The Role of Gut Microbiota in the Development of Type 2 Diabetes Mellitus

Main Article Content

Okoro Miracle Chinonso, MD Ifeoluwa Mary Falade, MD Pamela C William-Enemali, MBBS Eberechukwu .G. Anamazobi, MD Tricia O. Okoye, MD Chinelo Igweike, MD Ogochi Blessing Chukwuneke Sheeba Abraham Jeyaraj, MBBS, PGDFM, MSCR Falilatu Bose Akinyemi, MD, MBA Beloveth C. Annonye Evelyn Omowunmi Fatoye, MD Okelue Edwards Okobi, MD, MS

Abstract

Type 2 diabetes mellitus presents a significant global healthcare challenge with a steadily rising prevalence. Recent research has shed light on the correlation between gut bacteria and the improvement or progression of type 2 diabetes. This review article delves into an evaluation of current knowledge of how the gut microbiota affects type 2 diabetes, focusing on the impact of microbial imbalances on insulin resistance, inflammation, and metabolic dysfunction. By evaluating current knowledge in this field, the study highlights the potential of modifying the gut microbiota through food plan adjustments, probiotics, prebiotics, and fecal transplants as a promising strategy for managing type 2 diabetes. Additionally, it explores how specific microbial species and compounds influence glucose metabolism and insulin sensitivity, potentially providing targets for microbiota-focused interventions aimed at ameliorating the burden of type 2 diabetes.

Keywords: Gut Microbiota, Type 2 Diabetes Mellitus, Insulin Resistance, Microbial Imbalance, Inflammation, Probiotics, Glucose Metabolism

Article Details

How to Cite
CHINONSO, Okoro Miracle et al. The Role of Gut Microbiota in the Development of Type 2 Diabetes Mellitus. Medical Research Archives, [S.l.], v. 12, n. 7, july 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5454>. Date accessed: 30 dec. 2024. doi: https://doi.org/10.18103/mra.v12i7.5454.
Section
Research Articles

References

1. DeFronzo RA, Ferrannini E, Groop L, et al. Type 2 diabetes mellitus. Nat Rev Dis Primers. 2015;1(1):1-22. doi:10.1038/nrdp.2015.19

2. Reed J, Bain S, Kanamarlapudi V. A Review of Current Trends with Type 2 Diabetes Epidemiology, Aetiology, Pathogenesis, Treatments and Future Perspectives. Diabetes Metab Syndr Obes. 2021;14:3567-3602. doi:10.2147/DMSO.S319895

3. Sapra A, Bhandari P. Diabetes. In: StatPearls. StatPearls Publishing; 2024. Accessed April 19, 2024. http://www.ncbi.nlm.nih.gov/books/NBK551501/

4. Herold KC, Delong T, Perdigoto AL, Biru N, Brusko TM, Walker LSK. The immunology of type 1 diabetes. Nat Rev Immunol. Published online February 2, 2024:1-17. doi:10.1038/s41577-023-00985-4

5. Katsarou A, Gudbjörnsdottir S, Rawshani A, et al. Type 1 diabetes mellitus. Nat Rev Dis Primers. 2017;3(1):1-17. doi:10.1038/nrdp.2017.16

6. Lucier J, Weinstock RS. Type 1 Diabetes. In: StatPearls. StatPearls Publishing; 2024. Accessed April 19, 2024. http://www.ncbi.nlm.nih.gov/books/NBK507713/

7. Quattrin T, Mastrandrea LD, Walker LSK. Type 1 diabetes. The Lancet. 2023;401(10394):2149-2162. doi:10.1016/S0140-6736(23)00223-4

8. Goyal R, Singhal M, Jialal I. Type 2 Diabetes. In: StatPearls. StatPearls Publishing; 2024. Accessed April 19, 2024. http://www.ncbi.nlm.nih.gov/books/NBK513253/

9. Olokoba AB, Obateru OA, Olokoba LB. Type 2 Diabetes Mellitus: A Review of Current Trends. Oman Med J. 2012;27(4):269-273. doi:10.5001/ omj.2012.68

10. Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. doi:10.1016/j.diabres.201 9.107843

