Review of the Gut Microbiota Dynamics in Type-2 Diabetes Mellitus (T2DM): A Focus on Human-Based Studies http://www.doi.org/10.26538/tjnpr/v7i6.2
Main Article Content
Abstract
The gut microbiome contains a complex microbial community within the gastrointestinal tract (GIT), which benefits our health. Yet, studies have shown that persons with Type-2 diabetes mellitus (T2DM), compared to healthy controls, possess gut microbiota profile differences. Therefore, this study reviewed gut microbiome dynamics in the onset and progression of T2DM, starting from insulin resistance to how its modulation by drugs, food, and pre/postbiotics influences insulin resistance. First, an in-depth inquiry was executed on Google Scholar and PUBMED using the following keywords: Biomarker AND “Therapeutic targets” AND “Gut Microbiota” OR “Gut Microbiome” AND “Type 2 diabetes” NOT Cancer, and 755 papers were retrieved. Next, two independent authors screened the papers by title and abstract, leaving 64 articles for this study. Investigations revealed that some bacterial diversities occurred before the pathogenesis associated with T2DM. According to frequently published data, T2DM was adversely related with the genera Bifidobacterium, Bacteroides, Faecalibacterium, Akkermansia, and Roseburia, while it was positively associated with the genera Ruminococcus, Fusobacterium, and Blautia. Insulin sensitivity in T2DM was also improved with butyrate-producing short-chain
fatty acid bacteria. Notably, patients with T2DM were mostly identified by increased specific infectious microbes, such as Clostridium spp, whereas the majority of control samples were enriched in butyrate-producing bacteria and Lactobacillus spp. In summary, we observed several inconsistencies in T2DM disease-linked organism(s) and knowledge gaps due to inadequate data. Hence, future studies must prove the relationships between dysbiosis and the onset/progression of T2DM to provide useful information that may guide better management of T2DM.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Iweala EEJ. Propensity for diabetes and correlation of its predisposing factors in Ota, Nigeria. J. Med. Sci. 2013; 13(8):809-813.
Chamberlain JJ, Herman WH, Leal S, Rhinehart AS, Shubrook JH, Skolnik N, Kalyani RR. Pharmacologic therapy for type 2 diabetes: Synopsis of the 2017 American diabetes association standards of medical care in diabetes. Ann Intern Med. 2017; 166(8):572-578.
Zhang L, Chu J, Hao W, Zhang J, Li H, Yang C, Yang J, Chen X, Wang H. Gut microbiota and type 2 diabetes mellitus: Association, mechanism, and translational applications. Mediators Inflamm. 2021; 2021:5110276.
Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, Colagiuri S, Guariguata L, Motala AA, Ogurtsova K, Shaw JE, Bright D, Williams R, Committee IDFDA. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the
international diabetes federation diabetes atlas, 9(th) edition. Diabetes Res Clin Pract. 2019; 157:107843.
Ali MK, Siegel KR, Chandrasekar E, Tandon N, Montoya PA, Mbanya J-C, Chan J, Zhang P, Narayan K. Diabetes: An update on the pandemic and potential solutions. Disease control priorities. 2017; 5.
Thursby E, Juge N. Introduction to the human gut flora. Biochem J. 2017; 474(11):1823-1836.
Bäumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016; 535(7610):85-93.
Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 2010; 10(3):159-169.
Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005; 307(5717):1915-1920.
Neish AS. Microbes in gastrointestinal health and disease. Gastroenterol. 2009; 136(1):65-80.
Natividad JM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: Pathological and therapeutic implications. Pharmacol Res. 2013; 69(1):42-51.
Den Besten G, Van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 2013; 54(9):2325-2340.
Gensollen T, Iyer S, Kasper D. Antibiotic use and its consequences for the normal microbiome. Science. 2016; 352(6285):539-545
Bull MJ, Plummer NT. Part 1: The human gut microbiome in health and disease. Integr Med (Encinitas). 2014; 13(6):17-22.
