article  CAS  PubMed  Google Scholar 

  22. Schaafsma G, Meuling WJ, Van Dokkum W, Bouley C . Effects of a milk product, fermented by Lactobacillus acidophilus and with fructo-oligosaccharides added, on blood lipids in male volunteers. Eur J Clin Nutr 1998; 52: 436.

    Article  CAS  PubMed  Google Scholar 

  23. Ataie-Jafari A, Larijani B, Alavi Majd H, Tahbaz F . Cholesterol-lowering effect of probiotic yogurt in comparison with ordinary yogurt in mildly to moderately hypercholesterolemic subjects. Ann Nutr Metab 2009; 54: 22–27.

    Article  CAS  PubMed  Google Scholar 

  24. Agerbaek M, Gerdes LU, Richelsen B . Hypocholesterolaemic effect of a new fermented milk product in healthy middle-aged men. Eur J Clin Nutr 1995; 49: 346–352.

    CAS  PubMed  Google Scholar 

  25. Laitinen K, Poussa T, Isolauri E . Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br J Nutr 2009; 101: 1679–1687.

    Article  CAS  PubMed  Google Scholar 

  26. 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: 62–68.

    Article  PubMed  Google Scholar 

  27. 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: 1421–1424.

    Article  CAS  PubMed  Google Scholar 

  28. Yamano T, Tanida M, Niijima A, Maeda K, Okumura N, Fukushima Y et al. Effects of the probiotic strain Lactobacillus johnsonii strain La1 on autonomic nerves and blood glucose in rats. Life Sci 2006; 79: 1963–1967.

    Article  CAS  PubMed  Google Scholar 

  29. Ljungberg M, Korpela R, Ilonen J, Ludvigsson J, Vaarala O . Probiotics for the prevention of beta cell autoimmunity in children at genetic risk of type 1 diabetes—the PRODIA study. Ann N Y Acad Sci 2006; 1079: 360–364.

    Article  PubMed  Google Scholar 

  30. Matsuzaki T, Yamazaki R, Hashimoto S, Yokokura T . Antidiabetic effects of an oral administartion of Lactobacillus casei in a non-insulin-dependent diabetes mellitus (NIDDM) model using KK-Ay mice. Endocr J 1997; 44: 357–365.

    Article  CAS  PubMed  Google Scholar 

  31. Iyer C, Kosters A, Sethi G, Kunnumakkara AB, Aggarwal BB, Versalovic J . Probiotic Lactobacillus reuteri promotes TNF-induced apoptosis in human myeloid leukemia-derived cells by modulation of NF-κB and MAPK signalling. Cell Microbiol 2008; 10: 1442–1452.

    Article  CAS  PubMed  Google Scholar 

  32. Calcinaro F, Dionisi S, Marinaro M, Candeloro P, Bonato V, Marzotti S et al. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia 2005; 48: 1565–1575.

    Article  CAS  PubMed  Google Scholar 

  33. Thomas CM, Versalovic J . Probiotics-host communication: modulation of signaling pathways in the intestine. Gut Microbes 2010; 1: 148–163.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Hodge A, Patterson AJ, Brown WJ, Ireland P, Giles G . The Anti Cancer Council of Victoria FFQ: relative validity of nutrient intakes compared with weighed food records in young to middle-aged women in a study of iron supplementation. Aust N Z Public Health 2000; 24: 576–583.

    Article  CAS  Google Scholar 

  35. Ireland P, Jolley D, Giles G, O'Dea K, Powles J, Ritishauser I et al. Development of the Melbourne FFQ: a food frequency questionnaire for use in an Australian prospective study involving an ethnically diverse cohort. Asia Pac J Clin Nutr 1994; 3: 19–31.

    CAS  PubMed  Google Scholar 

  36. Foster-Powell K, Holt SH, Brand-Miller JC . International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr 2002; 76: 5–56.

    Article  CAS  PubMed  Google Scholar 

  37. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exer 2003; 35: 1381–1395.

    Article  Google Scholar 

  38. World Health Organization. Use of glycated haemoglobin (HbA1c) in the diagnosis of diabetes mellitus. Geneva (Switzerland) 2011.

  39. Matthews D, Hosker J, Rudenski A, Naylor B, Treacher D, Turner R . Homoeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412–419.

    Article  CAS  PubMed  Google Scholar 

  40. Montgomery A, Peters T, Little P . Design, analysis and presentation of factorial randomised controlled trials. BMC Medical Research Methodology 2003; 3: 26.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Bukowska H, Pieczul-Mróz J, Jastrzebska M, Chełstowski K, Naruszewicz M . 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.