11. Parker ED, Lin J, Mahoney T, et al. Economic Costs of Diabetes in the U.S. in 2022. Diabetes Care. 2024;47(1):26-43. doi:10.2337/dci23-0085

12. Wu Y, Ding Y, Tanaka Y, Zhang W. Risk Factors Contributing to Type 2 Diabetes and Recent Advances in the Treatment and Prevention. Int J Med Sci. 2014;11(11):1185-1200. doi:10.7150/ijms .10001

13. Crittenden S, Goepp M, Pollock J, et al. Prostaglandin E2 promotes intestinal inflammation via inhibiting microbiota-dependent regulatory T cells. Sci Adv. 2021;7(7):eabd7954. doi:10.1126/sci adv.abd7954

14. Han Q, Wang J, Li W, Chen ZJ, Du Y. Androgen-induced gut dysbiosis disrupts glucolipid metabolism and endocrinal functions in polycystic ovary syndrome. Microbiome. 2021;9 (1):101. doi:10.1186/s40168-021-01046-5

15. Mayneris-Perxachs J, Cardellini M, Hoyles L, et al. Iron status influences non-alcoholic fatty liver disease in obesity through the gut microbiome. Microbiome. 2021;9(1):104. doi:10.1186/s40168-021-01052-7

16. Kashtanova DA, Tkacheva ON, Doudinskaya EN, et al. Gut Microbiota in Patients with Different Metabolic Statuses: Moscow Study. Microorganisms. 2018;6(4):98. doi:10.3390/microorganisms6040098

17. Takagi T, Naito Y, Kashiwagi S, et al. Changes in the Gut Microbiota are Associated with Hypertension, Hyperlipidemia, and Type 2 Diabetes Mellitus in Japanese Subjects. Nutrients. 2020;12(10):2996. doi:10.3390/nu12102996

18. Wang TY, Zhang XQ, Chen AL, et al. A comparative study of microbial community and functions of type 2 diabetes mellitus patients with obesity and healthy people. Appl Microbiol Biotechnol. 2020;104(16):7143-7153. doi:10.1007/ s00253-020-10689-7

19. Zhou Z, Sun B, Yu D, Zhu C. Gut Microbiota: An Important Player in Type 2 Diabetes Mellitus. Front Cell Infect Microbiol. 2022;12. doi:10.3 389/fcimb.2022.834485

20. Gurung M, Li Z, You H, et al. Role of gut microbiota in type 2 diabetes pathophysiology. EBioMedicine. 2020;51:102590. doi:10.1016/j.ebi om.2019.11.051

21. Gao R, Zhu C, Li H, et al. Dysbiosis Signatures of Gut Microbiota Along the Sequence from Healthy, Young Patients to Those with Overweight and Obesity. Obesity (Silver Spring). 2018;26(2) :351-361. doi:10.1002/oby.22088

22. Candela M, Biagi E, Soverini M, et al. Modulation of gut microbiota dysbioses in type 2 diabetic patients by macrobiotic Ma-Pi 2 diet. Br J Nutr. 2016;116(1):80-93. doi:10.1017/S000711451 6001045

23. Sedighi M, Razavi S, Navab-Moghadam F, et al. Comparison of gut microbiota in adult patients with type 2 diabetes and healthy individuals. Microb Pathog. 2017;111:362-369. doi:10.1016/j. micpath.2017.08.038

24. Wu X, Ma C, Han L, et al. Molecular characterization of the fecal microbiota in patients with type II diabetes. Curr Microbiol. 2010;61(1):69 -78. doi:10.1007/s00284-010-9582-9

25. Barengolts E, Green SJ, Eisenberg Y, et al. Gut microbiota varies by opioid use, circulating leptin and oxytocin in African American men with diabetes and high burden of chronic disease. PLoS One. 2018;13(3):e0194171. doi:10.1371/journal.p one.0194171

26. Sasaki M, Ogasawara N, Funaki Y, et al. Transglucosidase improves the gut microbiota profile of type 2 diabetes mellitus patients: a randomized, double-blind, placebo-controlled study. BMC Gastroenterol. 2013;13:81. doi:10.118 6/1471-230X-13-81