Ugboko H, Nwinyi O, Oranusi S. Metagenomic profiling of gut microbiota of diarrhoeic children in southwest Nigeria. IJID. 2020; 101:181.
Soetoko AS CD, Ardiansyah F, Fatmawati D. Inulin from Dioscorea esculenta and metformin in combination ameliorates metabolic syndrome in rats by altering shortchain fatty acids. Trop J Nat Prod Res. 2023; 7(2):2421-2426.
de Vos WM, Tilg H, Van Hul M, Cani PD. Gut microbiome and health: Mechanistic insights. Gut. 2022; 71(5):1020-1032.
Kho ZY, Lal SK. The human gut microbiome - a potential controller of wellness and disease. Front Microbiol. 2018; 9:1835.
Gebrayel P, Nicco C, Al Khodor S, Bilinski J, Caselli E, Comelli EM, Egert M, Giaroni C, Karpinski TM, Loniewski I, Mulak A, Reygner J, Samczuk P, Serino M, Sikora M, Terranegra A, Ufnal M, Villeger R, Pichon C, Konturek P, Edeas M. Microbiota medicine: Towards clinical revolution.
J Transl Med. 2022; 20(1):111.
Al-Obaide MAI, Ibrahim BA, Al-Humaish S, Abdel-Salam AG. Genomic and bioinformatics approaches for analysis of genes associated with cancer risks following exposure to tobacco smoking. Front Public Health. 2018; 6:84.
Zhang J, Ni Y, Qian L, Fang Q, Zheng T, Zhang M, Gao Q, Zhang Y, Ni J, Hou X, Bao Y, Kovatcheva-Datchary P, Xu A, Li H, Panagiotou G, Jia W. Decreased abundance of Akkermansia muciniphila leads to the impairment of insulin secretion and glucose homeostasis in lean type 2 diabetes. Adv Sci (Weinh). 2021; 8(16):e2100536.
Ross MC, Muzny DM, McCormick JB, Gibbs RA, FisherHoch SP, Petrosino JF. 16s gut community of the Cameron County Hispanic cohort. Microbiome. 2015; 3(1):7-18.23. Dash NR, Al Bataineh MT. Metagenomic analysis of the gut microbiome reveals enrichment of menaquinones (vitamin k2) pathway in diabetes mellitus. Diabetes Metab J. 2021; 45(1):77-85.
Wang TY, Zhang XQ, Chen AL, Zhang J, Lv BH, Ma MH, Lian J, Wu YX, Zhou YT, Ma CC, Dong RJ, Ge DY, Gao SH, Jiang GJ. A comparative study of microbial community and functions of type 2 diabetes mellitus patients with obesity and healthy people. Appl Microbiol Biotechnol. 2020;
(16):7143-7153.
Yamashita M, Okubo H, Kobuke K, Ohno H, Oki K, Yoneda M, Tanaka J, Hattori N. Alteration of gut microbiota by a westernized lifestyle and its correlation with insulin resistance in non-diabetic Japanese men. J Diabetes Investig. 2019; 10(6):1463-1470.
Das T, Jayasudha R, Chakravarthy S, Prashanthi GS, Bhargava A, Tyagi M, Rani PK, Pappuru RR, Sharma S, Shivaji S. Alterations in the gut bacterial microbiome in people with type 2 diabetes mellitus and diabetic retinopathy. Sci Rep. 2021; 11(1):2738.
Wei B, Wang Y, Xiang S, Jiang Y, Chen R, Hu N. Alterations of gut microbiome in patients with type 2 diabetes mellitus who had undergone cholecystectomy. Am. J. Physiol. Endocrinol. 2021; 320(1):E113-E121.
Reitmeier S, Kiessling S, Clavel T, List M, Almeida EL, Ghosh TS, Neuhaus K, Grallert H, Linseisen J, Skurk T, Brandl B, Breuninger TA, Troll M, Rathmann W, Linkohr B, Hauner H, Laudes M, Franke A, Le Roy CI, Bell JT, Spector T, Baumbach J, O'Toole PW, Peters A, Haller D. Arrhythmic
gut microbiome signatures predict risk of type 2 diabetes. Cell Host Microbe. 2020; 28(2):258-272 e256.
