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Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Systematic Review Article

Association between Gut Microbiota Compositions with Microvascular Complications in Individuals with Diabetes: A Systematic Review

Author(s): Motahareh Hasani*, Zahra Asadi Pilerud, Atefe Kami, Amir Abbas Vaezi*, Sahar Sobhani, Hanieh-Sadat Ejtahed and Mostafa Qorbani

Volume 20, Issue 10, 2024

Published on: 24 January, 2024

Article ID: e240124226068 Pages: 16

DOI: 10.2174/0115733998280396231212114345

Price: $65

Abstract

Background: Diabetes is one of the chronic and very complex diseases that can lead to microvascular complications. Recent evidence demonstrates that dysbiosis of the microbiota composition might result in low-grade, local, and systemic inflammation, which contributes directly to the development of diabetes mellitus and its microvascular consequences.

Objective: The aim of this systematic review was to investigate the association between diabetes microvascular complications, including retinopathy, neuropathy, nephropathy, and gut microbiota composition.

Methods: A systematic search was carried out in PubMed, Scopus, and ISI Web of Science from database inception to March 2023. Screening, data extraction, and quality assessment were performed by two independent authors. The Newcastle-Ottawa Quality Assessment Scale was used for quality assessment.

Results: About 19 articles were selected from 590 retrieved articles. Among the included studies, nephropathy has been studied more than other complications of diabetes, showing that the composition of the healthy microbiota is changed, and large quantities of uremic solutes that cause kidney injury are produced by gut microbes. Phyla, including Fusobacteria and Proteobacteria, accounted for the majority of the variation in gut microbiota between Type 2 diabetic patients with and without neuropathy. In cases with retinopathy, an increase in pathogenic and proinflammatory bacteria was observed.

Conclusion: Our results revealed that increases in Bacteroidetes, Proteobacteria and Fusobacteria may be associated with the pathogenesis of diabetic nephropathy, neuropathy, and retinopathy.

In view of the detrimental role of intestinal dysbiosis in the development of diabetes-related complications, gut microbiota assessment may be used as a biomarker in the future and interventions that modulate the composition of microbiota in individuals with diabetes can be used to prevent and control these complications.

Keywords: Diabetes, microvascular complications, retinopathy, neuropathy, nephropathy, gut microbiota.

