Fermented Dairy Products, Probiotic Supplementation, and Cardiometabolic Diseases: A Systematic Review and Meta-analysis.

Fermented dairy foods (FDFs) and probiotics are promising tools for the prevention and management of cardiometabolic diseases (CMDs), respectively. The relation between the regular consumption of FDFs and CMD risk factors was assessed by prospective cohort studies (PCSs), and the effect of probiotic supplementation added into a dairy matrix on CMD parameters was evaluated by randomized controlled trials (RCTs). Moreover, the effects of probiotic supplementation added into a dairy matrix were compared with those administered in capsule/powder form. Twenty PCSs and 52 RCTs met the inclusion criteria for the systematic review and meta-analysis. In PCSs, fermented milk was associated with a 4% reduction in risk of stroke, ischemic heart disease, and cardiovascular mortality [RR (95% CI); 0.96 (0.94, 0.98)]; yogurt intake was associated with a risk reduction of 27% [RR (95% CI); 0.73 (0.70, 0.76)] for type 2 diabetes (T2D) and 20% [RR (95% CI); 0.80 (0.74, 0.87)] for metabolic syndrome development. In RCTs, probiotic supplementation added into dairy matrices produced a greater reduction in lipid biomarkers than when added into capsules/powder in hypercholesterolemic subjects, and probiotic supplementation by capsules/powder produced a greater reduction in T2D biomarkers than when added into dairy matrices in diabetic subjects. Both treatments (dairy matrix and capsules/powder) resulted in a significant reduction in anthropometric parameters in obese subjects. In summary, fermented milk consumption is associated with reduced cardiovascular risk, while yogurt intake is associated with a reduced risk of T2D and metabolic syndrome development in the general population. Furthermore, probiotic supplementation added into dairy matrices could be considered beneficial for lowering lipid concentrations and reducing anthropometric parameters. Additionally, probiotic capsule/powder supplementation could contribute to T2D management and reduce anthropometric parameters. However, these results should be interpreted with caution due to the heterogeneity of the studies and the different probiotic strains used in the studies. This trial is registered with PROSPERO (CRD42018091791) and the protocol can be accessed at http://www.crd.york.ac.uk/PROSPERO/display_record.php?ID=CRD42018091791.

[1]  ESC / EAS Guidelines for the Treatment of Dyslipidemias: Lipid Modification to Reduce Cardiovascular Risk , 2020, Digital Doctor.

[2]  M. Sabatine,et al.  2019 ESC/EAS Guidelines for the management of dyslipidaemias: lipid modification to reduce cardiovascular risk. , 2019, European heart journal.

[3]  N. Al-Daghri,et al.  Effects of a 6-month multi-strain probiotics supplementation in endotoxemic, inflammatory and cardiometabolic status of T2DM patients: A randomized, double-blind, placebo-controlled trial. , 2019, Clinical nutrition.

[4]  M. Jafarabadi,et al.  Effects of probiotic yogurt on glycemic indexes and endothelial dysfunction markers in patients with metabolic syndrome. , 2019, Nutrition.

[5]  M. Christman,et al.  Three probiotic strains exert different effects on plasma bile acid profiles in healthy obese adults: randomised, double-blind placebo-controlled crossover study. , 2019, Beneficial microbes.

[6]  J. Danesh,et al.  Consumption of meat, fish, dairy products, eggs and risk of ischemic heart disease: a prospective study of 7198 incident cases among 409,885 participants in the pan-European EPIC cohort , 2019 .

[7]  I. Johansson,et al.  Dairy Product Intake and Cardiometabolic Diseases in Northern Sweden: A 33-Year Prospective Cohort Study , 2019, Nutrients.

[8]  M. Covasa,et al.  Probiotics: How Effective Are They in the Fight against Obesity? , 2019, Nutrients.

[9]  P. Mirmiran,et al.  The effect of probiotic supplementation on glycemic control and lipid profile in patients with type 2 diabetes: A randomized placebo controlled trial. , 2019, Diabetes & metabolic syndrome.