Lambeth SM, Carson T, Lowe J, Ramaraj T, Leff JW, Luo L, Bell CJ, Shah VO. Composition, diversity and abundance of gut microbiome in prediabetes and type 2 diabetes. J Diabetes Obes. 2015; 2(3):1-7.
Salguero MV, Al-Obaide MAI, Singh R, Siepmann T, Vasylyeva TL. Dysbiosis of gram-negative gut microbiota and the associated serum lipopolysaccharide exacerbates inflammation in type 2 diabetic patients with chronic kidney disease. Exp Ther Med. 2019; 18(5):3461-3469.
Zhao X, Zhang Y, Guo R, Yu W, Zhang F, Wu F, Shang J. The alteration in composition and function of gut microbiome in patients with type 2 diabetes. J Diabetes Res. 2020; 2020:8842651.
Kitten AK, Ryan L, Lee GC, Flores BE, Reveles KR. Gut microbiome differences among Mexican Americans with and without type 2 diabetes mellitus. PloS one. 2021; 16(5):e0251245.
Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong M-L, Xu A, Chavakis T, Bornstein A, Ehrhart-Bornstein M. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: Correlation with inflammatory and metabolic parameters. J. Pharmacogenomics. 2013; 13(6):514-522.
Huang Y, Wang Z, Ma H, Ji S, Chen Z, Cui Z, Chen J, Tang S. Dysbiosis and implication of the gut microbiota in diabetic retinopathy. Front Cell Infect Microbiol. 2021; 11:646348.
Gou W, Ling CW, He Y, Jiang Z, Fu Y, Xu F, Miao Z, Sun TY, Lin JS, Zhu HL, Zhou H, Chen YM, Zheng JS. Interpretable machine learning framework reveals robust gut microbiome features associated with type 2 diabetes. Diabetes Care. 2021; 44(2):358-366.
Liu T, Chen X, Xu Y, Wu W, Tang W, Chen Z, Ji G, Peng J, Jiang Q, Xiao J, Li X, Zeng W, Xu X, Hu J, Guo Y, Zou F, Du Q, Zhou H, He Y, Ma W. Gut microbiota partially mediates the effects of fine particulate matter on type 2 diabetes: Evidence from a population-based epidemiological
study. Environ Int. 2019; 130:104882.
Khan R, Sharma A, Ravikumar R, Parekh A, Srinivasan R, George RJ, Raman R. Association between gut microbial abundance and sight-threatening diabetic retinopathy. IOVS. 2021; 62(7):19-19.
Karusheva Y, Koessler T, Strassburger K, Markgraf D, Mastrototaro L, Jelenik T, Simon MC, Pesta D, Zaharia OP, Bodis K, Barenz F, Schmoll D, Wolkersdorfer M, Tura A, Pacini G, Burkart V, Mussig K, Szendroedi J, Roden M. Short-term dietary reduction of branched-chain amino acids
reduces meal-induced insulin secretion and modifies microbiome composition in type 2 diabetes: A randomized controlled crossover trial. Am J Clin Nutr. 2019; 110(5):1098-1107.
39. Jia R, Huang M, Qian L, Yan X, Lv Q, Ye H, Ye L, Wu X, Chen W, Chen Y, Jia Y, Huang Y, Wu H. The depletion of carbohydrate metabolic genes in the gut microbiome contributes to the transition from central obesity to type 2 diabetes. Front Endocrinol (Lausanne). 2021; 12:747646.
Kim E, Kim AH, Lee Y, Ji SC, Cho JY, Yu KS, Chung JY. Effects of vancomycin-induced gut microbiome alteration on the pharmacodynamics of metformin in healthy malesubjects. Clin Transl Sci. 2021; 14(5):1955-1966.
