PDF (2.1 MB)
Collect
Submit Manuscript
Review Article | Open Access

Effects of probiotics, prebiotics and synbiotics supplementation on cardiovascular risk factors in patients with type 2 diabetes mellitus: a GRADE-assessed systematic review and meta-analysis of randomized controlled trials

Yanyan TianaJiayue XiaaLihua LibLigang Yanga()Hua XiaocGuoping GaocYuanyuan WangaChen ZhangaTiange BudGuiju Suna()
Key Laboratory of Environmental Medicine and Engineering of Ministry of Education, Department of Nutrition and Food Hygiene, School of Public Health, Southeast University, Nanjing 210009, China
Lianshui People’s Hospital Affiliated to Kangda College of Nanjing Medical University, Huai’an 223400, China
Gong’an County People’s Hospital, Jingzhou 434300, China
Department of Nutritional Sciences, University of Toronto, Toronto M5S 1A1, Canada

Peer review under responsibility of Beijing Academy of Food Sciences.

Show Author Information

Abstract

A systematic review and meta-analysis study was conducted to assess the effectiveness of probiotic/prebiotic/synbiotic supplementation on the effects of cardiovascular risk factors in patients with type 2 diabetes mellitus (T2DM) based on data from randomized controlled trials (RCTs). We searched electronic databases including PubMed, Cochrane Library, Embase, and Web of Science to identify clinical trials published up to 31 March 2023. Data was pooled using a random-effects model if significant heterogeneity (I² > 50%), otherwise use a fixed-effects model. Fifty-six trials that included 3317 patients were enrolled for analysis. Meta-analysis reported that probiotic/prebiotic/synbiotic supplementation significantly reduced systolic blood pressure (SBP) (weighted mean difference (WMD): −3.57 mmHg, 95% confidence interval (CI): −5.36, −1.78; P = 0.000), diastolic blood pressure (DBP) (WMD: −2.05 mmHg, 95% CI: −3.07, −1.04; P = 0.000), triglycerides (TG) (WMD: −16.10 mg/dL, 95% CI: −20.16, −12.05; P = 0.000), total cholesterol (TC) (WMD: −14.00 mg/dL, 95% CI: −20.46, −7.55; P = 0.000), low-density lipoprotein cholesterol (LDL-C) (WMD: −7.03 mg/dL, 95% CI: −9.25, −4.81; P = 0.000), fasting plasma glucose (FPG) (WMD: −16.57 mg/dL, 95% CI: −20.39, −12.74; P = 0.000), hemoglobin A1c (HbA1c) (WMD: −0.44%, 95% CI: −0.68, −0.20; P = 0.000), insulin (standardized mean difference (SMD): −0.37, 95% CI: −0.53, −0.21; P = 0.000), homeostatic model assessment of insulin resistance (HOMA-IR) (WMD: −1.05, 95% CI: −1.56, −0.54; P = 0.000), C-reactive protein (CRP) (SMD: −0.35, 95% CI: −0.57, −0.13; P = 0.002), tumor necrosis factor-α (TNF-α) (SMD: −1.07, 95% CI: −1.57, −0.56; P = 0.000), interleukin-6 (IL-6) (SMD: −0.37, 95% CI: −0.61, −0.13; P = 0.003) levels, they also increased the high-density lipoprotein cholesterol (HDL-C) (WMD: 3.70 mg/dL, 95% CI: 1.80, 5.60; P = 0.000) levels in T2DM patients, as compared to the placebo groups. This meta-analysis supports the use of probiotic/prebiotic/synbiotic supplementation as an adjunctive therapy to improve blood pressure, glycemic control parameters, lipid profile and inflammatory markers in patients with T2DM, which are well-known cardiovascular risk factors.

Electronic Supplementary Material

Download File(s)
fshw-14-1-9250002_ESM.doc (4 MB)

References

[1]

M.A. Nauck, J. Wefers, J.J. Meier, Treatment of type 2 diabetes: challenges, hopes, and anticipated successes, Lancet Diabetes Endocrinol. 9 (2021) 525-544. http://doi.org/10.1016/s2213-8587(21)00113-3.

[2]

American Diabetes Association Professional Practice Committee, 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2022, Diabetes Care 45 (2022) S17-S38. http://doi.org/10.2337/dc22-S002.

[3]

P. Toejing, N. Khampithum, S. Sirilun, et al., Influence of Lactobacillus paracasei HⅡ01 supplementation on glycemia and inflammatory biomarkers in type 2 diabetes: a randomized clinical trial, Foods 10 (2021) 1455. http://doi.org/10.3390/foods10071455.