[10]  Beitullah Alipour,et al.  The Effects of Lactobacillus casei on Glycemic Response, Serum Sirtuin1 and Fetuin-A Levels in Patients with Type 2 Diabetes Mellitus: A Randomized Controlled Trial , 2019, Iranian biomedical journal.

[11]  Kyong Park,et al.  Effects of Consuming Calcium-Rich Foods on the Incidence of Type 2 Diabetes Mellitus , 2018, Nutrients.

[12]  R. Hutkins,et al.  Yogurt and other fermented foods as sources of health-promoting bacteria. , 2018, Nutrition reviews.

[13]  Chi-Chen Lin,et al.  The beneficial effects of Lactobacillus reuteri ADR-1 or ADR-3 consumption on type 2 diabetes mellitus: a randomized, double-blinded, placebo-controlled trial , 2018, Scientific Reports.

[14]  T. Suzutani,et al.  A Double-Blind Controlled Study to Evaluate the Effects of Yogurt Enriched with Lactococcus lactis 11/19-B1 and Bifidobacterium lactis on Serum Low-Density Lipoprotein Level and Antigen-Specific Interferon-γ Releasing Ability , 2018, Nutrients.

[15]  D. Mozaffarian,et al.  Association of dairy intake with cardiovascular disease and mortality in 21 countries from five continents (PURE): a prospective cohort study , 2018, The Lancet.

[16]  R. Valls,et al.  Effects of daily consumption of the probiotic Bifidobacterium animalis subsp. lactis CECT 8145 on anthropometric adiposity biomarkers in abdominally obese subjects: a randomized controlled trial , 2018, International Journal of Obesity.

[17]  Mahsa Raji Lahiji,et al.  Effects of Probiotic Yogurt on Serum Omentin-1, Adropin, and Nesfatin-1 Concentrations in Overweight and Obese Participants Under Low-Calorie Diet , 2018, Probiotics and Antimicrobial Proteins.

[18]  T. Falalyeyeva,et al.  Effect of alive probiotic on insulin resistance in type 2 diabetes patients: Randomized clinical trial. , 2018, Diabetes & metabolic syndrome.

[19]  A. Feizi,et al.  The effects of probiotics and synbiotic supplementation on glucose and insulin metabolism in adults with prediabetes: a double-blind randomized clinical trial , 2018, Acta Diabetologica.

[20]  M. Mansournia,et al.  The effects of probiotic supplementation on metabolic status in type 2 diabetic patients with coronary heart disease , 2018, Diabetology & Metabolic Syndrome.

[21]  E. Esmerino,et al.  Probiotic Minas Frescal cheese added with L. casei 01: Physicochemical and bioactivity characterization and effects on hematological/biochemical parameters of hypertensive overweighted women – A randomized double-blind pilot trial , 2018, Journal of Functional Foods.

[22]  P. Bogdański,et al.  Dose-Dependent Effects of Multispecies Probiotic Supplementation on the Lipopolysaccharide (LPS) Level and Cardiometabolic Profile in Obese Postmenopausal Women: A 12-Week Randomized Clinical Trial , 2018, Nutrients.

[23]  K. Yamauchi,et al.  Effects of Bifidobacterium breve B-3 on body fat reductions in pre-obese adults: a randomized, double-blind, placebo-controlled trial , 2018, Bioscience of microbiota, food and health.

[24]  B. Cho,et al.  Lactobacillus gasseri BNR17 Supplementation Reduces the Visceral Fat Accumulation and Waist Circumference in Obese Adults: A Randomized, Double-Blind, Placebo-Controlled Trial. , 2018, Journal of medicinal food.

[25]  J. Hjelmesæth,et al.  Effects of probiotics on body weight, body mass index, fat mass and fat percentage in subjects with overweight or obesity: a systematic review and meta‐analysis of randomized controlled trials , 2018, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[26]  Hideki Ito,et al.  Effect of Lactobacillus casei strain Shirota-fermented milk on metabolic abnormalities in obese prediabetic Japanese men: a randomised, double-blind, placebo-controlled trial , 2017, Bioscience of microbiota, food and health.