[1]
Heald AH, Stedman M, Davies M, et al. Estimating life years lost to diabetes: Outcomes from analysis of national diabetes audit and office of national statistics data. Cardiovasc Endocrinol Metab 2020; 9(4): 183-5.
[http://dx.doi.org/10.1097/XCE.0000000000000210] [PMID: 33225235]
[2]
Sun H, Saeedi P, Karuranga S, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 2022; 183: 109119.
[http://dx.doi.org/10.1016/j.diabres.2021.109119] [PMID: 34879977]
[3]
Evans M, Chandramouli AS, Faurby M, Matthiessen KS, Mogensen PB, Verma S. Healthcare costs and hospitalizations in US patients with type 2 diabetes and cardiovascular disease: A retrospective database study (OFFSET). Diabetes Obes Metab 2022; 24(7): 1300-9.
[http://dx.doi.org/10.1111/dom.14703] [PMID: 35504854]
[4]
Ali A, Al-Awkally N-AM, Ahmer A, et al. Diabetes mellitus and renal failure effect on intestinal insulin. Brilliance. Research of Artificial Intelligence 2022; 2(3): 102-6.
[5]
Yousri NA, Suhre K, Yassin E, et al. Metabolic and metabo-clinical signatures of type 2 diabetes, obesity, retinopathy, and dyslipidemia. Diabetes 2022; 71(2): 184-205.
[http://dx.doi.org/10.2337/db21-0490] [PMID: 34732537]
[6]
Chan JCN, Lim LL, Wareham NJ, et al. The Lancet Commission on diabetes: Using data to transform diabetes care and patient lives. Lancet 2020; 396(10267): 2019-82.
[http://dx.doi.org/10.1016/S0140-6736(20)32374-6] [PMID: 33189186]
[7]
Magliano DJ, Islam RM, Barr EL, et al. Trends in incidence of total or type 2 diabetes: Systematic review. BMJ 2019; 366.
[8]
Organization WH. Global report on diabetes. World Health Organization 2016.
[9]
Baothman OA, Zamzami MA, Taher I, Abubaker J, Abu-Farha M. The role of gut microbiota in the development of obesity and Diabetes. Lipids Health Dis 2016; 15(1): 108.
[http://dx.doi.org/10.1186/s12944-016-0278-4] [PMID: 27317359]
[10]
Cox AJ, West NP, Cripps AW. Obesity, inflammation, and the gut microbiota. Lancet Diabetes Endocrinol 2015; 3(3): 207-15.
[http://dx.doi.org/10.1016/S2213-8587(14)70134-2] [PMID: 25066177]
[11]
Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 2012; 3(4): 279-88.
[http://dx.doi.org/10.4161/gmic.19625] [PMID: 22572877]
[12]
Kallus SJ, Brandt LJ. The intestinal microbiota and obesity. J Clin Gastroenterol 2012; 46(1): 16-24.
[http://dx.doi.org/10.1097/MCG.0b013e31823711fd] [PMID: 22064556]
[13]
Aspord C, Thivolet C. Nasal administration of CTB-insulin induces active tolerance against autoimmune diabetes in non-obese diabetic (NOD) mice. Clin Exp Immunol 2002; 130(2): 204-11.
[http://dx.doi.org/10.1046/j.1365-2249.2002.01988.x] [PMID: 12390307]
[14]
Pflughoeft KJ, Versalovic J. Human microbiome in health and disease. Annu Rev Pathol 2012; 7(1): 99-122.
[http://dx.doi.org/10.1146/annurev-pathol-011811-132421] [PMID: 21910623]
[15]
Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med 2016; 375(24): 2369-79.
[http://dx.doi.org/10.1056/NEJMra1600266] [PMID: 27974040]
[16]
Brown JM, Hazen SL. Microbial modulation of cardiovascular disease. Nat Rev Microbiol 2018; 16(3): 171-81.
[http://dx.doi.org/10.1038/nrmicro.2017.149] [PMID: 29307889]
[17]
Thomas RL, Halim S, Gurudas S, Sivaprasad S, Owens DR. IDF Diabetes Atlas: A review of studies utilising retinal photography on the global prevalence of diabetes related retinopathy between 2015 and 2018. Diabetes Res Clin Pract 2019; 157: 107840.
[http://dx.doi.org/10.1016/j.diabres.2019.107840] [PMID: 31733978]
[18]
Gandhi M, Fargo E, Prasad-Reddy L, Mahoney KM, Isaacs D. Diabetes: How to manage diabetic peripheral neuropathy. Drugs in Context 2022; 11
[19]