27. Wu H, Esteve E, Tremaroli V, et al. Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med. 2017;23(7):850-858. doi:10.1038/nm.4345

28. Murphy R, Tsai P, Jüllig M, Liu A, Plank L, Booth M. Differential Changes in Gut Microbiota After Gastric Bypass and Sleeve Gastrectomy Bariatric Surgery Vary According to Diabetes Remission. Obes Surg. 2017;27(4):917-925. doi:10. 1007/s11695-016-2399-2

29. Aoki R, Kamikado K, Suda W, et al. A proliferative probiotic Bifidobacterium strain in the gut ameliorates progression of metabolic disorders via microbiota modulation and acetate elevation. Sci Rep. 2017;7:43522. doi:10.1038/srep43522

30. Kikuchi K, Ben Othman M, Sakamoto K. Sterilized bifidobacteria suppressed fat accumulation and blood glucose level. Biochem Biophys Res Commun. 2018;501(4):1041-1047. doi:10.1016/j.bbrc.2018.05.105

31. Zhang Y, Lu S, Yang Y, et al. The diversity of gut microbiota in type 2 diabetes with or without cognitive impairment. Aging Clin Exp Res. 2021;33 (3):589-601. doi:10.1007/s40520-020-01553-9

32. Asemi Z, Aarabi MH, Hajijafari M, 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 Crossover Controlled Clinical Trial. Int J Prev Med. 2017;8:43. doi:10.4103/ijpvm.IJPVM_ 257_16

33. Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V. Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition. 2012;28(5):539-543. doi:10.1016/j.nut.2011.08.013

34. Nerstedt A, Nilsson EC, Ohlson K, et al. Administration of Lactobacillus evokes coordinated changes in the intestinal expression profile of genes regulating energy homeostasis and immune phenotype in mice. Br J Nutr. 2007;97(6):1117-1127. doi:10.1017/S0007114507682907

35. Lippert K, Kedenko L, Antonielli L, et al. Gut microbiota dysbiosis associated with glucose metabolism disorders and the metabolic syndrome in older adults. Benef Microbes. 2017;8(4):545-556. doi:10.3920/BM2016.0184

36. Munukka E, Wiklund P, Pekkala S, et al. Women with and without metabolic disorder differ in their gut microbiota composition. Obesity (Silver Spring). 2012;20(5):1082-1087. doi:10.1038/oby. 2012.8

37. He Y, Wu W, Wu S, et al. Linking gut microbiota, metabolic syndrome and economic status based on a population-level analysis. Microbiome. 2018;6:172. doi:10.1186/s40168-018-0557-6

38. Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143 (4):913-916.e7. doi:10.1053/j.gastro.2012.06.031

39. Shih CT, Yeh YT, Lin CC, Yang LY, Chiang CP. Akkermansia muciniphila is Negatively Correlated with Hemoglobin A1c in Refractory Diabetes. Microorganisms. 2020;8(9):1360. doi:10.3390/micr oorganisms8091360

40. Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55-60. doi:10.10 38/nature11450

41. Tilg H, Moschen AR. Microbiota and diabetes: an evolving relationship. Gut. 2014;63(9):1513-1521. doi:10.1136/gutjnl-2014-306928

42. Thomas C, Gioiello A, Noriega L, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10(3):167-177. doi:10.1016/j.cmet.2009.08.001

43. Tian R, Liu H, Feng S, et al. Gut microbiota dysbiosis in stable coronary artery disease combined with type 2 diabetes mellitus influences cardiovascular prognosis. Nutr Metab Cardiovasc Dis. 2021;31(5):1454-1466. doi:10.1016/j.numecd. 2021.01.007

44. Kim SH, Huh CS, Choi ID, et al. The antidiabetic activity of Bifidobacterium lactis HY8101 in vitro and in vivo. J Appl Microbiol. 2014;117(3):834-845. doi:10.1111/jam.12573

45. Kang JH, Yun SI, Park MH, Park JH, Jeong SY, Park HO. Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PLoS One. 2013;8(1):e54617. doi:10.1371/jo urnal.pone.0054617