[27]  A. Ortaglia,et al.  Design, Development and Construct Validation of the Children’s , 2018 .

[28]  S. Yakout,et al.  Effects of a multi-strain probiotic supplement for 12 weeks in circulating endotoxin levels and cardiometabolic profiles of medication naïve T2DM patients: a randomized clinical trial , 2017, Journal of Translational Medicine.

[29]  Yan Han,et al.  Effect of probiotics on lipid profiles and blood pressure in patients with type 2 diabetes , 2017, Medicine.

[30]  C. Ranadheera,et al.  Probiotic Delivery through Fermentation: Dairy vs. Non-Dairy Beverages , 2017 .

[31]  A. Tremblay,et al.  Yogurt and Cardiometabolic Diseases: A Critical Review of Potential Mechanisms. , 2017, Advances in nutrition.

[32]  C. Hampe,et al.  Probiotic strains and mechanistic insights for the treatment of type 2 diabetes , 2017, Endocrine.

[33]  J. Meigs,et al.  Associations of Dairy Intake with Incident Prediabetes or Diabetes in Middle-Aged Adults Vary by Both Dairy Type and Glycemic Status. , 2017, The Journal of nutrition.

[34]  D. Panagiotakos,et al.  Lipid-lowering nutraceuticals in clinical practice: position paper from an International Lipid Expert Panel , 2017, Nutrition reviews.

[35]  D. Panagiotakos,et al.  Lipid lowering nutraceuticals in clinical practice: position paper from an International Lipid Expert Panel# , 2017, Archives of medical science : AMS.

[36]  P. Fortina,et al.  Establishment of an orthotopic patient-derived xenograft mouse model using uveal melanoma hepatic metastasis , 2017, Journal of Translational Medicine.

[37]  C. Mottin,et al.  Weight‐loss interventions and gut microbiota changes in overweight and obese patients: a systematic review , 2017, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[38]  R. Malekzadeh,et al.  Dairy Food Intake and All-Cause, Cardiovascular Disease, and Cancer Mortality: The Golestan Cohort Study , 2017, American journal of epidemiology.

[39]  Fredrik H. Karlsson,et al.  Metabolic effects of Lactobacillus reuteri DSM 17938 in people with type 2 diabetes: A randomized controlled trial , 2017, Diabetes, obesity & metabolism.

[40]  A. Pihlanto,et al.  Health benefits of fermented foods: microbiota and beyond. , 2017, Current opinion in biotechnology.

[41]  R. Ghiasvand,et al.  Potential mechanisms linking probiotics to diabetes: a narrative review of the literature , 2017, Sao Paulo medical journal = Revista paulista de medicina.

[42]  Lei Wu,et al.  Consumption of Yogurt and the Incident Risk of Cardiovascular Disease: A Meta-Analysis of Nine Cohort Studies , 2017, Nutrients.

[43]  Hércia Stampini Duarte Martino,et al.  Clinical application of probiotics in type 2 diabetes mellitus: A randomized, double-blind, placebo-controlled study. , 2017, Clinical nutrition.

[44]  P. Prada,et al.  The additional effects of a probiotic mix on abdominal adiposity and antioxidant Status: A double‐blind, randomized trial , 2017, Obesity.

[45]  M. Mazidi,et al.  Impact of Probiotic Administration on Serum C-Reactive Protein Concentrations: Systematic Review and Meta-Analysis of Randomized Control Trials , 2017, Nutrients.

[46]  Ramamurthy,et al.  Effect of Probiotic Microbial Cell Preparation (MCP) on Fasting Blood Glucose, Body Weight, Waist Circumference, and Faecal Short Chain Fatty Acids among Overweight Malaysian Adults: A Pilot Randomised Controlled Trial of 4 Weeks , 2017 .

