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Systematic Review

Role of probiotics/synbiotic supplementation in glycemic control: A critical umbrella review of meta-analyses of randomized controlled trials

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References

  • Abdelqadir, Y. H., A. Hamdallah, E. A. Sibaey, A. S. Hussein, M. Abdelaziz, A. Abdelazim, K. M. Ragab, S. K. Helmy, and A. Z. Nourelden. 2020. Efficacy of probiotic supplementation in patients with diabetic nephropathy: A systematic review and meta-analysis. Clinical Nutrition ESPEN 40:57–67. doi: 10.1016/j.clnesp.2020.06.019
  • Andrade, C. 2020. Mean difference, standardized mean difference (SMD), and their use in meta-analysis: As simple as it gets. Journal of Clinical Psychiatry, 81(5):20f13681. doi: 10.4088/JCP.20f13681
  • Arabi, S. M., L. S. Bahrami, I. Rahnama, and A. Sahebkar. 2022. Impact of synbiotic supplementation on cardiometabolic and anthropometric indices in patients with metabolic syndrome: A systematic review and meta-analysis of randomized controlled trials. Pharmacological Research 176:106061. doi: 10.1016/j.phrs.2022.106061.
  • Ardeshirlarijani, E., O. Tabatabaei-Malazy, S. Mohseni, M. Qorbani, B. Larijani, and R. Baradar Jalili. 2019. Effect of probiotics supplementation on glucose and oxidative stress in type 2 diabetes mellitus: A meta-analysis of randomized trials. Daru-Journal of Pharmaceutical Sciences 27 (2):827–837. doi: 10.1007/s40199-019-00302-2
  • Aromataris, E., R. Fernandez, C. M. Godfrey, C. Holly, H. Khalil, and P. Tungpunkom. 2015. Summarizing systematic reviews: Methodological development, conduct and reporting of an umbrella review approach. International Journal of Evidence-Based Healthcare 13 (3):132–40.
  • Asemi, Z., Z. Zare, H. Shakeri, S. S. Sabihi, and A. Esmaillzadeh. 2013. Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Annals of Nutrition & Metabolism 63 (1–2):1–9.
  • Asher, G., and P. Sassone-Corsi. 2015. Time for food: The intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161 (1):84–92. doi: 10.1016/j.cell.2015.03.015.
  • Askari, G., A. Ghavami, F. Shahdadian, and A. R. Moravejolahkami. 2021. Effect of synbiotics and probiotics supplementation on autoimmune diseases: A systematic review and meta-analysis of clinical trials. Clinical Nutrition 40 (5):3221–34. doi: 10.1016/j.clnu.2021.02.015.
  • Barengolts, E., E. D. Smith, S. Reutrakul, L. Tonucci, and T. Anothaisintawee. 2019. The effect of probiotic yogurt on glycemic control in type 2 diabetes or obesity: A meta-analysis of nine randomized controlled trials. Nutrients 11 (3):671. doi: 10.3390/nu11030671.
  • Brunkwall, L., and M. Orho-Melander. 2017. The gut microbiome as a target for prevention and treatment of hyperglycaemia in type 2 diabetes: From current human evidence to future possibilities. Diabetologia 60 (6):943–51. doi: 10.1007/s00125-017-4278-3.
  • Cao, D. X., E. Y. Wong, M. N. Vela, and Q. T. Le. 2021. Effect of probiotic supplementation on glycemic outcomes in patients with abnormal glucose metabolism: A systematic review and meta-analysis of randomized controlled trials. Annals of Nutrition and Metabolism 77 (5):251–61. doi: 10.1159/000518677.
  • Chapman, C. M. C., G. R. Gibson, and I. Rowland. 2011. Health benefits of probiotics: Are mixtures more effective than single strains? European Journal of Nutrition 50 (1):1–17.
  • Chen, Y., R. Yue, B. Zhang, Z. Li, J. Shui, and X. Huang. 2020. Effects of probiotics on blood glucose, biomarkers of inflammation and oxidative stress in pregnant women with gestational diabetes mellitus: A meta-analysis of randomized controlled trials. Medicina Clinica, 154:206.
  • Clark, H. D., G. A. Wells, C. Huet, F. A. Mcalister, L. R. Salmi, D. Fergusson, and A. Laupacis. 1999. Assessing the quality of randomized trials: Reliability of the Jadad scale. Controlled Clinical Trials 20 (5):448–52.
  • Cozzolino, M., A. Vitagliano, L. Pellegrini, M. Chiurazzi, A. Andriasani, G. Ambrosini, and N. Garrido. 2020. Therapy with probiotics and synbiotics for polycystic ovarian syndrome: A systematic review and meta-analysis. European Journal of Nutrition 59 (7):2841–56.