Roesch LFW, Lorca GL, Casella G, et al. Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. ISME J 2009; 3(5): 536-48.
[http://dx.doi.org/10.1038/ismej.2009.5] [PMID: 19225551]
[20]
de Vos WM, Nieuwdorp M. A gut prediction. Nature 2013; 498(7452): 48-9.
[http://dx.doi.org/10.1038/nature12251] [PMID: 23719383]
[21]
Forslund K, Hildebrand F, Nielsen T, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 2015; 528(7581): 262-6.
[http://dx.doi.org/10.1038/nature15766] [PMID: 26633628]
[22]
Rozanova GN, Voevodin DA, Stenina MA, Kushnareva MV. Pathogenetic role of dysbacteriosis in the development of complications of type 1 diabetes mellitus in children. Bull Exp Biol Med 2002; 133(2): 164-6.
[http://dx.doi.org/10.1023/A:1015503006854] [PMID: 12428285]
[23]
Du X, Liu J, Xue Y, et al. Alteration of gut microbial profile in patients with diabetic nephropathy. Endocrine 2021; 73(1): 71-84.
[http://dx.doi.org/10.1007/s12020-021-02721-1] [PMID: 33905112]
[24]
Zhang P, Fang J, Li G, et al. Sex differences in fecal microbiota correlation with physiological and biochemical indices associated with end-stage renal disease caused by immunoglobulin a nephropathy or diabetes. Front Microbiol 2021; 12: 752393.
[http://dx.doi.org/10.3389/fmicb.2021.752393] [PMID: 34899638]
[25]
Zhong C, Dai Z, Chai L, et al. The change of gut microbiota‐derived short‐chain fatty acids in diabetic kidney disease. J Clin Lab Anal 2021; 35(12): e24062.
[http://dx.doi.org/10.1002/jcla.24062] [PMID: 34689373]
[26]
Yu W, Shang J, Guo R, et al. The gut microbiome in differential diagnosis of diabetic kidney disease and membranous nephropathy. Ren Fail 2020; 42(1): 1100-10.
[http://dx.doi.org/10.1080/0886022X.2020.1837869] [PMID: 33121301]
[27]
Chen W, Zhang M, Guo Y, et al. The profile and function of gut microbiota in diabetic nephropathy. Diabetes Metab Syndr Obes 2021; 14: 4283-96.
[http://dx.doi.org/10.2147/DMSO.S320169] [PMID: 34703261]
[28]
Tao S, Li L, Li L, et al. Understanding the gut–kidney axis among biopsy-proven diabetic nephropathy, type 2 diabetes mellitus and healthy controls: An analysis of the gut microbiota composition. Acta Diabetol 2019; 56(5): 581-92.
[http://dx.doi.org/10.1007/s00592-019-01316-7] [PMID: 30888537]
[29]
Wang Y, Ye X, Ding D, Lu Y. Characteristics of the intestinal flora in patients with peripheral neuropathy associated with type 2 diabetes. J Int Med Res 2020; 48(9)
[http://dx.doi.org/10.1177/0300060520936806] [PMID: 32938282]
[30]
Du Y, Neng Q, Li Y, et al. Gastrointestinal autonomic neuropathy exacerbates gut microbiota dysbiosis in adult patients with type 2 diabetes mellitus. Front Cell Infect Microbiol 2022; 11: 804733.
[http://dx.doi.org/10.3389/fcimb.2021.804733] [PMID: 35211420]
[31]
Ye P, Zhang X, Xu Y, Xu J, Song X, Yao K. Alterations of the gut microbiome and metabolome in patients with proliferative diabetic retinopathy. Front Microbiol 2021; 12: 667632.
[http://dx.doi.org/10.3389/fmicb.2021.667632] [PMID: 34566901]
[32]
Huang Y, Wang Z, Ma H, et al. Dysbiosis and implication of the gut microbiota in diabetic retinopathy. Front Cell Infect Microbiol 2021; 11: 646348.
[http://dx.doi.org/10.3389/fcimb.2021.646348] [PMID: 33816351]
[33]
Zhou Z, Zheng Z, Xiong X, et al. Gut microbiota composition and fecal metabolic profiling in patients with diabetic retinopathy. Front Cell Dev Biol 2021; 9: 732204.
[http://dx.doi.org/10.3389/fcell.2021.732204] [PMID: 34722512]
[34]
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): 526-37.
[http://dx.doi.org/10.1007/s12020-019-02103-8] [PMID: 31591683]
[35]