[47]  Jihye Kim,et al.  Dairy consumption is associated with a lower incidence of the metabolic syndrome in middle-aged and older Korean adults: the Korean Genome and Epidemiology Study (KoGES). , 2017, The British journal of nutrition.

[48]  A. Marette,et al.  Potential Health Benefits of Combining Yogurt and Fruits Based on Their Probiotic and Prebiotic Properties. , 2017, Advances in nutrition.

[49]  M. Martínez-González,et al.  Associations between Yogurt Consumption and Weight Gain and Risk of Obesity and Metabolic Syndrome: A Systematic Review. , 2017, Advances in nutrition.

[50]  A. Sanagoo,et al.  The Effect of Probiotic Yogurt on Blood Glucose and cardiovascular Biomarkers in Patients with Type II Diabetes: A Randomized Controlled Trial , 2017 .

[51]  N. Kamaruddin,et al.  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 , 2017, European Journal of Nutrition.

[52]  I. González-molero,et al.  Actualización de probióticos, prebióticos y simbióticos en nutrición clínica , 2016 .

[53]  A. Sahebkar,et al.  Lipid-modifying effects of nutraceuticals: An evidence-based approach. , 2016, Nutrition.

[54]  B. Lamarche,et al.  Systematic Review of the Association between Dairy Product Consumption and Risk of Cardiovascular-Related Clinical Outcomes , 2016, Advances in nutrition.

[55]  G. Olveira,et al.  An update on probiotics, prebiotics and symbiotics in clinical nutrition. , 2016, Endocrinologia y nutricion : organo de la Sociedad Espanola de Endocrinologia y Nutricion.

[56]  A. Tremblay,et al.  The Potential Role of Yogurt in Weight Management and Prevention of Type 2 Diabetes , 2016, Journal of the American College of Nutrition.

[57]  Xin Li,et al.  Effect of probiotics on metabolic profiles in type 2 diabetes mellitus , 2016, Medicine.

[58]  G. N. Costa,et al.  Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: A randomized trial. Effects of probiotics on metabolic syndrome. , 2016, Nutrition.

[59]  Shota Takahashi,et al.  Effect of Bifidobacterium animalis ssp. lactis GCL2505 on visceral fat accumulation in healthy Japanese adults: a randomized controlled trial , 2016, Bioscience of microbiota, food and health.

[60]  J. Geleijnse,et al.  Consumption of dairy foods and diabetes incidence: a dose-response meta-analysis of observational studies. , 2016, The American journal of clinical nutrition.

[61]  M. Noda,et al.  Antiobesity effect of Pediococcus pentosaceus LP28 on overweight subjects: a randomized, double-blind, placebo-controlled clinical trial , 2016, European Journal of Clinical Nutrition.

[62]  R. Malekzadeh,et al.  Comparison of the effect of daily consumption of probiotic compared with low-fat conventional yogurt on weight loss in healthy obese women following an energy-restricted diet: a randomized controlled trial. , 2016, The American journal of clinical nutrition.

[63]  Seong-Tshool Hong,et al.  Intestinal removal of free fatty acids from hosts by Lactobacilli for the treatment of obesity , 2016, FEBS open bio.

[64]  Y. Ishida,et al.  Effect of fragmented Lactobacillus amylovorus CP1563 on lipid metabolism in overweight and mildly obese individuals: a randomized controlled trial , 2016, Microbial ecology in health and disease.

[65]  Daniela Cardoso Umbelino Cavallini,et al.  Probiotic Soy Product Supplemented with Isoflavones Improves the Lipid Profile of Moderately Hypercholesterolemic Men: A Randomized Controlled Trial , 2016, Nutrients.

[66]  J. M. Carrión,et al.  A randomized clinical trial evaluating a proprietary mixture of Lactobacillus plantarum strains for lowering cholesterol1 , 2016 .

[67]  D. Corella,et al.  Dairy product consumption and risk of type 2 diabetes in an elderly Spanish Mediterranean population at high cardiovascular risk , 2016, European Journal of Nutrition.

[68]  Minkyung Kim,et al.  Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduced body adiposity and Lp-PLA2 activity in overweight subjects , 2015 .