[4]

C. Gérard, H. Vidal, Impact of gut microbiota on host glycemic control, Front. Endocrinol. 10 (2019) 29. http://doi.org/10.3389/fendo.2019.00029.

[5]

J.R. Petrie, T.J. Guzik, R.M. Touyz, Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms, Can. J. Cardiol. 34 (2018) 575-584. http://doi.org/10.1016/j.cjca.2017.12.005.

[6]

N. Sarwar, P. Gao, S.R. Seshasai, et al., Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies, Lancet 375 (2010) 2215-2222. http://doi.org/10.1016/s0140-6736(10)60484-9.

[7]

N.D. Wong, N. Sattar, Cardiovascular risk in diabetes mellitus: epidemiology, assessment and prevention, Nat. Rev. Cardiol. 20 (2023) 685-695. http://doi.org/10.1038/s41569-023-00877-z.

[8]

N. Naderpoor, A. Mousa, L.F. Gomez-Arango, et al., Faecal microbiota are related to insulin sensitivity and secretion in overweight or obese adults, J. Clin. Med. 8 (2019) 452. http://doi.org/10.3390/jcm8040452.

[9]

A. Vrieze, E. van Nood, F. Holleman, et al., Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome, Gastroenterology 143 (2012) 913-916. http://doi.org/10.1053/j.gastro.2012.06.031.

[10]

R.S. Kootte, E. Levin, J. Salojärvi, et al., Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition, Cell Metab. 26 (2017) 611-619. http://doi.org/10.1016/j.cmet.2017.09.008.

[11]

S. Mahboobi, F. Rahimi, S. Jafarnejad, Effects of prebiotic and synbiotic supplementation on glycaemia and lipid profile in type 2 diabetes: a meta-analysis of randomized controlled trials, Adv. Pharm. Bull. 8 (2018) 565-574. http://doi.org/10.15171/apb.2018.065.

[12]

M.A. Jafarabadi, A. Dehghani, L. Khalili, et al., A meta-analysis of randomized controlled trials of the effect of probiotic food or supplement on glycemic response and body mass index in patients with type 2 diabetes, updating the evidence, Curr. Diabetes Rev. 17 (2021) 356-364. http://doi.org/10.2174/1573399816666200812151029.

[13]

R.S. Madempudi, J.J. Ahire, J. Neelamraju, et al., Efficacy of UB0316, a multi-strain probiotic formulation in patients with type 2 diabetes mellitus: a double blind, randomized, placebo controlled study, PLoS One 14 (2019) e0225168. http://doi.org/10.1371/journal.pone.0225168.

[14]

C. Wang, C. Zhang, S. Li, et al., Effects of probiotic supplementation on dyslipidemia in type 2 diabetes mellitus: a meta-analysis of randomized controlled trials, Foods 9 (2020) 1540. http://doi.org/10.3390/foods9111540.

[15]

M. Yadav, N.S. Chauhan, Microbiome therapeutics: exploring the present scenario and challenges, Gastroenterol. Rep. 10 (2022) goab046. http://doi.org/10.1093/gastro/goab046.

[16]

D. Davani-Davari, M. Negahdaripour, I. Karimzadeh, et al., Prebiotics: definition, types, sources, mechanisms, and clinical applications, Foods 8 (2019) 92. http://doi.org/10.3390/foods8030092.

[17]

K.S. Swanson, G.R. Gibson, R. Hutkins, et al., The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics, Nat. Rev. Gastroenterol. Hepatol. 17 (2020) 687-701. http://doi.org/10.1038/s41575-020-0344-2.

[18]

L. Huang, C. Thonusin, N. Chattipakorn, et al., Impacts of gut microbiota on gestational diabetes mellitus: a comprehensive review, Eur. J. Nutr. 60 (2021) 2343-2360. http://doi.org/10.1007/s00394-021-02483-6.

[19]

H.Y. Li, D.D. Zhou, R.Y. Gan, et al., Effects and mechanisms of probiotics, prebiotics, synbiotics, and postbiotics on metabolic diseases targeting gut microbiota: a narrative review, Nutrients 13 (2021) 3211. http://doi.org/10.3390/nu13093211.

[20]

L. Fontana, M. Bermudez-Brito, J. Plaza-Diaz, et al., Sources, isolation, characterisation and evaluation of probiotics, Br. J. Nutr. 109(Suppl 2) (2013) S35-S50. http://doi.org/10.1017/s0007114512004011.