46. Alam F, Islam MA, Khalil MI, Gan SH. Metabolic Control of Type 2 Diabetes by Targeting the GLUT4 Glucose Transporter: Intervention Approaches. Curr Pharm Des. 2016;22(20):3034-3049. doi:10.2174/1381612822666160307145801

47. Aldahish A, Balaji P, Vasudevan R, Kandasamy G, James JP, Prabahar K. Elucidating the Potential Inhibitor against Type 2 Diabetes Mellitus Associated Gene of GLUT4. Journal of Personalized Medicine. 2023;13(4):660. doi:10.339 0/jpm13040660

48. Plovier H, Everard A, Druart C, et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med. 2017;23 (1):107-113. doi:10.1038/nm.4236

49. Liu WC, Yang MC, Wu YY, Chen PH, Hsu CM, Chen LW. Lactobacillus plantarum reverse diabetes-induced Fmo3 and ICAM expression in mice through enteric dysbiosis-related c-Jun NH2-terminal kinase pathways. PLoS One. 2018;13(5): e0196511. doi:10.1371/journal.pone.0196511

50. Miao J, Ling AV, Manthena PV, et al. Flavin-containing monooxygenase 3 as a potential player in diabetes-associated atherosclerosis. Nat Commun. 2015;6:6498. doi:10.1038/ncomms7498

51. Wang G, Li X, Zhao J, Zhang H, Chen W. Lactobacillus casei CCFM419 attenuates type 2 diabetes via a gut microbiota dependent mechanism. Food Funct. 2017;8(9):3155-3164. doi:10.1039/c7fo00593h

52. Althubiti M. Tyrosine Kinase Targeting: A Potential Therapeutic Strategy for Diabetes. Saudi J Med Med Sci. 2022;10(3):183-191. doi:10.4103 /sjmms.sjmms_492_21

53. Gupta P, Taiyab A, Hassan MI. Emerging role of protein kinases in diabetes mellitus: From mechanism to therapy. Adv Protein Chem Struct Biol. 2021;124:47-85. doi:10.1016/bs.apcsb.2020. 11.001

54. Tan K, Tesar C, Wilton R, Keigher L, Babnigg G, Joachimiak A. Novel α-glucosidase from human gut microbiome: substrate specificities and their switch. FASEB J. 2010;24(10):3939-3949. doi:10.10 96/fj.10-156257

55. Tan K, Tesar C, Wilton R, Jedrzejczak RP, Joachimiak A. Interaction of antidiabetic α‐glucosidase inhibitors and gut bacteria α‐glucosidase. Protein Sci. 2018;27(8):1498-1508. doi:10.1002/pro.3444

56. Groot BL de, Grubmüller H. Water Permeation Across Biological Membranes: Mechanism and Dynamics of Aquaporin-1 and GlpF. Science. 2001;294(5550):2353-2357. doi:10.1126/science.1066115

57. Tsai CY, Lu HC, Chou YH, et al. Gut Microbial Signatures for Glycemic Responses of GLP-1 Receptor Agonists in Type 2 Diabetic Patients: A Pilot Study. Front Endocrinol (Lausanne). 2021;12:814770. doi:10.3389/fendo.2021.814770

58. Zeng Y, Wu Y, Zhang Q, Xiao X. Crosstalk between glucagon-like peptide 1 and gut microbiota in metabolic diseases. mBio. 2023;15(1) :e02032-23. doi:10.1128/mbio.02032-23

59. André P, Laugerette F, Féart C. Metabolic Endotoxemia: A Potential Underlying Mechanism of the Relationship between Dietary Fat Intake and Risk for Cognitive Impairments in Humans? Nutrients. 2019;11(8):1887. doi:10.3390/nu11081887

60. Fuke N, Nagata N, Suganuma H, Ota T. Regulation of Gut Microbiota and Metabolic Endotoxemia with Dietary Factors. Nutrients. 2019;11(10):2277. doi:10.3390/nu11102277

61. Gomes JMG, Costa J de A, Alfenas R de CG. Metabolic endotoxemia and diabetes mellitus: A systematic review. Metabolism. 2017;68:133-144. doi:10.1016/j.metabol.2016.12.009