  • Crusell, M. K. W., T. H. Hansen, T. Nielsen, K. H. Allin, M. C. Ruhlemann, P. Damm, H. Vestergaard, C. Rorbye, N. R. Jorgensen, O. B. Christiansen, et al. 2018. Gestational diabetes is associated with change in the gut microbiota composition in third trimester of pregnancy and postpartum. Microbiome 6:89. doi: 10.1186/s40168-018-0472-x.
  • Dai, Y., J. Quan, L. Xiong, Y. Luo, and B. Yi. 2022. Probiotics improve renal function, glucose, lipids, inflammation and oxidative stress in diabetic kidney disease: A systematic review and meta-analysis. Renal Failure 44 (1):862–80. doi: 10.1080/0886022X.2022.2079522.
  • Dal Canto, E., A. Ceriello, L. Ryden, M. Ferrini, T. B. Hansen, O. Schnell, E. Standl, and J. W. J. Beulens. 2019. Diabetes as a cardiovascular risk factor: An overview of global trends of macro and micro vascular complications. European Journal of Preventive Cardiology 26 (2_suppl):25–32.
  • Delzenne, N. M., P. D. Cani, A. Everard, A. M. Neyrinck, and L. B. Bindels. 2015. Gut microorganisms as promising targets for the management of type 2 diabetes. Diabetologia 58 (10):2206–17.
  • Dong, Y., M. Xu, L. Chen, and A. Bhochhibhoya. 2019. Probiotic foods and supplements interventions for metabolic syndromes: A systematic review and meta-analysis of recent clinical trials. Annals of Nutrition & Metabolism 74 (3):224–41.
  • Egger, M., G. D. Smith, M. Schneider, and C. Minder. 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical Research ed.) 315 (7109):629–34.
  • Einarson, T. R., A. Acs, C. Ludwig, and U. H. Panton. 2018. Prevalence of cardiovascular disease in type 2 diabetes: A systematic literature review of scientific evidence from across the world in 2007–2017. Cardiovascular Diabetology 17:83. doi: 10.1186/s12933-018-0728-6
  • Federation, I. D. 2021. IDF Diabetes Atlas. 10th ed. International Diabetes Federation.
  • Gilbert, J. A., M. J. Blaser, J. G. Caporaso, J. K. Jansson, S. V. Lynch, and R. Knight. 2018. Current understanding of the human microbiome. Nature Medicine 24 (4):392–400. doi: 10.1038/nm.4517.
  • Grajower, M. M., and B. D. Horne. 2019. Clinical management of intermittent fasting in patients with diabetes mellitus. Nutrients, 11 (4):873. doi: 10.3390/nu11040873.
  • Grundy, S. M., I. J. Benjamin, G. L. Burke, A. Chait, R. H. Eckel, B. V. Howard, W. Mitch, S. C. Smith, and J. R. Sowers. 1999. Diabetes and cardiovascular disease - A statement for healthcare professionals from the American Heart Association. Circulation 100 (10):1134–46.
  • Gupta, V. K., S. Paul, and C. Dutta. 2017. Geography, ethnicity or subsistence-specificvariations in human microbiome composition and diversity. Frontiers in Microbiology 8:1162. doi: 10.3389/fmicb.2017.01162.
  • Gurung, M., Z. P. Li, H. You, R. Rodrigues, D. B. Jump, A. Morgun, and N. Shulzhenko. 2020. Role of gut microbiota in type 2 diabetes pathophysiology. Ebiomedicine 51:102590. doi: 10.1016/j.ebiom.2019.11.051
  • Guyatt, G., A. D. Oxman, E. A. Akl, R. Kunz, G. Vist, J. Brozek, S. Norris, Y. Falck-Ytter, P. Glasziou, H. Debeer, et al. 2011. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. Journal of Clinical Epidemiology 64 (4):383–94.
  • Hadi, A., A. Arab, S. Khalesi, N. Rafie, M. Kafeshani, and M. Kazemi. 2021. Effects of probiotic supplementation on anthropometric and metabolic characteristics in adults with metabolic syndrome: A systematic review and meta-analysis of randomized clinical trials. Clinical Nutrition (Edinburgh, Scotland) 40 (7):4662–73. doi: 10.1016/j.clnu.2021.05.027.
  • Hadi, A., H. Mohammadi, M. Miraghajani, and E. Ghaedi. 2019. Efficacy of synbiotic supplementation in patients with nonalcoholic fatty liver disease: A systematic review and meta-analysis of clinical trials: Synbiotic supplementation and NAFLD. Critical Reviews in Food Science and Nutrition 59 (15):2494–505.
  • Hadi, A., S. Moradi, A. Ghavami, S. Khalesi, and M. Kafeshani. 2020. Effect of probiotics and synbiotics on selected anthropometric and biochemical measures in women with polycystic ovary syndrome: A systematic review and meta-analysis. European Journal of Clinical Nutrition 74 (4):543–7.