[21]

K. Halloran, M.A. Underwood, Probiotic mechanisms of action, Early Hum. Dev. 135 (2019) 58-65. http://doi.org/10.1016/j.earlhumdev.2019.05.010.

[22]

Y.A. Kim, J.B. Keogh, P.M. Clifton, Probiotics, prebiotics, synbiotics and insulin sensitivity, Nutr. Res. Rev. 31 (2018) 35-51. http://doi.org/10.1017/s095442241700018x.

[23]

A. Everard, V. Lazarevic, M. Derrien, et al., Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice, Diabetes 60 (2011) 2775-2786. http://doi.org/10.2337/db11-0227.

[24]

K. Naseri, S. Saadati, F. Ghaemi, et al., The effects of probiotic and synbiotic supplementation on inflammation, oxidative stress, and circulating adiponectin and leptin concentration in subjects with prediabetes and type 2 diabetes mellitus: a GRADE-assessed systematic review, meta-analysis, and meta-regression of randomized clinical trials, Eur. J. Nutr. 62 (2023) 543-561. http://doi.org/10.1007/s00394-022-03012-9.

[25]

M.J. Page, J.E. McKenzie, P.M. Bossuyt, et al., The PRISMA 2020 statement: an updated guideline for reporting systematic reviews, PLoS Med. 18 (2021) e1003583. http://doi.org/10.1371/journal.pmed.1003583.

[26]

S. Minozzi, K. Dwan, F. Borrelli, et al., Reliability of the revised Cochrane risk-of-bias tool for randomised trials (RoB2) improved with the use of implementation instruction, J. Clin. Epidemiol. 141 (2022) 99-105. http://doi.org/10.1016/j.jclinepi.2021.09.021.

[27]

G.H. Guyatt, A.D. Oxman, G.E. Vist, et al., GRADE: an emerging consensus on rating quality of evidence and strength of recommendations, Brit. Med. J. 336 (2008) 924-926. http://doi.org/10.1136/bmj.39489.470347.ad.

[28]

S.P. Hozo, B. Djulbegovic, I. Hozo, Estimating the mean and variance from the median, range, and the size of a sample, BMC Med. Res. Methodol. 5 (2005) 13. http://doi.org/10.1186/1471-2288-5-13.

[29]

L.A. Brondani, T.S. Assmann, B.M. de Souza, et al., Meta-analysis reveals the association of common variants in the uncoupling protein (UCP) 1-3 genes with body mass index variability, PLoS One 9 (2014) e96411. http://doi.org/10.1371/journal.pone.0096411.

[30]

H. Zahedi, S. Djalalinia, O. Sadeghi, et al., Dietary inflammatory potential score and risk of breast cancer: systematic review and meta-analysis, Clin. Breast Cancer 18 (2018) e561-e570. http://doi.org/10.1016/j.clbc.2018.01.007.

[31]

N. Takeshima, T. Sozu, A. Tajika, et al., Which is more generalizable, powerful and interpretable in meta-analyses, mean difference or standardized mean difference?, BMC Med. Res. Methodol. 14 (2014) 30. http://doi.org/10.1186/1471-2288-14-30.

[32]

I. Bakbergenuly, D.C. Hoaglin, E. Kulinskaya, On the Q statistic with constant weights for standardized mean difference, Br. J. Math. Stat. Psychol. 75 (2022) 444-465. http://doi.org/10.1111/bmsp.12263.

[33]

A. Hasanpour, S. Babajafari, S.M. Mazloomi, et al., The effects of soymilk plus probiotics supplementation on cardiovascular risk factors in patients with type 2 diabetes mellitus: a randomized clinical trial, BMC Endocr. Disord. 23 (2023) 36. http://doi.org/10.1186/s12902-023-01290-w.

[34]

L. Khalili, B. Alipour, M. Asghari Jafarabadi, et al., Probiotic assisted weight management as a main factor for glycemic control in patients with type 2 diabetes: a randomized controlled trial, Diabetol. Metab. Syndr. 11 (2019) 5. http://doi.org/10.1186/s13098-019-0400-7.

[35]

E. Razmpoosh, A. Javadi, H.S. Ejtahed, et al., The effect of probiotic supplementation on glycemic control and lipid profile in patients with type 2 diabetes: a randomized placebo controlled trial, Diabetes Metab. Synd. 13 (2019) 175-182. http://doi.org/10.1016/j.dsx.2018.08.008.

[36]

S. Sabico, A. Al-Mashharawi, N.M. 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, Endocr. Rev. 38 (2019) 1561-1569. http://doi.org/10.1016/j.clnu.2018.08.009.