Das T, Jayasudha R, Chakravarthy S, et al. Alterations in the gut bacterial microbiome in people with type 2 diabetes mellitus and diabetic retinopathy. Sci Rep 2021; 11(1): 2738.
[http://dx.doi.org/10.1038/s41598-021-82538-0] [PMID: 33531650]
[36]
Khan R, Sharma A, Ravikumar R, et al. Association between gut microbial abundance and sight-threatening diabetic retinopathy. Invest Ophthalmol Vis Sci 2021; 62(7): 19.
[http://dx.doi.org/10.1167/iovs.62.7.19] [PMID: 34132747]
[37]
Winther SA, Mannerla MM, Frimodt-Møller M, et al. Faecal biomarkers in type 1 diabetes with and without diabetic nephropathy. Sci Rep 2021; 11(1): 15208.
[http://dx.doi.org/10.1038/s41598-021-94747-8] [PMID: 34312454]
[38]
Gradisteanu G, Stoica R, Petcu L, et al. Microbiota signatures in type-2 diabetic patients with chronic kidney disease-a pilot study. Journal of Mind and Medical Sciences 2019; 6(1): 130-6.
[http://dx.doi.org/10.22543/7674.61.P130136]
[39]
Moubayed NMS, Bhat RS, Al Farraj D, Dihani NA, El Ansary A, Fahmy RM. Screening and identification of gut anaerobes (Bacteroidetes) from human diabetic stool samples with and without retinopathy in comparison to control subjects. Microb Pathog 2019; 129: 88-92.
[http://dx.doi.org/10.1016/j.micpath.2019.01.025] [PMID: 30708043]
[40]
Singh H, Yu Y, Suh MJ, et al. Type 1 Diabetes: Urinary proteomics and protein network analysis support perturbation of lysosomal function. Theranostics 2017; 7(10): 2704-17.
[http://dx.doi.org/10.7150/thno.19679] [PMID: 28819457]
[41]
Więdłocha M, Marcinowicz P, Janoska-Jaździk M, Szulc A. Gut microbiota, kynurenine pathway and mental disorders-review. Prog Neuropsychopharmacol Biol Psychiatry 2021; 106: 110145.
[http://dx.doi.org/10.1016/j.pnpbp.2020.110145] [PMID: 33203568]
[42]
Kim JE, Nam H, Park JI, et al. Gut microbial genes and metabolism for methionine and branched-chain amino acids in diabetic nephropathy. Microbiol Spectr 2023; 11(2): e02344-22.
[http://dx.doi.org/10.1128/spectrum.02344-22] [PMID: 36877076]
[43]
Zhang L, Wang Z, Zhang X, et al. Alterations of the gut microbiota in patients with diabetic nephropathy. Microbiol Spectr 2022; 10(4): e00324-22.
[http://dx.doi.org/10.1128/spectrum.00324-22] [PMID: 35863004]
[44]
Fan G, Cao F, Kuang T, et al. Alterations in the gut virome are associated with type 2 diabetes and diabetic nephropathy. Gut Microbes 2023; 15(1): 2226925.
[http://dx.doi.org/10.1080/19490976.2023.2226925] [PMID: 37349979]
[45]
Li L, Yang K, Li C, et al. Metagenomic shotgun sequencing and metabolomic profiling identify specific human gut microbiota associated with diabetic retinopathy in patients with type 2 diabetes. Front Immunol 2022; 13: 943325.
[http://dx.doi.org/10.3389/fimmu.2022.943325] [PMID: 36059453]
[46]
Bai J, Wan Z, Zhang Y, Wang T, Xue Y, Peng Q. Composition and diversity of gut microbiota in diabetic retinopathy. Front Microbiol 2022; 13: 926926.
[http://dx.doi.org/10.3389/fmicb.2022.926926] [PMID: 36081798]
[47]
Winther SA, Henriksen P, Vogt JK, et al. Gut microbiota profile and selected plasma metabolites in type 1 diabetes without and with stratification by albuminuria. Diabetologia 2020; 63(12): 2713-24.
[http://dx.doi.org/10.1007/s00125-020-05260-y] [PMID: 32886190]
[48]
Padakandla SR, Das T, Sai Prashanthi G, et al. Dysbiosis in the gut microbiome in streptozotocin-induced diabetes rats and follow-up during retinal changes. Invest Ophthalmol Vis Sci 2021; 62(10): 31.
[http://dx.doi.org/10.1167/iovs.62.10.31] [PMID: 34431974]
[49]
Di S, Yao C, Qiao L, et al. Exploration of the mechanisms underlying the beneficial effect of Luo Tong formula on retinal function in diabetic rats via the “gut microbiota–inflammation–retina” axis. Chin Med 2022; 17(1): 133.