  • Han, M.-M., J.-F. Sun, X.-H. Su, Y.-F. Peng, H. Goyal, C.-H. Wu, X.-Y. Zhu, and L. Li. 2019. Probiotics improve glucose and lipid metabolism in pregnant women: A meta-analysis. Annals of Translational Medicine 7 (5):99. doi: 10.21037/atm.2019.01.61.
  • Hasain, Z., N. A. C. Roos, F. Rahmat, M. Mustapa, R. A. R. Ali, and N. M. Mokhtar. 2021. Diet and pre-intervention washout modifies the effects of probiotics on gestational diabetes mellitus: A comprehensive systematic review and meta-analysis of randomized controlled trials. Nutrients 13 (9):3045. doi: 10.3390/nu13093045.
  • Heshmati, J., F. Farsi, S. Yosaee, M. Razavi, M. Rezaeinejad, E. Karimie, and M. Sepidarkish. 2019. The effects of probiotics or synbiotics supplementation in women with polycystic ovarian syndrome: A systematic review and meta-analysis of randomized clinical trials. Probiotics and Antimicrobial Proteins 11 (4):1236–47. doi: 10.1007/s12602-018-9493-9.
  • Higgins, J. P. T., D. G. Altman, P. C. Gotzsche, P. Jueni, D. Moher, A. D. Oxman, J. Savovic, K. F. Schulz, L. Weeks, J. A. C. Sterne, et al. 2011. The Cochrane collaboration’s tool for assessing risk of bias in randomised trials. BMJ - British Medical Journal 343: d5928. doi: 10.1136/bmj.d5928
  • Higgins, J. P. T., S. G. Thompson, J. J. Deeks, and D. G. Altman. 2003. Measuring inconsistency in meta-analyses. BMJ (Clinical Research ed.) 327 (7414):557–60.
  • Hill, C., F. Guarner, G. Reid, G. R. Gibson, D. J. Merenstein, B. Pot, L. Morelli, R. B. Canani, H. J. Flint, S. Salminen, et al. 2014. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews. Gastroenterology & Hepatology 11 (8):506–14. doi: 10.1038/nrgastro.2014.66.
  • Horiuchi, H., K. Kamikado, R. Aoki, N. Suganuma, T. Nishijima, A. Nakatani, and I. Kimura. 2020. Bifidobacterium animalis subsp. lactis GCL2505 modulates host energy metabolism via the short-chain fatty acid receptor GPR43. Scientific Reports 10 (1):4158. doi: 10.1038/s41598-020-60984-6.
  • Hu, Y.-M., F. Zhou, Y. Yuan, and Y.-C. Xu. 2017. Effects of probiotics supplement in patients with type 2 diabetes mellitus: A meta-analysis of randomized trials. Medicina Clínica 148 (8):362–70. doi: 10.1016/j.medcli.2016.11.036.
  • Huang, Y., X. Wang, L. Zhang, K. Zheng, J. Xiong, J. Li, C. Cong, Z. Gong, and J. Mao. 2022. Effect of probiotics therapy on nonalcoholic fatty liver disease. Computational and Mathematical Methods in Medicine 2022:1–15. doi: 10.1155/2022/7888076.
  • Hummel, S., K. Veltman, C. Cichon, U. Sonnenborn, and M. A. Schmidt. 2012. Differential targeting of the E-cadherin/beta-catenin complex by gram-positive probiotic lactobacilli improves epithelial barrier function. Applied and Environmental Microbiology 78 (4):1140–7.
  • Ioannidis, J. P. A. 2009. Integration of evidence from multiple meta-analyses: A primer on umbrella reviews, treatment networks and multiple treatments meta-analyses. CMAJ: Canadian Medical Association Journal = Journal de L'Association Medicale Canadienne 181 (8):488–93.
  • Jasim, O. H., M. M. Mahmood, and A. H. Ad'hiah. 2022. Significance of lipid profile parameters in predicting pre-diabetes. Archives of Razi Institute 77:277–84.
  • Jin, S. X., L. Y. Sha, J. L. Dong, J. Yi, Y. Liu, Z. X. Guo, and B. Hu. 2020. Effects of nutritional strategies on glucose homeostasis in gestational diabetes mellitus: A systematic review and network meta-analysis. Journal of Diabetes Research, 2020:1–12. doi: 10.1155/2020/6062478.
  • Kannel, W. B., and D. L. McGee. 1979. Diabetes and cardiovascular-disease - Framingham-study. JAMA 241 (19):2035–8. doi: 10.1001/jama.1979.03290450033020.
  • Kasińska, M. A., and J. Drzewoski. 2015. Effectiveness of probiotics in type 2 diabetes: A meta-analysis. Polish Archives of Internal Medicine 125 (11):803–13. doi: 10.20452/pamw.3156.