[37]

S. Firouzi, H.A. Majid, A. Ismail, 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, Eur. J. Nutr. 56 (2017) 1535-1550. http://doi.org/10.1007/s00394-016-1199-8.

[38]

F. Bahmani, M. Tajadadi-Ebrahimi, F. Kolahdooz, et al., The consumption of synbiotic bread containing Lactobacillus sporogenes and inulin affects nitric oxide and malondialdehyde in patients with type 2 diabetes mellitus: randomized, double-blind, placebo-controlled trial, J. Am. Coll. Nutr. 35 (2016) 506-513. http://doi.org/10.1080/07315724.2015.1032443.

[39]

K.D. Hove, C. Brøns, K. Færch, 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, Eur. J. Endocrinol. 172 (2015) 11-20. http://doi.org/10.1530/EJE-14-0554.

[40]

M. Hariri, R. Salehi, A. Feizi, et al., The effect of probiotic soy milk and soy milk on anthropometric measures and blood pressure in patients with type Ⅱ diabetes mellitus: a randomized double-blind clinical trial, Arya Atheroscler. 11 (2015) 74-80.

[41]

M. Tajadadi-Ebrahimi, F. Bahmani, H. Shakeri, et al., Effects of daily consumption of synbiotic bread on insulin metabolism and serum high-sensitivity C-reactive protein among diabetic patients: a double-blind, randomized, controlled clinical trial, Ann. Nutr. Metab. 65 (2014) 34-41. http://doi.org/10.1159/000365153.

[42]

M. Mohamadshahi, M. Veissi, F. Haidari, et al., 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.

[43]

M.A. Farhangi, P. Dehghan, N. Namazi, Prebiotic supplementation modulates advanced glycation end-products (AGEs), soluble receptor for AGEs (sRAGE), and cardiometabolic risk factors through improving metabolic endotoxemia: a randomized-controlled clinical trial, Eur. J. Nutr. 59 (2020) 3009-3021. http://doi.org/10.1007/s00394-019-02140-z.

[44]

A. Ghafouri, M. Zarrati, F. Shidfar, et al., Effect of synbiotic bread containing lactic acid on glycemic indicators, biomarkers of antioxidant status and inflammation in patients with type 2 diabetes: a randomized controlled trial, Diabetes Metab. Synd. 11 (2019) 103. http://doi.org/10.1186/s13098-019-0496-9.

[45]

Z. Ebrahimi, E. Nasli-Esfahani, A. Nadjarzade, et al., Effect of symbiotic supplementation on glycemic control, lipid profiles and microalbuminuria in patients with non-obese type 2 diabetes: a randomized, double-blind, clinical trial, J. Diabetes Metab. Dis. 16 (2017) 23. http://doi.org/10.1186/s40200-017-0304-8.

[46]

Z. Asemi, M.H. Aarabi, M. Hajijafari, et al., Effects of synbiotic food consumption on serum minerals, liver enzymes, and blood pressure in patients with type 2 diabetes: a double-blind randomized cross-over controlled clinical trial, Int. J. Prev. Med. 8 (2017) 43. http://doi.org/10.4103/ijpvm.IJPVM_257_16.

[47]

Z. Asemi, S.A. Alizadeh, K. Ahmad, et al., Effects of β-carotene fortified synbiotic food on metabolic control of patients with type 2 diabetes mellitus: a double-blind randomized cross-over controlled clinical trial, Clin. Nutr. 35 (2016) 819-825. http://doi.org/10.1016/j.clnu.2015.07.009.

[48]

P. Dehghan, M.A. Farhangi, F. Tavakoli, et al., Impact of prebiotic supplementation on T-cell subsets and their related cytokines, anthropometric features and blood pressure in patients with type 2 diabetes mellitus: a randomized placebo-controlled trial, Complement. Ther. Med. 24 (2016) 96-102. http://doi.org/10.1016/j.ctim.2015.12.010.

[49]

A. Aliasgharzadeh, P. Dehghan, B.P. Gargari, et al., Resistant dextrin, as a prebiotic, improves insulin resistance and inflammation in women with type 2 diabetes: a randomised controlled clinical trial, Brit. J. Nutr. 113 (2015) 321-330. http://doi.org/10.1017/S0007114514003675.

[50]

M. Mohamadshahi, M. Veissi, F. Haidari, et al., Effects of probiotic yogurt consumption on inflammatory biomarkers in patients with type 2 diabetes, BioImpacts 4 (2014) 83-88. http://doi.org/10.5681/bi.2014.007.

[51]

Z. Asemi, Z. Zare, H. Shakeri, et al., 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. http://doi.org/10.1159/000349922.