62. Pussinen PJ, Havulinna AS, Lehto M, Sundvall J, Salomaa V. Endotoxemia Is Associated With an Increased Risk of Incident Diabetes. Diabetes Care. 2011;34(2):392-397. doi:10.2337/dc10-1676

63. Chelakkot C, Choi Y, Kim DK, et al. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Exp Mol Med. 2018;50(2):e450. doi:10.1038/emm.2017.282

64. Yoshida N, Emoto T, Yamashita T, et al. Bacteroides vulgatus and Bacteroides dorei Reduce Gut Microbial Lipopolysaccharide Production and Inhibit Atherosclerosis. Circulation. 2018;138(22):2486-2498. doi:10.1161/CIRCULATIONAHA.118.033714

65. Houmard JA. Intramuscular lipid oxidation and obesity. Am J Physiol Regul Integr Comp Physiol. 2008;294(4):R1111-R1116. doi:10.1152/ajpregu.00396.2007

66. Everard A, Belzer C, Geurts L, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066-9071. doi:10.10 73/pnas.1219451110

67. Yang JY, Lee YS, Kim Y, et al. Gut commensal Bacteroides acidifaciens prevents obesity and improves insulin sensitivity in mice. Mucosal Immunol. 2017;10(1):104-116. doi:10.1038/mi.2016.42

68. Mayorga-Ramos A, Barba-Ostria C, Simancas-Racines D, Guamán LP. Protective role of butyrate in obesity and diabetes: New insights. Front Nutr. 2022;9:1067647. doi:10.3389/fnut.2022.1067647

69. Noureldein MH, Bitar S, Youssef N, Azar S, Eid AA. Butyrate modulates diabetes-linked gut dysbiosis: epigenetic and mechanistic modifications. J Mol Endocrinol. 2020;64(1):29-42. doi:10.1530/ JME-19-0132

70. Siptroth J, Moskalenko O, Krumbiegel C, Ackermann J, Koch I, Pospisil H. Variation of butyrate production in the gut microbiome in type 2 diabetes patients. Int Microbiol. 2023;26(3):601-610. doi:10.1007/s10123-023-00324-6

71. BAHGAT MM, IBRAHIM DR. Pro-inflammatory cytokine polarization in type 2 diabetes. Cent Eur J Immunol. 2020;45(2):170-175. doi:10.5114/ceji.20 20.97904

72. Velikova TV, Kabakchieva PP, Assyov YS, Georgiev TА. Targeting Inflammatory Cytokines to Improve Type 2 Diabetes Control. Biomed Res Int. 2021;2021:7297419. doi:10.1155/2021/7297419

73. Chang YC, Ching YH, Chiu CC, et al. TLR2 and interleukin-10 are involved in Bacteroides fragilis-mediated prevention of DSS-induced colitis in gnotobiotic mice. PLoS One. 2017;12(7):e0180025 . doi:10.1371/journal.pone.0180025

74. Chen J, Vitetta L. The Role of Butyrate in Attenuating Pathobiont-Induced Hyperinflammation. Immune Netw. 2020;20(2):e15. doi:10.4110/in.202 0.20.e15

75. Siddiqui MT, Cresci GAM. The Immunomodulatory Functions of Butyrate. J Inflamm Res. 2021;14:6025-6041. doi:10.2147/JIR. S300989

76. Wang JW, Kuo CH, Kuo FC, et al. Fecal microbiota transplantation: Review and update. Journal of the Formosan Medical Association. 2019;118:S23-S31. doi:10.1016/j.jfma.2018.08.011

77. Feng J, Chen Y, Liu Y, et al. Efficacy and safety of fecal microbiota transplantation in the treatment of ulcerative colitis: a systematic review and meta-analysis. Sci Rep. 2023;13(1):14494. doi:10.1038/s 41598-023-41182-6

78. Ng SC, Xu Z, Mak JWY, et al. Microbiota engraftment after faecal microbiota transplantation in obese subjects with type 2 diabetes: a 24-week, double-blind, randomised controlled trial. Gut. 2022;71(4):716-723. doi:10.1136/gutjnl-2020-323617