  • Kothari, D., S. Patel, and S. K. Kim. 2019. Probiotic supplements might not be universally-effective and safe: A review. Biomedicine & Pharmacotherapy 111:537–47. doi: 10.1016/j.biopha.2018.12.104.
  • Koutnikova, H., B. Genser, M. Monteiro-Sepulveda, J.-M. Faurie, S. Rizkalla, J. Schrezenmeir, and K. Clement. 2019. Impact of bacterial probiotics on obesity, diabetes and non-alcoholic fatty liver disease related variables: A systematic review and meta-analysis of randomised controlled trials. BMJ Open, 9 (3):e017995. doi: 10.1136/bmjopen-2017-017995.
  • Łagowska, K., A. M. Malinowska, B. Zawieja, and E. Zawieja. 2020. Improvement of glucose metabolism in pregnant women through probiotic supplementation depends on gestational diabetes status: Meta-analysis. Scientific Reports 10 (1):17796. doi: 10.1038/s41598-020-74773-8.
  • Lambeth, S. M., T. Carson, J. Lowe, T. Ramaraj, J. W. Leff, L. Luo, C. J. Bell, and V. O. Shah. 2015. Composition, diversity and abundance of gut microbiome in prediabetes and type 2 diabetes. Journal of Diabetes and Obesity 2 (3):1–7.
  • Ley, S. H., O. Hamdy, V. Mohan, and F. B. Hu. 2014. Prevention and management of type 2 diabetes: Dietary components and nutritional strategies. Lancet (London, England) 383 (9933):1999–2007. doi: 10.1016/S0140-6736(14)60613-9.
  • Li, C., X. Li, H. Han, H. Cui, M. Peng, G. Wang, and Z. Wang. 2016. Effect of probiotics on metabolic profiles in type 2 diabetes mellitus: A meta-analysis of randomized, controlled trials. Medicine 95 (26):e4088. doi: 10.1097/MD.0000000000004088.
  • Li, K. K., P. J. Tian, S. D. Wang, P. Lei, L. Qu, J. P. Huang, Y. J. Shan, and B. L. Li. 2017a. Targeting gut microbiota: Lactobacillus alleviated type 2 diabetes via inhibiting LPS secretion and activating GPR43 pathway. Journal of Functional Foods 38:561–70. doi: 10.1016/j.jff.2017.09.049.
  • Li, X., E. Wang, B. Yin, D. Fang, P. Chen, G. Wang, J. Zhao, H. Zhang, and W. Chen. 2017b. Effects of Lactobacillus casei CCFM419 on insulin resistance and gut microbiota in type 2 diabetic mice. Beneficial Microbes 8 (3):421–32.
  • Li, Y., Y. Tan, G. Xia, and J. Shuai. 2021. Effects of probiotics, prebiotics, and synbiotics on polycystic ovary syndrome: A systematic review and meta-analysis. Critical Reviews in Food Science and Nutrition: 1–17. doi: 10.1080/10408398.2021.1951155.
  • Li, Y. Z., D. Teng, X. G. Shi, G. J. Qin, Y. F. Qin, H. B. Quan, B. Y. Shi, H. Sun, J. M. Ba, B. Chen, et al. 2020. Prevalence of diabetes recorded in mainland China using 2018 diagnostic criteria from the American Diabetes Association: National cross sectional study. BMJ - British Medical Journal 369:m997. doi: 10.1136/bmj.m997
  • Liang, T., L. Wu, Y. Xi, Y. Li, X. Xie, C. Fan, L. Yang, S. Yang, X. Chen, J. Zhang, et al. 2021. Probiotics supplementation improves hyperglycemia, hypercholesterolemia, and hypertension in type 2 diabetes mellitus: An update of meta-analysis. Critical Reviews in Food Science and Nutrition 61 (10):1670–88. doi: 10.1080/10408398.2020.1764488.
  • Liu, L., P. Li, Y. Liu, and Y. Zhang. 2019. Efficacy of probiotics and synbiotics in patients with nonalcoholic fatty liver disease: A meta-analysis. Digestive Diseases and Sciences 64 (12):3402–12.
  • Luo, C., J. Wan, Z. Rao, and Y. Zhang. 2021. Synbiotic supplementation for glycemic status in pregnant women: A meta-analysis of randomized clinical trials. Gynecological Endocrinology 37 (2):146–51.
  • Ma, Y.-Y., L. Lin, C.-H. Yu, Z. Shen, L.-H. Chen, and Li, Y.-M. 2013. Effects of probiotics on nonalcoholic fatty liver disease: A meta-analysis. World Journal of Gastroenterology 19 (40):6911–8. doi: 10.3748/wjg.v19.i40.6911.