[52]

L. Khalili, B. Alipour, M. Asghari Jafar-Abadi, 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, Iran. Biomed. J. 23 (2019) 68-77. http://doi.org/10.29252/.23.1.68.

[53]

R. Mobini, V. Tremaroli, M. Ståhlman, et al., Metabolic effects of Lactobacillus reuteri DSM 17938 in people with type 2 diabetes: a randomized controlled trial, Diabetes Obes. Metab. 19 (2017) 579-589. http://doi.org/10.1111/dom.12861.

[54]

P. Hosseinzadeh, M.H. Javanbakht, S.A. Mostafavi, et al., Brewer’s yeast improves glycemic indices in type 2 diabetes mellitus, Int. J. Prev. Med. 4 (2013) 1131-1138.

[55]

J. Sato, A. Kanazawa, K. Azuma, et al., Probiotics reduce bacterial translocation in Japanese patients with type 2 diabetes mellitus, Diabetes 66 (2017) A352.

[56]

M. Tajabadi-Ebrahimi, Erratum: a randomized controlled clinical trial investigating the effect of synbiotic administration on markers of insulin metabolism and lipid profiles in overweight type 2 diabetic patients with coronary heart disease, Exp. Clin. Endocr. Diab. 125 (2017) E2. http://doi.org/10.1055/a-1736-9432.

[57]

N. Rustanti, A. Murdiati, M. Juffrie, et al., Effect of probiotic Lactobacillus plantarum Dad-13 on metabolic profiles and gut microbiota in type 2 diabetic women: a randomized double-blind controlled trial, Microorganisms 10 (2022) 1806. http://doi.org/10.3390/microorganisms10091806.

[58]

N. Alihosseini, S.A. Moahboob, N. Farrin, et al., Effect of probiotic fermented milk (KEFIR) on serum level of insulin and homocysteine in type 2 diabetes patients, Acta. Endocrinol-Buch. 13 (2017) 431-436. http://doi.org/10.4183/aeb.2017.431.

[59]

Z. Asemi, S. Bahmani, H. Shakeri, et al., Effect of multispecies probiotic supplements on serum minerals, liver enzymes and blood pressure in patients with type 2 diabetes, Int. J. Diabetes Dev. Ctries. 35 (2015) 90-95. http://doi.org/10.1007/s13410-013-0187-2.

[60]

N. Djaja, I. Permadi, F. Witjaksono, et al., The effect of Job’s tears-enriched yoghurt on GLP-1, calprotectin, blood glucose levels and weight of patients with type 2 diabetes mellitus, Med. J. Nutrition Metab. 12 (2019) 163-171. http://doi.org/10.3233/MNM-180258.

[61]

M.A. Farhangi, A.Z. Javid, P. Dehghan, The effect of enriched chicory inulin on liver enzymes, calcium homeostasis and hematological parameters in patients with type 2 diabetes mellitus: a randomized placebo-controlled trial, Prim. Care Diabetes 10 (2016) 265-271. http://doi.org/10.1016/j.pcd.2015.10.009.

[62]

A.A. Ismail, O.A. Darwish, D.I. Tayel, et al., Impact of probiotic intake on the glycemic control, lipid profile and inflammatory markers among patients with type 2 diabetes mellitus, Clin. Diabetol. 10 (2021) 468-475. http://doi.org/10.5603/DK.a2021.0037.

[63]

F. Ahmadian, E. Razmpoosh, H.S. Ejtahed, et al., Effects of probiotic supplementation on major cardiovascular-related parameters in patients with type-2 diabetes mellitus: a secondary-data analysis of a randomized double-blind controlled trial, Diabetol. Metab. Syndr. 14 (2022) 52. http://doi.org/10.1186/s13098-022-00822-z.

[64]

A. Bayat, F. Azizi-Soleiman, M. Heidari-Beni, et al., Effect of cucurbita ficifolia and probiotic yogurt consumption on blood glucose, lipid profile, and inflammatory marker in type 2 diabetes, Int. J. Prev. Med. 7 (2016) 30. http://doi.org/10.4103/2008-7802.175455.

[65]

F. Raygan, Z. Rezavandi, F. Bahmani, et al., The effects of probiotic supplementation on metabolic status in type 2 diabetic patients with coronary heart disease, Diabetol. Metab. Syndr. 10 (2018) 51. http://doi.org/10.1186/s13098-018-0353-2.

