Effect of multi-strain probiotics (multi-strain microbial cell preparation) on glycemic control and other diabetes-related outcomes in people with type 2 diabetes: a randomized controlled trial

European Journal of Nutrition

Volumn 56, Issue 4, 2017, Pages 1535-1550

  Firouzi, Somayyeh ^a   Majid, Hazreen Abdul ^b   Ismail, Amin ^a   Kamaruddin, Nor Azmi ^c   Barakatun Nisak, Mohd Yusof ^a  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b UNIVERSITY OF MALAYA   (Malaysia)

^c DEPARTMENT OF PHARMACOLOGY   (Malaysia)

Author keywords

Blood pressure; Glycated hemoglobin; Glycemic control; High sensitivity C reactive protein; Homeostasis model assessment estimated insulin resistance; Lipid profile; Probiotics; Type 2 diabetes mellitus

Indexed keywords

ANTIHYPERTENSIVE AGENT; ANTILIPEMIC AGENT; C REACTIVE PROTEIN; CARBOHYDRATE; CHOLESTEROL; FAT; HEMOGLOBIN A1C; INSULIN; LIPID; ORAL ANTIDIABETIC AGENT; PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT; PROTEIN; SODIUM; GLYCOSYLATED HEMOGLOBIN;

ADULT; ANTHROPOMETRIC PARAMETERS; ARTICLE; BIFIDOBACTERIUM; BLOOD PRESSURE; CLINICAL PROTOCOL; CONTROLLED STUDY; DIABETIC PATIENT; DIET RESTRICTION; DIET SUPPLEMENTATION; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; EFFECT SIZE; FEMALE; GASTROINTESTINAL TRACT; GLYCEMIC CONTROL; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; INSULIN BLOOD LEVEL; INTENTION TO TREAT ANALYSIS; LACTOBACILLUS; LIPID ANALYSIS; LIPID BLOOD LEVEL; MAJOR CLINICAL STUDY; MALAYSIA; MALE; MEDICATION COMPLIANCE; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; OUTCOME ASSESSMENT; PATIENT COMPLIANCE; RANDOMIZED CONTROLLED TRIAL; TEACHING HOSPITAL; TREATMENT DURATION; TREATMENT OUTCOME; ADMINISTRATION AND DOSAGE; AGED; BLOOD; CARBOHYDRATE DIET; DIET; EXERCISE; FAT INTAKE; GLUCOSE BLOOD LEVEL; INTESTINE FLORA; METABOLISM; PROTEIN INTAKE;

ADULT; AGED; BIFIDOBACTERIUM; BLOOD GLUCOSE; C-REACTIVE PROTEIN; DIABETES MELLITUS, TYPE 2; DIET; DIETARY CARBOHYDRATES; DIETARY FATS; DIETARY PROTEINS; DOUBLE-BLIND METHOD; EXERCISE; FEMALE; GASTROINTESTINAL MICROBIOME; GLYCATED HEMOGLOBIN A; HUMANS; INSULIN; LACTOBACILLUS; MALAYSIA; MALE; MIDDLE AGED; PROBIOTICS; TREATMENT OUTCOME;

EID: 84961197300     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-016-1199-8     Document Type: Article

References (61)