Al Bataineh MT, Dash NR, Bel Lassen P, Banimfreg BH, Nada AM, Belda E, Clément K. Revealing links between gut microbiome and its fungal community in type 2 diabetes mellitus among Emirati subjects: A pilot study. Sci Rep. 2020; 10(1):1-11.
Radwan S, Gilfillan D, Eklund B, Radwan HM, El Menofy NG, Lee J, Kapuscinski M, Abdo Z. A comparative study of the gut microbiome in Egyptian patients with Type I and Type II diabetes. PLoS One. 2020; 15(9):e0238764.
Zhong H, Ren H, Lu Y, Fang C, Hou G, Yang Z, Chen B, Yang F, Zhao Y, Shi Z, Zhou B, Wu J, Zou H, Zi J, Chen J, Bao X, Hu Y, Gao Y, Zhang J, Xu X, Hou Y, Yang H, Wang J, Liu S, Jia H, Madsen L, Brix S, Kristiansen K, Liu F, Li J. Distinct gut metagenomics and metaproteomics signatures in
prediabetics and treatment-naive type 2 diabetics. EBioMedicine. 2019; 47:373-383.
Wang Y, Luo X, Mao X, Tao Y, Ran X, Zhao H, Xiong J, Li L. Gut microbiome analysis of type 2 diabetic patients from the Chinese minority ethnic groups the Uyghurs and Kazaks. PLoS One. 2017; 12(3):e0172774.
Wang X, Xu X, Xia Y. Further analysis reveals new gut microbiome markers of type 2 diabetes mellitus. Antonie Van Leeuwenhoek. 2017; 110(3):445-453.
Zhang Y, Gu Y, Ren H, Wang S, Zhong H, Zhao X, Ma J, Gu X, Xue Y, Huang S, Yang J, Chen L, Chen G, Qu S, Liang J, Qin L, Huang Q, Peng Y, Li Q, Wang X, Kong P, Hou G, Gao M, Shi Z, Li X, Qiu Y, Zou Y, Yang H, Wang J, Xu G, Lai S, Li J, Ning G, Wang W. Gut microbiome-related effects
of berberine and probiotics on type 2 diabetes (the premote study). Nat Commun. 2020; 11(1):5015.
Candela M, Biagi E, Soverini M, Consolandi C, Quercia S, Severgnini M, Peano C, Turroni S, Rampelli S, Pozzilli P, Pianesi M, Fallucca F, Brigidi P. Modulation of gut microbiota dysbioses in type 2 diabetic patients by macrobiotic ma-pi 2 diet. Br J Nutr. 2016; 116(1):80-93.
Zhang F, Wang M, Yang J, Xu Q, Liang C, Chen B, Zhang J, Yang Y, Wang H, Shang Y, Wang Y, Mu X, Zhu D, Zhang C, Yao M, Zhang L. Response of gut microbiota in type 2 diabetes to hypoglycemic agents. Endocrine. 2019; 66(3):485-493.
Gaike AH, Paul D, Bhute S, Dhotre DP, Pande P, Upadhyaya S, Reddy Y, Sampath R, Ghosh D, Chandraprabha D. The gut microbial diversity of newly diagnosed diabetics but not of prediabetics is significantly different from that of healthy nondiabetics. mSystems. 2020; 5(2):e00578-00519.
Bakir-Gungor B, Bulut O, Jabeer A, Nalbantoglu OU, Yousef M. Discovering potential taxonomic biomarkers of type 2 diabetes from human gut microbiota via different feature selection methods. Front Microbiol. 2021; 12:628426.
Talukdar R, Sarkar P, Jakkampudi A, Sarkar S, Aslam M, Jandhyala M, Deepika G, Unnisa M, Reddy DN. The gut microbiome in pancreatogenic diabetes differs from that of type 1 and type 2 diabetes. Sci Rep. 2021; 11(1):1-12.