[66]

A. Farrokhian, F. Raygan, A. Soltani, et al., The effects of synbiotic supplementation on carotid intima-media thickness, biomarkers of inflammation, and oxidative stress in people with overweight, diabetes, and coronary heart disease: a randomized, double-blind, placebo-controlled trial, Probiotics Antimicro. 11 (2019) 133-142. http://doi.org/10.1007/s12602-017-9343-1.

[67]

M. Mirjalili, A. Salari Sharif, A.A. Sangouni, et al., Effect of probiotic yogurt consumption on glycemic control and lipid profile in patients with type 2 diabetes mellitus: a randomized controlled trial, Clin. Nutr. Espen. 54 (2023) 144-149. http://doi.org/10.1016/j.clnesp.2023.01.014.

[68]

S. Saleh-Ghadimi, P. Dehghan, B. Sarmadi, et al., Improvement of sleep by resistant dextrin prebiotic in type 2 diabetic women coincides with attenuation of metabolic endotoxemia: involvement of gut-brain axis, J. Sci. Food Agr. 102 (2022) 5229-5237. http://doi.org/10.1002/jsfa.11876.

[69]

H. Jiang, Y. Zhang, D. Xu, et al., Probiotics ameliorates glycemic control of patients with diabetic nephropathy: a randomized clinical study, J. Clin. Lab. Anal. 35 (2021) e23650. http://doi.org/10.1002/jcla.23650.

[70]

S. Feizollahzadeh, R. Ghiasvand, A. Rezaei, et al., Effect of probiotic soy milk on serum levels of adiponectin, inflammatory mediators, lipid profile, and fasting blood glucose among patients with type Ⅱ diabetes mellitus, Probiotics Antimicro. 9 (2017) 41-47. http://doi.org/10.1007/s12602-016-9233-y.

[71]

B.P. Gargari, N. Namazi, M. Khalili, et al., Is there any place for resistant starch, as alimentary prebiotic, for patients with type 2 diabetes?, Complement. Ther. Med. 23 (2015) 810-815. http://doi.org/10.1016/j.ctim.2015.09.005.

[72]

P. Dehghan, B.P. Gargari, M.A. Jafar-Abadi, et al., Inulin controls inflammation and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized-controlled clinical trial, Int. J. Food Sci. Nutr. 65 (2014) 117-123. http://doi.org/10.3109/09637486.2013.836738.

[73]

Z. Mazloom, A. Yousefinejad, M.H. Dabbaghmanesh, 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.

[74]

H.S. Ejtahed, J. Mohtadi-Nia, A. Homayouni-Rad, et al., Probiotic yogurt improves antioxidant status in type 2 diabetic patients, Nutrition 28 (2012) 539-543. http://doi.org/10.1016/j.nut.2011.08.013.

[75]

A. Horvath, B. Leber, N. Feldbacher, et al., Effects of a multispecies synbiotic on glucose metabolism, lipid marker, gut microbiome composition, gut permeability, and quality of life in diabesity: a randomized, double-blind, placebo-controlled pilot study, Eur. J. Nutr. 59 (2020) 2969-2983. http://doi.org/10.1007/s00394-019-02135-w.

[76]

A. Ostadrahimi, A. Taghizadeh, 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, Iran J. Public Health 44 (2015) 228-237.

[77]

L.B. Tonucci, K.M.O. dos Santos, L.L. de Oliveira, et al., Clinical application of probiotics in type 2 diabetes mellitus: a randomized, double-blind, placebo-controlled study, Clin. Nutr. 36 (2017) 85-92. http://doi.org/10.1016/j.clnu.2015.11.011.

[78]

P. Dehghan, B.P. Gargari, M.A. Jafar-Abadi, Oligofructose-enriched inulin improves some inflammatory markers and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized controlled clinical trial, Nutrition 30 (2014) 418-423. http://doi.org/10.1016/j.nut.2013.09.005.

[79]

C. Moroti, L.F.S. Magri, M.D. Costa, et al., 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 (2012) 29. http://doi.org/10.1186/1476-511x-11-29.

[80]

B. Abbasi, M. Mirlohi, M. Daniali, et al., Effects of probiotic soy milk on lipid panel in type 2 diabetic patients with nephropathy: a double-blind randomized clinical trial, Prog. Nutr. 20 (2018) 70-78. http://doi.org/10.23751/pn.v20i2-S.5342.

[81]

H.S. Ejtahed, J. Mohtadi-Nia, A. Homayouni-Rad, 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. http://doi.org/10.3168/jds.2010-4128.

[82]

A. Akram Kooshki, T. Tofighiyan, M.H. Rakhshani, Effects of synbiotics on inflammatory markers in patients with type 2 diabetes mellitus, Glob. J. Health Sci. 7 (2015) 1-5. http://doi.org/10.5539/gjhs.v7n7p1.