  • Madeo, B., C. Diazzi, A. R. M. Granata, M. El Ghoch, C. Greco, S. Romano, S. Scaltriti, and V. Rochira. 2020. Effect of a standard schema of self-monitoring blood glucose in patients with poorly controlled, non-insulin-treated type 2 diabetes mellitus: A controlled longitudinal study. Journal of Population Therapeutics & Clinical Pharmacology 27 (SP2):E1–E11. doi: 10.15586/jptcp.v27iSP2.680.
  • Mahdizade Ari, M., S. Teymouri, T. Fazlalian, P. Asadollahi, R. Afifirad, M. Sabaghan, F. Valizadeh, R. Ghanavati, and A. Darbandi. 2022. The effect of probiotics on gestational diabetes and its complications in pregnant mother and newborn: A systematic review and meta-analysis during 2010–2020. Journal of Clinical Laboratory Analysis 36 (4): e24326. doi: 10.1002/jcla.24326.
  • Maher, C. G., C. Sherrington, R. D. Herbert, A. M. Moseley, and M. Elkins. 2003. Reliability of the PEDro scale for rating quality of randomized controlled trials. Physical Therapy 83 (8):713–21.
  • Memarrast, F., S. Ghafouri-Fard, S. Kolivand, S. Jafary-Nodooshan, N. Neyazi, E. Sadroddiny, and E. Motevaseli. 2017. Comparative evaluation of probiotics effects on plasma glucose, lipid, and insulin levels in streptozotocin-induced diabetic rats. Diabetes-Metabolism Research and Reviews, 33(7):e1912. doi: 10.1002/dmrr.2912
  • Miao, C., Q. Guo, X. Fang, Y. Chen, Y. Zhao, and Q. Zhang. 2021. Effects of probiotic and synbiotic supplementation on insulin resistance in women with polycystic ovary syndrome: A meta-analysis. Journal of International Medical Research 49 (7):030006052110317. doi: 10.1177/03000605211031758.
  • Mobini, R., V. Tremaroli, M. Ståhlman, F. Karlsson, M. Levin, M. Ljungberg, M. Sohlin, H. Bertéus Forslund, R. Perkins, F. Bäckhed, et al. 2017. Metabolic effects of Lactobacillus reuteri DSM 17938 in people with type 2 diabetes: A randomized controlled trial. Diabetes, Obesity and Metabolism 19 (4):579–89. doi: 10.1111/dom.12861.
  • Mohammadi, H., A. Ghavami, A. Hadi, G. Askari, M. Symonds, and M. Miraghajani. 2019. Effects of pro-/synbiotic supplementation on anthropometric and metabolic indices in overweight or obese children and adolescents: A systematic review and meta-analysis. Complementary Therapies in Medicine 44:269–76. doi: 10.1016/j.ctim.2019.05.008.
  • Nasser, M. 2020. Cochrane handbook for systematic reviews of interventions. American Journal of Public Health 110 (6):753–754. doi: 10.2105/AJPH.2020.305609.
  • Nemet, I., P. P. Saha, N. Gupta, W. Zhu, K. A. Romano, S. M. Skye, T. C. Cajka, M. L. Mohan, Y. Wu, M. Funabashi, et al. 2020. A cardiovascular disease-linked gut microbial metabolite acts via adrenergic receptors. Cell 180 (5):862–77.e22. +. doi: 10.1016/j.cell.2020.02.016.
  • Nikbakht, E., S. Khalesi, I. Singh, L. T. Williams, N. P. West, and N. Colson. 2018. Effect of probiotics and synbiotics on blood glucose: A systematic review and meta-analysis of controlled trials. European Journal of Nutrition 57 (1):95–106. doi: 10.1007/s00394-016-1300-3.
  • Oh, M. R., H. Y. Jang, S. Y. Lee, S. J. Jung, S. W. Chae, S. O. Lee, and B. H. Park. 2021. Lactobacillus plantarum HAC01 supplementation improves glycemic control in prediabetic subjects: A randomized, double-blind, placebo-controlled trial. Nutrients 13 (7):2337. doi: 10.3390/nu13072337.
  • Pan, J., Q. Pan, Y. Chen, H. Zhang, and X. Zheng. 2019. Efficacy of probiotic supplement for gestational diabetes mellitus: A systematic review and meta-analysis. Journal of Maternal-Fetal & Neonatal Medicine, 32:323.
  • Park, K. Y., B. Kim, and C. K. Hyun. 2015. Lactobacillus rhamnosus GG improves glucose tolerance through alleviating ER stress and suppressing macrophage activation in db/db mice. Journal of Clinical Biochemistry and Nutrition 56 (3):240–6.
  • Peng, T.-B., T.-W. Wu, and Y.-C. Chao. 2018. Effect of probiotics on the glucose levels of pregnant women: A meta-analysis of randomized controlled trials. Medicina 54 (5):77. doi: 10.3390/medicina54050077.