Breuninger TA, Wawro N, Breuninger J, Reitmeier S, Clavel T, Six-Merker J, Pestoni G, Rohrmann S, Rathmann W, Peters A. Associations between habitual diet, metabolic disease, and the gut microbiota using latent Dirichlet allocation. Microbiome. 2021; 9(1):1-18.
Li J, Morrow C, Barnes S, Wilson L, Womack ED, McLain A, Yarar-Fisher C. Gut microbiome composition and serum metabolome profile among individuals with spinal cord injury and normal glucose tolerance or prediabetes/type 2 diabetes. Arch Phys Med Rehabil. 2022; 103(4):702-710.
Wu H, Tremaroli V, Schmidt C, Lundqvist A, Olsson LM, Kramer M, Gummesson A, Perkins R, Bergstrom G, Backhed F. The gut microbiota in prediabetes and diabetes: A population-based cross-sectional study. Cell Metab. 2020; 32(3):379-390 e373.
Yassour M, Lim MY, Yun HS, Tickle TL, Sung J, Song YM, Lee K, Franzosa EA, Morgan XC, Gevers D, Lander ES, Xavier RJ, Birren BW, Ko G, Huttenhower C. Sub-clinical detection of gut microbial biomarkers of obesity and type 2 diabetes. Genome Med. 2016; 8(1):17.
Zhang YH, Guo W, Zeng T, Zhang S, Chen L, Gamarra M, Mansour RF, Escorcia-Gutierrez J, Huang T, Cai YD. Identification of microbiota biomarkers with orthologous gene annotation for type 2 diabetes. Front Microbiol. 2021; 12:711244.
Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites. Cell. 2016; 165(6):1332-1345.
Mandøe MJ, Hansen KB, Hartmann B, Rehfeld JF, Holst JJ, Hansen HS. The 2-monoacylglycerol moiety of dietary fat appears to be responsible for the fat-induced release of GLP-1 in humans. AJCN. 2015; 102(3):548-555.
Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, Cameron J, Grosse J, Reimann F, Gribble FM. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the g-protein-coupled receptor ffar2. Diabetes. 2012; 61(2):364-371.
Cunningham AL, Stephens JW, Harris DA. Gut microbiota influence in type 2 diabetes mellitus (t2dm). Gut Pathog. 2021; 13(1):50.
Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, Petersen KF, Kibbey RG, Goodman AL, Shulman GI. Acetate mediates a microbiome-brain-beta-cell axis topromote metabolic syndrome. Nature. 2016; 534(7606):213-217.
Rosario D, Benfeitas R, Bidkhori G, Zhang C, Uhlen M, Shoaie S, Mardinoglu A. Understanding the representative gut microbiota dysbiosis in metformin-treated type 2 diabetes patients using genome-scale metabolic modeling. Front Physiol. 2018; 9:775.
Sanna S, van Zuydam NR, Mahajan A, Kurilshikov A, Vich Vila A, Võsa U, Mujagic Z, Masclee AA, Jonkers DM, Oosting M. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat. Genet. 2019; 51(4):600-605.
He J, Zhang P, Shen L, Niu L, Tan Y, Chen L, Zhao Y, Bai L, Hao X, Li X. Short-chain fatty acids and their association with signalling pathways in inflammation, glucose and lipid metabolism. Int. J. Mol. Sci. 2020; 21(17):6356.
Zhao L, Lou H, Peng Y, Chen S, Zhang Y, Li X. Comprehensive relationships between gut microbiome and faecal metabolome in individuals with type 2 diabetes and its complications. Endocrine. 2019; 66(3):526-537.
Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, Anastasovska J, Ghourab S, Hankir M, Zhang S, Carling D, Swann JR, Gibson G, Viardot A, Morrison D, Louise Thomas E, Bell JD. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun. 2014; 5(1):3611.
Aasmets O, Lull K, Lang JM, Pan C, Kuusisto J, Fischer K, Laakso M, Lusis AJ, Org E. Machine learning reveals timevarying microbial predictors with complex effects on glucose regulation. mSystems. 2021; 6(1):e01191-01120.