[http://dx.doi.org/10.1186/s13020-022-00688-3] [PMID: 36461068]
[50]
Wang P, Wang T, Zheng X, Cui W, Shang J, Zhao Z. Gut microbiota, key to unlocking the door of diabetic kidney disease. Nephrology 2021; 26(8): 641-9.
[http://dx.doi.org/10.1111/nep.13874] [PMID: 33715272]
[51]
Zhang M, Yang L, Zhu M, et al. Moutan Cortex polysaccharide ameliorates diabetic kidney disease via modulating gut microbiota dynamically in rats. Int J Biol Macromol 2022; 206: 849-60.
[http://dx.doi.org/10.1016/j.ijbiomac.2022.03.077] [PMID: 35307460]
[52]
Mosterd CM, Kanbay M, van den Born BJH, van Raalte DH, Rampanelli E. Intestinal microbiota and diabetic kidney diseases: The Role of microbiota and derived metabolites inmodulation of renal inflammation and disease progression. Best Pract Res Clin Endocrinol Metab 2021; 35(3): 101484.
[http://dx.doi.org/10.1016/j.beem.2021.101484] [PMID: 33546983]
[53]
Yang Y, Wu C. Traditional chinese medicine in ameliorating diabetic kidney disease via modulating gut microbiota. Integrative Medicine in Nephrology and Andrology 2021; 8(1): 8.
[http://dx.doi.org/10.4103/imna.imna_28_21]
[54]
Hida M, Aiba Y, Sawamura S, Suzuki N, Satoh T, Koga Y. Inhibition of the accumulation of uremic toxins in the blood and their precursors in the feces after oral administration of Lebenin, a lactic acid bacteria preparation, to uremic patients undergoing hemodialysis. Nephron 1996; 74(2): 349-55.
[http://dx.doi.org/10.1159/000189334] [PMID: 8893154]
[55]
Kikuchi K, Saigusa D, Kanemitsu Y, et al. Gut microbiome-derived phenyl sulfate contributes to albuminuria in diabetic kidney disease. Nat Commun 2019; 10(1): 1835.
[http://dx.doi.org/10.1038/s41467-019-09735-4] [PMID: 31015435]
[56]
Lu C, Hu Z, Wang R, et al. Gut microbiota dysbiosis-induced activation of the intrarenal renin–angiotensin system is involved in kidney injuries in rat diabetic nephropathy. Acta Pharmacol Sin 2020; 41(8): 1111-8.
[http://dx.doi.org/10.1038/s41401-019-0326-5] [PMID: 32203081]
[57]
Liu JR, Miao H, Deng DQ, Vaziri ND, Li P, Zhao YY. Gut microbiota-derived tryptophan metabolism mediates renal fibrosis by aryl hydrocarbon receptor signaling activation. Cell Mol Life Sci 2021; 78(3): 909-22.
[http://dx.doi.org/10.1007/s00018-020-03645-1] [PMID: 32965514]
[58]
Pawlak K, Myśliwiec M, Pawlak D. Kynurenine pathway – a new link between endothelial dysfunction and carotid atherosclerosis in chronic kidney disease patients. Adv Med Sci 2010; 55(2): 196-203.
[http://dx.doi.org/10.2478/v10039-010-0015-6] [PMID: 20439183]
[59]
Hirayama A, Nakashima E, Sugimoto M, et al. Metabolic profiling reveals new serum biomarkers for differentiating diabetic nephropathy. Anal Bioanal Chem 2012; 404(10): 3101-9.
[http://dx.doi.org/10.1007/s00216-012-6412-x] [PMID: 23052862]
[60]
Wei H, Wang L, An Z, et al. QiDiTangShen granules modulated the gut microbiome composition and improved bile acid profiles in a mouse model of diabetic nephropathy. Biomed Pharmacother 2021; 133: 111061.
[http://dx.doi.org/10.1016/j.biopha.2020.111061] [PMID: 33378964]
[61]
Sanmiguel C, Gupta A, Mayer EA. Gut Microbiome and Obesity: A Plausible Explanation for Obesity. Curr Obes Rep 2015; 4(2): 250-61.
[http://dx.doi.org/10.1007/s13679-015-0152-0] [PMID: 26029487]
[62]
Ridaura V. col. La microbiota intestinal de gemelos discordantes para la obesidad modula el metabolismo en ratones. Science 2013; 341: 1241214.
[http://dx.doi.org/10.1126/science.1241214] [PMID: 24009397]

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