1. Guariguata L, Whiting DR, Hambleton I et al (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103:137–149. doi:10.1016/j.diabres.2013.11.002
2. Wan Nazaimoon WM, Md Isa SH, Wan Mohamad WB et al (2013) Prevalence of diabetes in Malaysia and usefulness of HbA1c as a diagnostic criterion. Diabet Med 30:825–828. doi:10.1111/dme.12161
3. Firouzi S, Barakatun-Nisak MY, Azmi KN (2015) Nutritional status, glycemic control and its associated risk factors among a sample of type 2 diabetic individuals, a pilot study. J Res Med Sci 20:40–46
4. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60. doi:10.1016/j.phrs.2012.10.020
5. Musso G, Gambino R, Cassader M (2010) Obesity, diabetes, and gut microbiota. The hygiene hypothesis expanded? Diabetes Care 33:2277–2284
6. Larsen N, Vogensen FK, van den Berg FWJ et al (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5:e9085
7. de Kort S, Keszthelyi D, Masclee AAM (2011) Leaky gut and diabetes mellitus: What is the link? Obes Rev 12:449–458. doi:10.1111/j.1467-789X.2010.00845.x
8. FAO/WHO (2002) WHO|guidelines for the evaluation of probiotics in food: joint FAO/WHO working group meeting, London Ontario, Canada, 30 April–1 May 2002. World Health Organization, London Ontario, Canada
9. Firouzi S, Barakatun-Nisak MY, Ismail A et al (2013) Role of probiotics in modulating glucose homeostasis: evidence from animal and human studies. Int J Food Sci Nutr 64:780–786. doi:10.3109/09637486.2013.775227
10. Ejtahed HS, Mohtadi Nia J, Homayouni Rad A et al (2011) The effects of probiotic and conventional yoghurt on diabetes markers and insulin resistance in type 2 diabetic patients: a randomized controlled clinical trial. Iran J Endocrinol Metab 13:1–8
11. 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 38:38–43
12. Asemi Z, Zare Z, Shakeri H et al (2013) Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 63:1–9
13. Le Chatelier E, Nielsen T, Qin J et al (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500:541–546. doi:10.1038/nature12506
14. Park S, Bae J-H (2015) Probiotics for weight loss: a systematic review and meta-analysis. Nutr Res 35:566–575. doi:10.1016/j.nutres.2015.05.008
15. Naito E, Yoshida Y, Makino K et al (2011) Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. J Appl Microbiol 110:650–657
16. Chen JJ, Wang R, Li X (2011) Bifidobacterium longum supplementation improved high-fat-fed-induced metabolic syndrome and promoted intestinal Reg I gene expression. Exp Biol Med 236:823–831
17. Jauhiainen T, Collin M, Narva M et al (2005) Effect of long-term intake of milk peptides and minerals on blood pressure and arterial function in spontaneously hypertensive rats. Milchwissenschaft-Milk Sci Int 60:358–362
18. Agerholm-Larsen L, Raben A, Haulrik N et al (2000) Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur J Clin Nutr 54:288–297
19. Guo Z, Liu XM, Zhang QX et al (2011) Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomised controlled trials. Nutr Metab Cardiovasc Dis 21:844–850
20. Malaysian Dietitians’ Association (2013) Clinical Practice Guideline, Medical nutrition therapy guideline for type 2 diabetes Mellitus. Ministry of Health, Kuala Lumpur, Malaysia
21. Cole HS, Camerini-Davalos RA (1970) Diet therapy of diabetes mellitus. Med Clin North Am 54:1577–1587
22. Krueger KP, Felkey BG, Berger BA (2003) Improving adherence and persistence: a review and assessment of interventions and description of steps toward a national adherence initiative. J Am Pharm Assoc 43:668–679
23. WHO expert consultation (2000) Obesity: preventing and managing the global epidemic Report of a WHO Consultation (WHO Technical Report Series 894). Geneva
24. Matthews DR, Hosker JP, Rudenski AS et al (1985) Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419
25. Katz A, Nambi SS, Mather K et al (2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 85:2402–2410
26. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502
27. Chu AHY, Moy FM (2012) Reliability and validity of the malay international physical activity questionnaire (IPAQ-M) among a malay population in Malaysia. Asia Pac J Public Health 27:NP2381–NP2389
28. De Vrese M, Winkler P, Rautenberg P et al (2005) Effect of Lactobacillus gasseri PA 16/8, Bifidobacterium longum SP 07/3, B. bifidum MF 20/5 on common cold episodes: a double blind, randomized, controlled trial. Clin Nutr 24:481–491. doi:10.1016/j.clnu.2005.02.006
29. Albertini B, Vitali B, Passerini N et al (2010) Development of microparticulate systems for intestinal delivery of Lactobacillus acidophilus and Bifidobacterium lactis. Eur J Pharm Sci 40:359–366. doi:10.1016/j.ejps.2010.04.011
30. Haarman M, Knol J (2006) Quantitative real-time PCR analysis of fecal Lactobacillus species in infants receiving a prebiotic infant formula. Appl Environ Microbiol 72:2359–2365. doi:10.1128/AEM.72.4.2359
31. Andreasen AS, Larsen N, Pedersen-Skovsgaard T et al (2010) Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br J Nutr 104:1831–1838