Alfa MJ, Strang D, Tappia PS, Olson N, DeGagne P, Bray D, Murray BL, Hiebert B. A randomized placebo-controlled clinical trial to determine the impact of digestion-resistant starch MSprebiotic((r)) on glucose, insulin, and insulin resistance in elderly and mid-age adults. Front Med
(Lausanne). 2017; 4:260.
Meijnikman AS, Gerdes VE, Nieuwdorp M, Herrema H. Evaluating causality of gut microbiota in obesity and diabetes in humans. Endocr Rev. 2018; 39(2):133-153.
Saad MJ, Santos A, Prada PO. Linking gut microbiota and inflammation to obesity and insulin resistance. Physiology (Bethesda). 2016; 31(4):283-293.
Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, Tito RY, Chaffron S, Rymenans L, Verspecht C, De Sutter L, Lima-Mendez G, D'Hoe K, Jonckheere K, Homola D, Garcia R, Tigchelaar EF, Eeckhaudt L, Fu J, Henckaerts L, Zhernakova A, Wijmenga C, Raes J. Population-level analysis of gut microbiome variation. Science. 2016; 352(6285):560-564.
Mikkelsen KH, Knop FK, Frost M, Hallas J, Pottegard A. Use of antibiotics and risk of type 2 diabetes: A populationbased case-control study. J Clin Endocrinol Metab. 2015; 100(10):3633-3640.
Therdtatha P, Song Y, Tanaka M, Mariyatun M, Almunifah M, Manurung NEP, Indriarsih S, Lu Y, Nagata K, Fukami K, Ikeda T, Lee YK, Rahayu ES, Nakayama J. Gut microbiome of Indonesian adults associated with obesity and type 2 diabetes: A cross-sectional study in an Asian city,
Yogyakarta. Microorganisms. 2021; 9(5):897-916.
Balvers M, Deschasaux M, van den Born BJ, Zwinderman K, Nieuwdorp M, Levin E. Analyzing type 2 diabetes associations with the gut microbiome in individuals from two ethnic backgrounds living in the same geographic area. Nutrients. 2021; 13(9):3289.
Elbere I, Kalnina I, Silamikelis I, Konrade I, Zaharenko L, Sekace K, Radovica-Spalvina I, Fridmanis D, Gudra D, Pirags V, Klovins J. Association of metformin administration with gut microbiome dysbiosis in healthy volunteers. PLoS One. 2018; 13(9):e0204317.
Lee Y, Kim AH, Kim E, Lee S, Yu K-S, Jang I-J, Chung JY, Cho J-Y. Changes in the gut microbiome influence the hypoglycemic effect of metformin through the altered metabolism of branched-chain and nonessential amino acids. Diabetes Res. Clin. Pract. 2021; 178:108985.
Wu H, Esteve E, Tremaroli V, Khan MT, Caesar R, Manneras-Holm L, Stahlman M, Olsson LM, Serino M, Planas-Felix M, Xifra G, Mercader JM, Torrents D, Burcelin R, Ricart W, Perkins R, Fernandez-Real JM, Backhed F. 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.
Panwar H, Rashmi HM, Batish VK, Grover S. Probiotics as potential biotherapeutics in the management of type 2 diabetes–prospects and perspectives. Diabetes Metab Res Rev. 2013; 29(2):103-112.
Primec M, Škorjanc D, Langerholc T, Mičetić-Turk D, Gorenjak M. Specific lactobacillus probiotic strains decrease transepithelial glucose transport through GLUT-2 downregulation in intestinal epithelial cell models. Nutr Res. 2021; 86:10-22.
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014; 11(8):506-514.
Louis P, Flint HJ, Michel C. How to manipulate the microbiota: Prebiotics. Hum. Microbiome J. 2016:119-142.