    Article  CAS  PubMed  Google Scholar 

  42. 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.

    Article  CAS  PubMed  Google Scholar 

  43. Sanggaard K, Holst J, Rehfeld J, Sandstrom B, Raben A, Tholstrup T . Different effects of whole milk and a fermented milk with the same fat and lactose content on gastric emptying and postprandial lipaemia, but not on glycaemic response and appetite. Br J Nutr 2004; 92: 447–459.

    Article  CAS  PubMed  Google Scholar 

  44. Shenderov BA . Metabiotics: novel idea or natural development of probiotic conception. Microb Ecol Health Dis 2013; 24.

  45. Savard P, Lamarche B, Paradis M-E, Thiboutot H, Laurin É, Roy D . Impact of Bifidobacterium animalis subsp. lactis BB-12 and Lactobacillus acidophilus LA-5-containing yoghurt on fecal bacterial counts of healthy adults. Int J Food Microbiol 2011; 149: 50–57.

    Article  CAS  PubMed  Google Scholar 

  46. Sonnenburg JL, Chen CTL, Genomic Gordon JI . Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 2006; 4: e413.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Louis P, Scott KP, Duncan SH, Flint HJ . Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 2007; 102: 1197–1208.

    Article  CAS  PubMed  Google Scholar 

  48. Bell A, Bauman D . Adaptations of glucose metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 1997; 2: 265–278.

    Article  CAS  PubMed  Google Scholar 

  49. Bauman DE, Bruce Currie W . Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homoeostasis and homeorhesis. J Dairy Sci 1980; 63: 1514–1529.

    Article  CAS  PubMed  Google Scholar 

  50. Kalkhoff R, Kissebah A, Kim H . Carbohydrate and lipid metabolism during normal pregnancy: relationship to gestational hormone action. Semin Perinatol 1978; 2: 291–307.

    CAS  PubMed  Google Scholar 

  51. Lye HS, Rusul G, Liong MT . Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. J Dairy Sci 2010; 93: 1383–1392.

    Article  CAS  PubMed  Google Scholar 

  52. Alander M, Mättö J, Kneifel W, Johansson M, Kögler B, Crittenden R et al. Effect of galacto-oligosaccharide supplementation on human faecal microflora and on survival and persistence of Bifidobacterium lactis Bb-12 in the gastrointestinal tract. Int Dairy J 2001; 11: 817–825.

    Article  CAS  Google Scholar 

  53. Fukushima Y, Kawata Y, Hara H, Terada A, Mitsuoka T . Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. Int J Food Microbiol 1998; 42: 39–44.

    Article  CAS  PubMed  Google Scholar 

  54. Savard P, Lamarche B, Paradis M-E, Thiboutot H, Laurin É, Roy D . Impact of Bifidobacterium animalis subsp.lactis BB-12 and Lactobacillus acidophilus LA-5-containing yoghurt, on fecal bacterial counts of healthy adults. Int J Food Microbiol 2011; 149: 50–57.

    Article  CAS  PubMed  Google Scholar 

  55. Schillinger U, Guigas C, Heinrich Holzapfel W . In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J 2005; 15: 1289–1297.

    Article  CAS  Google Scholar 

  56. Collado MC, Jalonen L, Meriluoto J, Salminen S . Protection mechanism of probiotic combination against human pathogens: in vitro adhesion to human intestinal mucus. Asia Pac J Clin Nutr 2006; 15: 570–575.

    PubMed  Google Scholar 

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Acknowledgements

The study was supported by a research grant from Sir Charles Gairdner Hospital Research Advisory Committee. Probiotic yoghurt was donated by Casa Dairy, Australia. Probiotic capsules were donated by Chr. Hansen, Australia. The salary of JRL is supported by a Raine Medical Research Foundation Priming Grant. The salary of JMH is supported by the National Health and Medical Research Council. None of these sources of support had any input into any aspect of the design and management of this study.

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Correspondence to K L Ivey.

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All work was carried out at the University of Western Australia, School of Medicine and Pharmacology, Sir Charles Gairdner Hospital Unit and the Sir Charles Gairdner Hospital, Department of Endocrinology and Diabetes.

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Ivey, K., Hodgson, J., Kerr, D. et al. The effects of probiotic bacteria on glycaemic control in overweight men and women: a randomised controlled trial. Eur J Clin Nutr 68, 447–452 (2014). https://doi.org/10.1038/ejcn.2013.294

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