  • Qin, J. J., Y. R. Li, Z. M. Cai, S. H. Li, J. F. Zhu, F. Zhang, S. S. Liang, W. W. Zhang, Y. L. Guan, D. Q. Shen, et al. 2012. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (7418):55–60.
  • Qiu, X., Q. Wu, W. Li, K. Tang, and J. Zhang. 2022. Effects of Lactobacillus supplementation on glycemic and lipid indices in overweight or obese adults: A systematic review and meta-analysis. Clinical Nutrition (Edinburgh, Scotland) 41 (8):1787–97. doi: 10.1016/j.clnu.2022.06.030.
  • Ramanathan, K., N. S. Jagadeesh, U. Vishwanath, C. Dayal, R. Chandrababu, and M. Hayter. 2021. Efficacy of supplementation of probiotics on maternal glycaemic control - A systematic review and meta-analysis of randomized controlled trials. Clinical Epidemiology and Global Health, 10:100674. doi: 10.1016/j.cegh.2020.11.007.
  • Rezaei, M., A. Sanagoo, L. Jouybari, N. Behnampoo, and A. Kavosi. 2017. The effect of probiotic yogurt on blood glucose and cardiovascular biomarkers in patients with type II diabetes: A randomized controlled trial. Journal of Evidence-Based Care 6 (4):26–35. doi: 10.22038/EBCJ.2016.7984
  • Rittiphairoj, T., K. Pongpirul, K. Janchot, N. T. Mueller, and T. Li. 2021. Probiotics contribute to glycemic control in patients with type 2 diabetes mellitus: A systematic review and meta-analysis. Advances in Nutrition 12 (3):722–34. doi: 10.1093/advances/nmaa133.
  • Roth, G. A., D. Abate, K. H. Abate, S. M. Abay, C. Abbafati, N. Abbasi, H. Abbastabar, L. Abd-Allah, J. Abdela, A. Abdelalim, et al. 2018. Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: A systematic analysis for the Global Burden of Disease Study 2017. The Lancet 392 (10159):1736–88. doi: 10.1016/S0140-6736(18)32203-7.
  • Ruan, Y., J. Sun, J. He, F. Chen, R. Chen, and H. Chen. 2015. Effect of probiotics on glycemic control: A systematic review and meta-analysis of randomized, controlled trials. PLoS One 10 (7):e0132121. doi: 10.1371/journal.pone.0132121.
  • Sabico, S., A. Al-Mashharawi, N. M. Al-Daghri, K. Wani, O. E. Amer, D. S. Hussain, M. G. A. Ansari, M. S. Masoud, M. S. Alokail, and P. G. Mcternan. 2019. 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. Clinical Nutrition (Edinburgh, Scotland) 38 (4):1561–9. doi: 10.1016/j.clnu.2018.08.009.
  • Sabico, S., A. Al-Mashharawi, N. M. Al-Daghri, S. Yakout, A. M. Alnaami, M. S. Alokail, and P. G. Mcternan. 2017. Effects of a multi-strain probiotic supplement for 12 weeks in circulating endotoxin levels and cardiometabolic profiles of medication naive T2DM patients: A randomized clinical trial. Journal of Translational Medicine 15 (1):249. doi: 10.1186/s12967-017-1354-x.
  • Salari, A., M. Mahdavi-Roshan, J. Kheirkhah, and Z. Ghorbani. 2021. Probiotics supplementation and cardiometabolic risk factors: A new insight into recent advances, potential mechanisms, and clinical implications. PharmaNutrition 16:100261. doi: 10.1016/j.phanu.2021.100261.
  • Samah, S., K. Ramasamy, S. M. Lim, and C. F. Neoh. 2016. Probiotics for the management of type 2 diabetes mellitus: A systematic review and meta-analysis. Diabetes Research and Clinical Practice 118:172–82. doi: 10.1016/j.diabres.2016.06.014.
  • Schellekens, H., C. Torres-Fuentes, M. Van De Wouw, C. M. Long-Smith, A. Mitchell, C. Strain, K. Berding, T. F. S. Bastiaanssen, K. Rea, A. V. Golubeva, et al. 2021. Bifidobacterium longum counters the effects of obesity: Partial successful translation from rodent to human. EBioMedicine 63:103176. doi: 10.1016/j.ebiom.2020.103176.
  • Sender, R., S. Fuchs, and R. Milo. 2016. Revised estimates for the number of human and bacteria cells in the body. PLoS Biology 14 (8):e1002533. doi: 10.1371/journal.pbio.1002533
  • Sharin, T., B. Ahammed, M. Elahi, M. S. A. Mamun, and D. K. Paul. 2021. Impact of physical exercise and food habit on type ii diabetes mellitus medicated patients - A cross sectional study. Journal of Chemical Health Risks 11:33–43.