Isibor PO, Akinduti PA, Aworunse OS, Oyewale JO, Oshamika O, Ugboko HU, Taiwo OS, Ahuekwe EF, Obafemi YD, Onibokun EA, Oziegbe O, Oniha MI, Olopade BK, Atolagbe OM, Adekeye BT, Ajiboye IB, Bello OA, Popoola JO, Ayanda OI, Akinnola OO, Olasehinde GI, Eni AO, Nwinyi OC, Omonhinmin CA, Oranusi SU, Obembe OO. Significance of African diets in biotherapeutic modulation of the gut microbiome. Bioinform Biol Insights. 2021; 15:11779322211012697.
Swanson KS, Gibson GR, Hutkins R, Reimer RA, Reid G, Verbeke K, Scott KP, Holscher HD, Azad MB, Delzenne NM, Sanders ME. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol. 2020; 17(11):687-701.
Palacios T, Vitetta L, Coulson S, Madigan CD, Denyer GS, Caterson ID. The effect of a novel probiotic on metabolic biomarkers in adults with prediabetes and recently diagnosed type 2 diabetes mellitus: Study protocol for a randomized controlled trial. Trials. 2017; 18(1):7-15.
Barbaza MYU DC-CK, ,RamosJLT, Hsieh CL,Tsai PW. . Synergistic antidiabetic activity of extracts of Asystasia gangetica and Morus alba. Trop J Nat Prod Res. . 2021; 5(2):243-247.
Siregar RS HR, Kamil I, Nazir N, Nofialdi N. . Ginger (Zingiber officinaler.) as a potent medicinal plant for the prevention and treatment of diabetes mellitus: A review. Trop J Nat Prod Res. 2022; 6(4):462-469.
de Groot P, Nikolic T, Pellegrini S, Sordi V, Imangaliyev S, Rampanelli E, Hanssen N, Attaye I, Bakker G, Duinkerken G, Joosten A, Prodan A, Levin E, Levels H, Potter van Loon B, van Bon A, Brouwer C, van Dam S, Simsek S, van Raalte D, Stam F, Gerdes V, Hoogma R, Diekman M, Gerding M, Rustemeijer C, de Bakker B, Hoekstra J, Zwinderman A, Bergman J, Holleman F, Piemonti L, De Vos W, Roep B, Nieuwdorp M. Faecal microbiota transplantation halts progression of human new-onset type 1 diabetes in a randomized controlled trial. Gut. 2021; 70(1):92-105.
Ahmad A, Yang W, Chen G, Shafiq M, Javed S, Ali Zaidi SS, Shahid R, Liu C, Bokhari H. Analysis of gut microbiota of obese individuals with type 2 diabetes and healthy individuals. PLoS One. 2019; 14(12):e0226372.
Chen Z, Radjabzadeh D, Chen L, Kurilshikov A, Kavousi M, Ahmadizar F, Ikram MA, Uitterlinden AG, Zhernakova A, Fu J, Kraaij R, Voortman T. Association of insulin resistance and type 2 diabetes with gut microbial diversity: A microbiome-wide analysis from population studies. JAMA
Netw Open. 2021; 4(7):e2118811.
Elbere I, Silamikelis I, Dindune II, Kalnina I, Ustinova M,Zaharenko L, Silamikele L, Rovite V, Gudra D, Konrade I, Sokolovska J, Pirags V, Klovins J. Baseline gut microbiome composition predicts metformin therapy short-term efficacy in newly diagnosed type 2 diabetes patients. PLoS One. 2020; 15(10):e0241338.
Ghosh TS, Arnoux J, O'Toole PW. Metagenomic analysis reveals distinct patterns of gut lactobacillus prevalence, abundance, and geographical variation in health and disease. Gut Microbes. 2020; 12(1):1-19.
Horvath A, Leber B, Feldbacher N, Tripolt N, Rainer F, Blesl A, Trieb M, Marsche G, Sourij H, Stadlbauer V. 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, placebocontrolled pilot study. Eur J Nutr. 2020; 59(7):2969-2983.
Labbe A, Ganopolsky JG, Martoni CJ, Prakash S, Jones ML. Bacterial bile metabolizing gene abundance in Crohn's, ulcerative colitis and type 2 diabetes metagenomes. PLoS One. 2014; 9(12):e115175.