79. Ding D, Yong H, You N, et al. Prospective Study Reveals Host Microbial Determinants of Clinical Response to Fecal Microbiota Transplant Therapy in Type 2 Diabetes Patients. Front Cell Infect Microbiol. 2022;12:820367. doi:10.3389/ fcimb.2022.820367

80. Wu Z, Zhang B, Chen F, et al. Fecal microbiota transplantation reverses insulin resistance in type 2 diabetes: A randomized, controlled, prospective study. Front Cell Infect Microbiol. 2023;12:108999 1. doi:10.3389/fcimb.2022.1089991

81. Hota S, Poutanen S, et al. Fecal microbiota transplantation for recurrent Clostridium difficile infection. CMAJ Jun 2018, 190 (24) E746; DOI: 10.1503/cmaj.171454

82. Tanase DM, Gosav EM, Neculae E, et al. Role of Gut Microbiota on Onset and Progression of Microvascular Complications of Type 2 Diabetes (T2DM). Nutrients. 2020;12(12):3719. doi:10.3390 /nu12123719

83. Liu Q, Xu Z, Dai M, Su Q, Leung Chan FK, Ng SC. Fecal microbiota transplantations and the role of bacteriophages. Clin Microbiol Infect. 2023;29(6 ):689-694. doi:10.1016/j.cmi.2022.11.012

84. Ren R, Gao X, Shi Y, et al. Long-Term Efficacy of Low-Intensity Single Donor Fecal Microbiota Transplantation in Ulcerative Colitis and Outcome-Specific Gut Bacteria. Front Microbiol. 2021;12:7 42255. doi:10.3389/fmicb.2021.742255

85. Bresser LRF, de Goffau MC, Levin E, Nieuwdorp M. Gut Microbiota in Nutrition and Health with a Special Focus on Specific Bacterial Clusters. Cells. 2022;11(19):3091. doi:10.3390/cell s11193091

86. Su L, Hong Z, Zhou T, et al. Health improvements of type 2 diabetic patients through diet and diet plus fecal microbiota transplantation. Sci Rep. 2022;12(1):1152. doi:10.1038/s41598-022-05127-9

87. Dostal Webster A, Staley C, Hamilton MJ, et al. Influence of short-term changes in dietary sulfur on the relative abundances of intestinal sulfate-reducing bacteria. Gut Microbes. 2019;10(4):447-457. doi:10.1080/19490976.2018.1559682

88. Bibbò S, Settanni CR, Porcari S, et al. Fecal Microbiota Transplantation: Screening and Selection to Choose the Optimal Donor. J Clin Med. 2020;9(6):1757. doi:10.3390/jcm9061757

89. Aràjol C, Aira Gómez A, González-Suárez B, et al. Donor selection for fecal microbiota transplantation. Consensus document of the Catalan Society of Gastroenterology and the Catalan Society of Infectious Diseases and Clinical Microbiology. Gastroenterología y Hepatología (English Edition). 2021;44(2):175-180. doi:10.1016/ j.gastre.2020.07.005

90. Wilson BC, Vatanen T, Cutfield WS, O’Sullivan JM. The Super-Donor Phenomenon in Fecal Microbiota Transplantation. Front Cell Infect Microbiol. 2019;9:2. doi:10.3389/fcimb.2019.00002

91. Stenman LK, Waget A, Garret C, Klopp P, Burcelin R, Lahtinen S. Potential probiotic Bifidobacterium animalis ssp. lactis 420 prevents weight gain and glucose intolerance in diet-induced obese mice. Benef Microbes. 2014;5(4) :437-445. doi:10.3920/BM2014.0014

92. Uusitupa HM, Rasinkangas P, Lehtinen MJ, et al. Bifidobacterium animalis subsp. lactis 420 for Metabolic Health: Review of the Research. Nutrients. 2020;12(4):892. doi:10.3390/nu12040892

93. Yao K, Zeng L, He Q, Wang W, Lei J, Zou X. Effect of Probiotics on Glucose and Lipid Metabolism in Type 2 Diabetes Mellitus: A Meta-Analysis of 12 Randomized Controlled Trials. Med Sci Monit. 2017;23:3044-3053. doi:10.12659/MSM .902600

94. Mahboobi S, Rahimi F, Jafarnejad S. 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. 2018;8(4):565-574. doi:10.151 71/apb.2018.065

95. Toejing P, Khampithum N, Sirilun S, Chaiyasut C, Lailerd N. Influence of Lactobacillus paracasei HII01 Supplementation on Glycemia and Inflammatory Biomarkers in Type 2 Diabetes: A Randomized Clinical Trial. Foods. 2021 Jun 23;10(7):1455. doi: 10.3390/foods10071455.