  • Shea, B. J., B. C. Reeves, G. Wells, M. Thuku, C. Hamel, J. Moran, D. Moher, P. Tugwell, V. Welch, E. Kristjansson, et al. 2017. AMSTAR 2: A critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ-British Medical Journal, 358:j4008 doi: 10.1136/bmj.j4008
  • Simon, M. C., K. Strassburger, B. Nowotny, H. Kolb, P. Nowotny, V. Burkart, F. Zivehe, J. H. Hwang, P. Stehle, G. Pacini, et al. 2015. Intake of Lactobacillus reuteri improves incretin and insulin secretion in glucose-tolerant humans: A proof of concept. Diabetes Care 38 (10):1827–34. doi: 10.2337/dc14-2690.
  • Stanaway, J. D., A. Afshin, E. Gakidou, S. S. Lim, D. Abate, K. H. Abate, C. Abbafati, N. Abbasi, H. Abbastabar, F. Abd-Allah, et al. 2018. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990-2017: A systematic analysis for the Global Burden of Disease Study 2017. The Lancet 392 (10159):1923–94. doi: 10.1016/S0140-6736(18)32225-6.
  • Sterne, J. A. C., A. J. Sutton, J. P. A. Ioannidis, N. Terrin, D. R. Jones, J. Lau, J. Carpenter, G. Rucker, R. M. Harbord, C. H. Schmid, et al. 2011. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ - British Medical Journal, 343 (Jul 22 1):d4002–d4002. doi: 10.1136/bmj.d4002.
  • Sun, Z. K., X. J. Sun, J. Li, Z. Y. Li, Q. W. Hu, L. L. Li, X. Q. Hao, M. P. Song, and C. W. Li. 2020. Using probiotics for type 2 ­diabetes mellitus intervention: Advances, questions, and potential. Critical Reviews in Food Science and Nutrition 60 (4):670–83.
  • Suwal, S., Q. Wu, W. L. Liu, Q. Y. Liu, H. X. Sun, M. Liang, J. Gao, B. Zhang, Y. B. Kou, Z. Z. Liu, et al. 2018. The probiotic effectiveness in preventing experimental colitis is correlated with host gut microbiota. Frontiers in Microbiology 9:2675. doi: 10.3389/fmicb.2018.02675.
  • Swanson, K. S., G. R. Gibson, R. Hutkins, R. A. Reimer, G. Reid, K. Verbeke, K. P. Scott, H. D. Holscher, M. B. Azad, N. M. Delzenne, et al. 2020. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nature Reviews. Gastroenterology & Hepatology 17 (11):687–701. doi: 10.1038/s41575-020-0344-2.
  • Tabrizi, R., M. Moosazadeh, K. B. Lankarani, M. Akbari, S. T. Heydari, F. Kolahdooz, and Z. Asemi. 2018. The effects of synbiotic supplementation on glucosemetabolism and lipid profiles in patients with diabetes: A systematic review and meta-analysis of randomized controlled trials. Probiotics and Antimicrobial Proteins 10 (2):329–42. doi: 10.1007/s12602-017-9299-1.
  • Tabrizi, R., V. Ostadmohammadi, M. Akbari, K. B. Lankarani, S. Vakili, P. Peymani, M. Karamali, F. Kolahdooz, and Z. Asemi. 2022. The effects of probiotic supplementation on clinical symptom, weight loss, glycemic control, lipid and hormonal profiles, biomarkers of inflammation, and oxidative stress in women with polycystic ovary syndrome: A systematic review and meta-analysis of randomized controlled trials. Probiotics and Antimicrobial Proteins 14 (1):1–14. doi: 10.1007/s12602-019-09559-0.
  • Tang, Y., J. Huang, W. Y. Zhang, S. Qin, Y. X. Yang, H. Ren, Q. B. Yang, and H. Hu. 2019. Effects of probiotics on nonalcoholic fatty liver disease: A systematic review and meta-analysis. Therapeutic Advances in Gastroenterology 12:175628481987804. doi: 10.1177/1756284819878046.
  • Taylor, B. L., G. E. Woodfall, K. E. Sheedy, M. L. O’Riley, K. A. Rainbow, E. L. Bramwell, and N. J. Kellow. 2017. Effect of probiotics on metabolic outcomes in pregnant women with gestational diabetes: A systematic review and meta-analysis of randomized controlled trials. Nutrients 9 (5):461. doi: 10.3390/nu9050461.
  • Tiderencel, K. A., D. A. Hutcheon, and J. Ziegler. 2020. Probiotics for the treatment of type 2 diabetes: A review of randomized controlled trials. Diabetes-Metabolism Research and Reviews 36 (1):e3213. doi: 10.1002/dmrr.3213
  • Trabelsi, M. S., S. Lestavel, B. Staels, and X. Collet. 2017. Intestinal bile acid receptors are key regulators of glucose homeostasis. Proceedings of the Nutrition Society, 76, 192–202.