Li Q, Chang Y, Zhang K, Chen H, Tao S, Zhang Z. Implication of the gut microbiome composition of type 2 diabetic patients from northern China. Sci Rep. 2020; 10(1):5450-5458.
Liu F, Li P, Chen M, Luo Y, Prabhakar M, Zheng H, He Y, Qi Q, Long H, Zhang Y, Sheng H, Zhou H.Fructooligosaccharide (FOS) and galactooligosaccharide (GOS) increase bifidobacterium but reduce butyrateproducing bacteria with adverse glycemic metabolism in healthy young populations. Sci Rep. 2017; 7(1):11789-11801.
Menni C, Zhu J, Le Roy CI, Mompeo O, Young K, Rebholz CM, Selvin E, North KE, Mohney RP, Bell JT, Boerwinkle E, Spector TD, Mangino M, Yu B, Valdes AM. Serum metabolites reflecting gut microbiome alpha diversity predict type 2 diabetes. Gut Microbes. 2020; 11(6):1632-1642.
Alvarez-Silva C, Kashani A, Hansen TH, Pinna NK, Anjana RM, Dutta A, Saxena S, Stoy J, Kampmann U, Nielsen T, Jorgensen T, Gnanaprakash V, Gnanavadivel R, Sukumaran A, Rani CSS, Faerch K, Radha V, Balasubramanyam M, Nair GB, Das B, Vestergaard H, Hansen T, Mande SS, Mohan V, Arumugam M, Pedersen O. Trans-ethnic gut microbiota signatures of type 2 diabetes in Denmark and India. Genome Med. 2021; 13(1):37.
Shi Q, Wang Q, Zhong H, Li D, Yu S, Yang H, Wang C, Yin Z. Roux-en-y gastric bypass improved insulin resistance via alteration of the human gut microbiome and alleviation of endotoxemia. Biomed Res Int. 2021; 2021:5554991.
Si J, Lee G, You HJ, Joo SK, Lee DH, Ku BJ, Park S, Kim W, Ko G. Gut microbiome signatures distinguish type 2 diabetes mellitus from non-alcoholic fatty liver disease. Comput Struct Biotechnol J. 2021; 19:5920-5930.
Takewaki F, Nakajima H, Takewaki D, Hashimoto Y, Majima S, Okada H, Senmaru T, Ushigome E, Hamaguchi M, Yamazaki M, Tanaka Y, Nakajima S, Ohno H, Fukui M. Habitual dietary intake affects the altered pattern of gut microbiome by acarbose in patients with type 2 diabetes. Nutrients. 2021; 13(6):2107.
Tily H, Patridge E, Cai Y, Gopu V, Gline S, Genkin M, Lindau H, Sjue A, Slavov I, Perlina A, Klitgord N, Messier H, Vuyisich M, Banavar G. Gut microbiome activity contributes to prediction of individual variation in glycemic response in adults. Diabetes Ther. 2022; 13(1):89-111.
Wang M, Doak TG, Ye Y. Subtractive assembly for comparative metagenomics, and its application to type 2 diabetes metagenomes. Genome Biol. 2015; 16(1):243-258.
Watanabe M, Sianoya A, Mishima R, Therdtatha P, Rodriguez A, Ramos DC, Lee YK, Dalmacio LM, Nakayama J. Gut microbiome status of urban and rural Filipino adults in relation to diet and metabolic disorders. FEMS Microbiol Lett. 2021; 368(20):fnab149.
Wu H, Cai L, Li D, Wang X, Zhao S, Zou F, Zhou K. Metagenomics biomarkers selected for prediction of three different diseases in Chinese population. Biomed Res Int. 2018; 2018:2936257.
Zhang Z, Tian T, Chen Z, Liu L, Luo T, Dai J. Characteristics of the gut microbiome in patients with prediabets and type 2 diabetes. PeerJ. 2021; 9:e10952.