[83]

C. Churuangsuk, J. Hall, A. Reynolds, et al., Diets for weight management in adults with type 2 diabetes: an umbrella review of published meta-analyses and systematic review of trials of diets for diabetes remission, Diabetologia 65 (2022) 14-36. http://doi.org/10.1007/s00125-021-05577-2.

[84]

J.G. Pastors, H. Warshaw, A. Daly, et al., The evidence for the effectiveness of medical nutrition therapy in diabetes management, Diabetes Care 25 (2002) 608-613. http://doi.org/10.2337/diacare.25.3.608.

[85]

K. Naseri, S. Saadati, Z. Yari, et al., Beneficial effects of probiotic and synbiotic supplementation on some cardiovascular risk factors among individuals with prediabetes and type 2 diabetes mellitus: a grade-assessed systematic review, meta-analysis, and meta-regression of randomized clinical trials, Pharmacol. Res. 182 (2022) 106288. http://doi.org/10.1016/j.phrs.2022.106288.

[86]

B.R. Loman, D. Hernández-Saavedra, R. An, et al., Prebiotic and probiotic treatment of nonalcoholic fatty liver disease: a systematic review and meta-analysis, Nutr. Rev. 76 (2018) 822-839. http://doi.org/10.1093/nutrit/nuy031.

[87]

A. Hadi, M. Pourmasoumi, M. Kazemi, et al., Efficacy of synbiotic interventions on blood pressure: a systematic review and meta-analysis of clinical trials, Crit. Rev. Food Sci. Nutr. 62 (2022) 5582-5591. http://doi.org/10.1080/10408398.2021.1888278.

[88]

A. Dixon, K. Robertson, A. Yung, et al., Efficacy of probiotics in patients of cardiovascular disease risk: a systematic review and meta-analysis, Curr. Hypertens. Rep. 22 (2020) 74. http://doi.org/10.1007/s11906-020-01080-y.

[89]

F.Z. Marques, C.R. Mackay, D.M. Kaye, Beyond gut feelings: how the gut microbiota regulates blood pressure, Nat. Rev. Cardiol. 15 (2018) 20-32. http://doi.org/10.1038/nrcardio.2017.120.

[90]

A. Upadrasta, R.S. Madempudi, Probiotics and blood pressure: current insights, Integr. Blood Press. C. 9 (2016) 33-42. http://doi.org/10.2147/ibpc.S73246.

[91]

S. Al Khodor, B. Reichert, I.F. Shatat, The microbiome and blood pressure: can microbes regulate our blood pressure?, Front. Pediatr. 5 (2017) 138. http://doi.org/10.3389/fped.2017.00138.

[92]

A.F.G. Cicero, F. Fogacci, M. Bove, et al., Impact of a short-term synbiotic supplementation on metabolic syndrome and systemic inflammation in elderly patients: a randomized placebo-controlled clinical trial, Eur. J. Nutr. 60 (2021) 655-663. http://doi.org/10.1007/s00394-020-02271-8.

[93]

C. Kalofoutis, C. Piperi, A. Kalofoutis, et al., Type Ⅱ diabetes mellitus and cardiovascular risk factors: current therapeutic approaches, Exp. Clin. Cardiol. 12 (2007) 17-28.

[94]

T. Hirano, Pathophysiology of diabetic dyslipidemia, J. Atheroscler. Thromb. 25 (2018) 771-782. http://doi.org/10.5551/jat.RV17023.

[95]

T.M. Al Quran, Z.A. Bataineh, A.H. Al-Mistarehi, et al., Prevalence and pattern of dyslipidemia and its associated factors among patients with type 2 diabetes mellitus in Jordan: a cross-sectional study, Int. J. Gen. Med. 15 (2022) 7669-7683. http://doi.org/10.2147/ijgm.S377463.

[96]

S.A. Peters, Y. Singhateh, D. Mackay, et al., Total cholesterol as a risk factor for coronary heart disease and stroke in women compared with men: a systematic review and meta-analysis, Atherosclerosis 248 (2016) 123-131. http://doi.org/10.1016/j.atherosclerosis.2016.03.016.

[97]

C. Baigent, L. Blackwell, J. Emberson, et al., Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials, Lancet 376 (2010) 1670-1681. http://doi.org/10.1016/s0140-6736(10)61350-5.

[98]

Z. Ghorbani, A. Kazemi, T.U.P. Bartolomaeus, et al., The effect of probiotic and synbiotic supplementation on lipid parameters among patients with cardiometabolic risk factors: a systematic review and meta-analysis of clinical trials, Cardiovasc. Res. 119 (2023) 933-956. http://doi.org/10.1093/cvr/cvac128.