32. Laitinen K, Poussa T, Isolauri E (2009) Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br J Nutr 101:1679–1687
33. Ivey KL, Hodgson JM, Kerr DA et al (2014) The effects of probiotic bacteria on glycaemic control in overweight men and women: a randomised controlled trial. Eur J Clin Nutr 68:447–452. doi:10.1038/ejcn.2013.294
34. Gobel RJ, Larsen N, Jakobsen M et al (2012) Probiotics to obese adolescents; RCT examining the effects on inflammation and metabolic syndrome. J Pediatr Gastroenterol Nutr 5:673–678
35. Al-Salami H, Butt G, Fawcett JP et al (2008) Probiotic treatment reduces blood glucose levels and increases systemic absorption of gliclazide in diabetic rats. Eur J Drug Metab Pharmacokinet 33:101–106
36. Zhou J, Martin RJ, Tulley RT et al (2008) Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Metab 295:E1160–E1166
37. Jensen TE, Richter EA (2012) Regulation of glucose and glycogen metabolism during and after exercise. J Physiol 590:1069–1076. doi:10.1113/jphysiol.2011.224972
38. Munsters MJM, Saris WHM (2012) Effects of meal frequency on metabolic profiles and substrate partitioning in lean healthy males. PLoS ONE 7:e38632. doi:10.1371/journal.pone.0038632
39. Morton GJ, Schwartz MW (2011) Leptin and the central nervous system control of glucose metabolism. Physiol Rev 91:389–411. doi:10.1152/physrev.00007.2010
40. Burcelin R, Serino M, Chabo C et al (2011) Gut microbiota and diabetes: from pathogenesis to therapeutic perspective. Acta Diabetol 48(4):257–273
41. Pi-Sunyer FX (2005) Weight loss in type 2 diabetic patients. Diabetes Care 28:1526–1527
42. Pereira DIA, Gibson GR (2002) Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Crit Rev Biochem Mol Biol 37:259–281. doi:10.1080/10409230290771519
43. Ejtahed HS, Mohtadi Nia J, Homayouni Rad A et al (2011) Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J Dairy Sci 94:3288–3294
44. Sadrzadeh-Yeganeh H, Elmadfa I, Djazayery A et al (2010) The effects of probiotic and conventional yoghurt on lipid profile in women. Br J Nutr 103:1778–1783. doi:10.1017/S0007114509993801
45. Laakso M, Sarlund H, Salonen R et al (1991) Asymptomatic atherosclerosis and insulin resistance. Arterioscler Thromb Vasc Biol 11:1068–1076. doi:10.1161/01.ATV.11.4.1068
46. Chew BH, Ismail M, Lee PY et al (2012) Determinants of uncontrolled dyslipidaemia among adult type 2 diabetes in Malaysia: the Malaysian Diabetes Registry 2009. Diabetes Res Clin Pract 96:339–347. doi:10.1016/j.diabres.2012.01.017
47. Ooi LG, Liong MT (2010) Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int J Mol Sci 11:2499–2522. doi:10.3390/ijms11062499
48. Seppo L, Jauhiainen T, Poussa T, Korpela R (2003) A fermented milk high in bioactive peptides has a blood pressure–lowering effect in hypertensive subjects. Am J Clin Nutr 77:326
49. Ansell BJ, Watson KE, Weiss RE, Fonarow GC (2003) hsCRP and HDL effects of statins trial (CHEST): rapid effect of statin therapy on C-reactive protein and high-density lipoprotein levels A clinical investigation. Heart Dis 5:2–7. doi:10.1097/01.HDX.0000050407.62572.DE
50. Ridker PM, Danielson E, Fonseca FA et al (2009) Reduction in C-reactive protein and LDL cholesterol and cardiovascular event rates after initiation of rosuvastatin: a prospective study of the JUPITER trial. Lancet 373:1175–1182. doi:10.1016/S0140-6736(09)60447-5
51. WHO expert consultation (2004) BMI classification. http://apps.who.int/bmi/index.jsp?introPage=intro_3.html
52. Turnbaugh PJ, Hamady M, Yatsunenko T et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484. doi:10.1038/nature07540
53. Million M, Angelakis E, Maraninchi M et al (2013) Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int J Obes 37:1460–1466. doi:10.1038/ijo.2013.20
54. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249. doi:10.1038/nature11552
55. Caricilli AM, Picardi PK, de Abreu LL et al (2011) Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice. PLoS Biol 9:e1001212. doi:10.1371/journal.pbio.1001212
56. Singh B, Saxena A (2010) Surrogate markers of insulin resistance: a review. World J Diabetes 1:36–47
57. Renga B, Mencarelli A, Vavassori P et al (2010) The bile acid sensor FXR regulates insulin transcription and secretion. Biochim Biophys Acta 1802:363–372. doi:10.1016/j.bbadis.2010.01.002
58. Ding L, Yang L, Wang Z, Huang W (2015) Bile acid nuclear receptor FXR and digestive system diseases. Acta Pharm Sin B 5:135–144. doi:10.1016/j.apsb.2015.01.004
59. Shyangdan DS, Royle P, Clar C et al (2011) Glucagon-like peptide analogues for type 2 diabetes mellitus. Cochrane Database Syst Rev. doi:10.1002/14651858.CD006423.pub2
60. Tilg H, Moschen AR (2014) Microbiota and diabetes: an evolving relationship. Gut 63:1513–1521. doi:10.1136/gutjnl-2014-306928
61. Puddu A, Sanguineti R, Montecucco F, Viviani GL (2014) Evidence for the gut microbiota short-chain fatty acids as key pathophysiological molecules improving diabetes. Mediators Inflamm 2014:162021. doi:10.1155/2014/162021