[69]  M. Mochizuki,et al.  Meta-Analysis: Effects of Probiotic Supplementation on Lipid Profiles in Normal to Mildly Hypercholesterolemic Individuals , 2015, PloS one.

[70]  M. Rafraf,et al.  Probiotic yogurt improves body mass index and fasting insulin levels without affecting serum leptin and adiponectin levels in non-alcoholic fatty liver disease (NAFLD) , 2015 .

[71]  J. Martínez,et al.  Consumption of Yogurt, Low-Fat Milk, and Other Low-Fat Dairy Products Is Associated with Lower Risk of Metabolic Syndrome Incidence in an Elderly Mediterranean Population. , 2015, The Journal of nutrition.

[72]  E. Le Chatelier,et al.  Dietary modulation of the gut microbiota – a randomised controlled trial in obese postmenopausal women , 2015, British Journal of Nutrition.

[73]  Sunmin Park,et al.  Probiotics for weight loss: a systematic review and meta-analysis. , 2015, Nutrition research.

[74]  T. Odamaki,et al.  Oral administration of Bifidobacterium breve B-3 modifies metabolic functions in adults with obese tendencies in a randomised controlled trial , 2015, Journal of Nutritional Science.

[75]  M. Orho-Melander,et al.  Food sources of fat may clarify the inconsistent role of dietary fat intake for incidence of type 2 diabetes. , 2015, The American journal of clinical nutrition.

[76]  S. Rerksuppaphol,et al.  A Randomized Double-blind Controlled Trial of Lactobacillus acidophilus Plus Bifidobacterium bifidum versus Placebo in Patients with Hypercholesterolemia. , 2015, Journal of clinical and diagnostic research : JCDR.

[77]  A. Martí,et al.  Association between yogurt consumption and the risk of Metabolic Syndrome over 6 years in the SUN study , 2015, BMC Public Health.

[78]  M. Mobasseri,et al.  Effect of Probiotic Fermented Milk (Kefir) on Glycemic Control and Lipid Profile In Type 2 Diabetic Patients: A Randomized Double-Blind Placebo-Controlled Clinical Trial , 2015, Iranian journal of public health.

[79]  A. Vaag,et al.  Effects of 12 weeks of treatment with fermented milk on blood pressure, glucose metabolism and markers of cardiovascular risk in patients with type 2 diabetes: a randomised double-blind placebo-controlled study. , 2014, European journal of endocrinology.

[80]  D. Kerr,et al.  The effect of yoghurt and its probiotics on blood pressure and serum lipid profile; a randomised controlled trial. , 2015, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[81]  O. Franco,et al.  Dairy products and the risk of stroke and coronary heart disease: the Rotterdam Study , 2015, European Journal of Nutrition.

[82]  J. Manson,et al.  Dairy consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis , 2014, BMC Medicine.

[83]  M. Chamari,et al.  Effects of Probiotic Yogurt on Fat Distribution and Gene Expression of Proinflammatory Factors in Peripheral Blood Mononuclear Cells in Overweight and Obese People with or without Weight-Loss Diet , 2014, Journal of the American College of Nutrition.

[84]  M. Martínez-González,et al.  Yogurt consumption, weight change and risk of overweight/obesity: the SUN cohort study. , 2014, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[85]  Majid Mohamadshahi,et al.  Effects of probiotic yogurt consumption on inflammatory biomarkers in patients with type 2 diabetes , 2014, BioImpacts : BI.

[86]  Majid Mohamadshahi,et al.  Effects of probiotic yogurt consumption on lipid profile in type 2 diabetic patients: A randomized controlled clinical trial , 2014, Journal of research in medical sciences : the official journal of Isfahan University of Medical Sciences.

[87]  S. Madsbad.  The role of glucagon‐like peptide‐1 impairment in obesity and potential therapeutic implications , 2014, Diabetes, obesity & metabolism.