96. Yadav H, Jain S, Sinha PR. Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus case in high fructose fed rats. Nutrition. 2007;23(1):62-68. doi:10.1016/j. nut.2006.09.002

97. Stenman LK, Waget A, Garret C, Briand F, Burcelin R, Sulpice T, Lahtinen S. Probiotic B420 and prebiotic polydextrose improve efficacy of antidiabetic drugs in mice. Diabetol Metab Syndr. 2015 Sep 12;7:75. doi: 10.1186/s13098-015-0075-7.

98. Reimer RA, Grover GJ, Koetzner L, Gahler RJ, Lyon MR, Wood S. Combining sitagliptin/ metformin with a functional fiber delays diabetes progression in Zucker rats. J Endocrinol. 2014 Feb 10;220(3):361-73. doi: 10.1530/JOE-13-0484.

99. Venugopalan V, Shriner KA, Wong-Beringer A. Regulatory Oversight and Safety of Probiotic Use. Emerg Infect Dis. 2010;16(11):1661-1665. doi:10.3 201/eid1611.100574

100. Dore MP, Bibbò S, Fresi G, Bassotti G, Pes GM. Side Effects Associated with Probiotic Use in Adult Patients with Inflammatory Bowel Disease: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients. 2019;1 1(12):2913. doi:10.3390/nu11122913

101. Shen NT, Leff JA, Schneider Y, et al. Cost-Effectiveness Analysis of Probiotic Use to Prevent Clostridium difficile Infection in Hospitalized Adults Receiving Antibiotics. Open Forum Infect Dis. 2017;4(3):ofx148. doi:10.1093/ofid/ofx148

102. Singh TP, Natraj B.H. Next-generation probiotics: a promising approach towards designing personalized medicine. Crit Rev Microbiol. 2021;47(4):479-498. doi:10.1080/10408 41X.2021.1902940

103. Mao T, Huang F, Zhu X, Wei D, Chen L. Effects of dietary fiber on glycemic control and insulin sensitivity in patients with type 2 diabetes: A systematic review and meta-analysis. Journal of Functional Foods. 2021;82:104500. doi:10.1016/j.j ff.2021.104500

104. Xu X, Zhang F, Ren J, et al. Dietary intervention improves metabolic levels in patients with type 2 diabetes through the gut microbiota: a systematic review and meta-analysis. Front Nutr. 2024;10: 1243095. doi:10.3389/fnut.2023.1243095

105. Ajala O, English P, Pinkney J. Systematic review and meta-analysis of different dietary approaches to the management of type 2 diabetes. Am J Clin Nutr. 2013;97(3):505-516. doi:10.3945/ajcn.112.042457

106. Zimmermann M, Zimmermann-Kogadeeva M, Wegmann R, Goodman AL. Mapping human microbiome drug metabolism by gut bacteria and their genes. Nature. 2019;570(7762):462-467. doi:10.1038/s41586-019-1291-3

107. Javdan B, Lopez JG, Chankhamjon P, et al. Personalized Mapping of Drug Metabolism by the Human Gut Microbiome. Cell. 2020;181(7):1661-1679.e22. doi:10.1016/j.cell.2020.05.001

108. Heinken A, Basile A, Hertel J, Thinnes C, Thiele I. Genome-Scale Metabolic Modeling of the Human Microbiome in the Era of Personalized Medicine. Annu Rev Microbiol. 2021;75:199-222. doi:10.1146/annurev-micro-060221-012134

109. Lagier JC, Khelaifia S, Alou MT, et al. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol. 2016;1:16203. doi:10.1038/nmicrobiol.2016.203

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