[99]

M. Zarezadeh, V. Musazadeh, A.H. Faghfouri, et al., Probiotics act as a potent intervention in improving lipid profile: an umbrella systematic review and meta-analysis, Crit. Rev. Food Sci. Nutr. 63 (2023) 145-158. http://doi.org/10.1080/10408398.2021.2004578.

[100]

V.L. O’Morain, D.P. Ramji, The potential of probiotics in the prevention and treatment of atherosclerosis, Mol. Nutr. Food Res. 64 (2020) e1900797. http://doi.org/10.1002/mnfr.201900797.

[101]

J.Y. Yoo, S.S. Kim, Probiotics and prebiotics: present status and future perspectives on metabolic disorders, Nutrients 8 (2016) 173. http://doi.org/10.3390/nu8030173.

[102]

H. Ohira, W. Tsutsui, Y. Fujioka, Are short chain fatty acids in gut microbiota defensive players for inflammation and atherosclerosis?, J. Atheroscler. Thromb. 24 (2017) 660-672. http://doi.org/10.5551/jat.RV17006.

[103]

M.N. Huda, M. Kim, B.J. Bennett, Modulating the microbiota as a therapeutic intervention for type 2 diabetes, Front. Endocrinol. 12 (2021) 632335. http://doi.org/10.3389/fendo.2021.632335.

[104]

A.L. Cunningham, J.W. Stephens, D.A. Harris, Gut microbiota influence in type 2 diabetes mellitus (T2DM), Gut. Pathog. 13 (2021) 50. http://doi.org/10.1186/s13099-021-00446-0.

[105]

L. Liu, J. Zhang, Y. Cheng, et al., Gut microbiota: a new target for T2DM prevention and treatment, Front. Endocrinol. 13 (2022) 958218. http://doi.org/10.3389/fendo.2022.958218.

[106]

P. Paul, R. Kaul, M. Harfouche, et al., The effect of microbiome-modulating probiotics, prebiotics and synbiotics on glucose homeostasis in type 2 diabetes: a systematic review, meta-analysis, and meta-regression of clinical trials, Pharmacol. Res. 185 (2022) 106520. http://doi.org/10.1016/j.phrs.2022.106520.

[107]

L. Coutts, K. Ibrahim, Q.Y. Tan, et al., Can probiotics, prebiotics and synbiotics improve functional outcomes for older people: a systematic review, Eur. Geriatr. Med. 11 (2020) 975-993. http://doi.org/10.1007/s41999-020-00396-x.

[108]

X. Wang, W. Bao, J. Liu, et al., Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis, Diabetes Care 36 (2013) 166-175. http://doi.org/10.2337/dc12-0702.

[109]

H.J. Zheng, J. Guo, Q. Jia, et al., The effect of probiotic and synbiotic supplementation on biomarkers of inflammation and oxidative stress in diabetic patients: a systematic review and meta-analysis of randomized controlled trials, Pharmacol. Res. 142 (2019) 303-313. http://doi.org/10.1016/j.phrs.2019.02.016.

[110]

Y. Zhang, H. Zhang, Microbiota associated with type 2 diabetes and its related complications, Food Sci. Hum. Well. 2 (2013) 167-172. http://doi.org/10.1016/j.fshw.2013.09.002.

[111]

O. Asbaghi, D. Ashtary-Larky, R. Bagheri, et al., Folic acid supplementation improves glycemic control for diabetes prevention and management: a systematic review and dose-response meta-analysis of randomized controlled trials, Nutrients 13 (2021) 2355. http://doi.org/10.3390/nu13072355.

[112]

O. Asbaghi, D. Ashtary-Larky, R. Bagheri, et al., Effects of folic acid supplementation on inflammatory markers: a grade-assessed systematic review and dose-response meta-analysis of randomized controlled trials, Nutrients 13 (2021) 2327. http://doi.org/10.3390/nu13072327.

Food Science and Human Wellness
Article number: 9250002
Cite this article:
Tian Y, Xia J, Li L, et al. Effects of probiotics, prebiotics and synbiotics supplementation on cardiovascular risk factors in patients with type 2 diabetes mellitus: a GRADE-assessed systematic review and meta-analysis of randomized controlled trials. Food Science and Human Wellness, 2025, 14(1): 9250002. https://doi.org/10.26599/FSHW.2024.9250002
Metrics & Citations  
Article History
Copyright
Rights and Permissions