  • Valdes, A. M., L. Walter, E. Segal, and T. D. Spector. 2018. Role of the gut microbiota in nutrition and health. BMJ - British Medical Journal, 361:k2179. doi: 10.1136/bmj.k2179
  • Van Rosendal, S. P., M. A. Osborne, R. G. Fassett, and J. S. Coombes. 2010. Guidelines for glycerol use in hyperhydration and rehydration associated with exercise. Sports Medicine 40:113–39.
  • Wang, X., Q.-F. Juan, Y.-W. He, L. Zhuang, Y.-Y. Fang, and Y.-H. Wang. 2017. Multiple effects of probiotics on different types of diabetes: A systematic review and meta-analysis of randomized, placebo-controlled trials. Journal of Pediatric Endocrinology & Metabolism: JPEM 30 (6):611–22. doi: 10.1515/jpem-2016-0230.
  • Wang, Y. M., D. Dilidaxi, Y. C. Wu, J. Sailike, X. Sun, and X. H. Nabi. 2020. Composite probiotics alleviate type 2 diabetes by regulating intestinal microbiota and inducing GLP-1 secretion in db/db mice. Biomedicine & Pharmacotherapy 125: 109914. doi: 10.1016/j.biopha.2020.109914
  • WHO. 2016. Global report on diabetes. [Online].
  • Yadav, H., J. H. Lee, J. Lloyd, P. Walter, and S. G. Rane. 2013. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. The Journal of Biological Chemistry 288 (35):25088–97.
  • Yatsunenko, T., F. E. Rey, M. J. Manary, I. Trehan, M. G. Dominguez-Bello, M. Contreras, M. Magris, G. Hidalgo, R. N. Baldassano, A. P. Anokhin, et al. 2012. Human gut microbiome viewed across age and geography. Nature 486 (7402):222–7. +. doi: 10.1038/nature11053.
  • Zhang, C., J. Jiang, C. Wang, S. Li, L. Yu, F. Tian, J. Zhao, H. Zhang, W. Chen, and Q. Zhai. 2022a. Meta-analysis of randomized controlled trials of the effects of probiotics on type 2 diabetes in adults. Clinical Nutrition 41 (2):365–73. doi: 10.1016/j.clnu.2021.11.037.
  • Zhang, C. C., Z. M. Yu, J. X. Zhao, H. Zhang, Q. X. Zhai, and W. Chen. 2019. Colonization and probiotic function of Bifidobacterium longum. Journal of Functional Foods 53:157–65. doi: 10.1016/j.jff.2018.12.022.
  • Zhang, J., S. Ma, S. Wu, C. Guo, S. Long, and H. Tan. 2019. Effects of probiotic supplement in pregnant women with gestational diabetes mellitus: A systematic review and meta-analysis of randomized controlled trials. Journal of Diabetes Research 2019:5364730. doi: 10.1155/2019/5364730.
  • Zhang, L., X. Hu, Y. Wang, C. He, J. Yu, X. Fang, Y. Zhang, X. Xu, and J. Yang. 2022b. Effects of probiotic supplementation on glucose metabolism in pregnant women without diabetes: A systematic review and meta-analysis. Food & Function 13 (16):8388–98. doi: 10.1039/d1fo04333a.
  • Zhang, Q., Y. Wu, and X. Fei. 2016. Effect of probiotics on glucose metabolism in patients with type 2 diabetes mellitus: A meta-analysis of randomized controlled trials. Medicina 52 (1):28–34. doi: 10.1016/j.medici.2015.11.008.
  • Zhao, L. P., F. Zhang, X. Y. Ding, G. J. Wu, Y. Y. Lam, X. J. Wang, H. Q. Fu, X. H. Xue, C. H. Lu, J. L. Ma, et al. 2018. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science (New York, N.Y.) 359 (6380):1151–6. +. doi: 10.1126/science.aao5774.
  • Zheng, F. L., Z. Wang, C. Stanton, R. P. Ross, J. X. Zhao, H. Zhang, B. Yang, and W. Chen. 2021. Lactobacillus rhamnosus FJSYC4-1 and Lactobacillus reuteri FGSZY33L6 alleviate metabolic syndrome via gut microbiota regulation. Food & Function 12 (9):3919–30.
  • Zhou, L., C. Ding, J. Wu, X. Chen, D. M. Ng, H. Wang, Y. Zhang, and N. Shi. 2021. Probiotics and synbiotics show clinical efficacy in treating gestational diabetes mellitus: A meta-analysis. Primary Care Diabetes 15 (6):937–47.

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