[88]  W. Garvey,et al.  The Progression of Cardiometabolic Disease: Validation of a New Cardiometabolic Disease Staging System Applicable to Obesity , 2013, Obesity.

[89]  M. Chamari,et al.  Lactobacillus acidophilus La5, Bifidobacterium BB12, and Lactobacillus casei DN001 modulate gene expression of subset specific transcription factors and cytokines in peripheral blood mononuclear cells of obese and overweight people. , 2013, BioFactors.

[90]  O. A. Plotnikova,et al.  Hypocaloric diet supplemented with probiotic cheese improves body mass index and blood pressure indices of obese hypertensive patients - a randomized double-blind placebo-controlled pilot study , 2013, Nutrition Journal.

[91]  J. Geleijnse,et al.  Dairy product intake in relation to glucose regulation indices and risk of type 2 diabetes. , 2013, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[92]  S. Rane,et al.  Beneficial Metabolic Effects of a Probiotic via Butyrate-induced GLP-1 Hormone Secretion* , 2013, The Journal of Biological Chemistry.

[93]  Masao Sato,et al.  Effect of Lactobacillus gasseri SBT2055 in fermented milk on abdominal adiposity in adults in a randomised controlled trial , 2013, British Journal of Nutrition.

[94]  Han-Oh Park,et al.  Effect of Lactobacillus gasseri BNR17 on Overweight and Obese Adults: A Randomized, Double-Blind Clinical Trial , 2013, Korean journal of family medicine.

[95]  M. Dabbaghmanesh,et al.  Effect of Probiotics on Lipid Profile, Glycemic Control, Insulin Action, Oxidative Stress, and Inflammatory Markers in Patients with Type 2 Diabetes: A Clinical Trial , 2013, Iranian journal of medical sciences.

[96]  J. Geleijnse,et al.  Consumption of dairy products and associations with incident diabetes, CHD and mortality in the Whitehall II study. , 2013, The British journal of nutrition.

[97]  Maria Kechagia,et al.  Health Benefits of Probiotics: A Review , 2013, ISRN nutrition.

[98]  S. Prakash,et al.  Lactobacillus fermentum and Lactobacillus amylovorus as probiotics alter body adiposity and gut microflora in healthy persons , 2013 .

[99]  S. Prakash,et al.  Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial , 2012, European Journal of Clinical Nutrition.

[100]  J. Shaw,et al.  The association between dairy food intake and the incidence of diabetes in Australia: the Australian Diabetes Obesity and Lifestyle Study (AusDiab) , 2012, Public Health Nutrition.

[101]  M. Asghari-Jafarabadi,et al.  Probiotic yogurt improves antioxidant status in type 2 diabetic patients. , 2012, Nutrition.

[102]  J. Manson,et al.  A diet high in low-fat dairy products lowers diabetes risk in postmenopausal women. , 2011, The Journal of nutrition.

[103]  D. D. de Luis,et al.  Effect of a probiotic on liver aminotransferases in nonalcoholic fatty liver disease patients: a double blind randomized clinical trial. , 2011, European review for medical and pharmacological sciences.

[104]  M. Orho-Melander,et al.  Dairy products and its association with incidence of cardiovascular disease: the Malmö diet and cancer cohort , 2011, European Journal of Epidemiology.

[105]  R. Goldbohm,et al.  Dairy consumption and 10-y total and cardiovascular mortality: a prospective cohort study in the Netherlands. , 2011, The American journal of clinical nutrition.

[106]  Lawrence Joseph,et al.  The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. , 2010, Journal of the American College of Cardiology.

[107]  K. Imaizumi,et al.  Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial , 2010, European Journal of Clinical Nutrition.

[108]  J. Ioannidis,et al.  The PRISMA Statement for Reporting Systematic Reviews and Meta-Analyses of Studies That Evaluate Health Care Interventions: Explanation and Elaboration , 2009, Annals of Internal Medicine [serial online].

[109]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

[110]  K. Heller.  Probiotic bacteria in fermented foods: product characteristics and starter organisms. , 2001, The American journal of clinical nutrition.