Abstract
Background
Regarding the role of gut microbial dysbiosis in hyperglycemia, we aimed to compare the main gut bacterial composition among type 1 and type 2 diabetic patients and healthy non-diabetic adults.
Methods
A total of 110 adult subjects (49 patients diagnosed with type 2 diabetes, 21 patients diagnosed with type 1 diabetes and 40 healthy persons) were included in this case-control study. The intestinal microbiota composition was investigated by quantitative real-time polymerase chain reaction (qPCR) method targeting bacterial 16S rRNA gene. Comparison between three groups was done using one-way analysis of variance.
Results
The participants’ mean age in the type 1 diabetes, type 2 diabetes and control groups was 35.4, 57.2 and 38.0 years, respectively. Higher level of Escherichia, Prevotella and Lactobacillus was observed in both type 1 and type 2 diabetic patients compared with the healthy group (P ˂0.001). In contrast, bacterial load of Bifidobacterium, Roseburia and Bacteroides was higher in healthy control group (P < 0.05). Faecalibacterium was significantly lower in type 1 diabetic patients compared with the other two groups (P ˂0.001). No significant difference was found in Akkermansia level among three groups.
Conclusions
Gut microbial alterations have been observed among patients suffering from type 1 and type 2 diabetes mellitus and healthy control adults. Butyrate producing genera including Roseburia and Faecalibacterium decreased while Escherichia, Prevotella and Lactobacillus increased in diabetic patients compared to healthy subjects. Modulating approaches of gut microbiota composition could be helpful in diabetes management.
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Data Availability
Data will be provided in case of requesting.
References
Unwin N, Gan D, Whiting D. The IDF diabetes atlas: providing evidence, raising awareness and promoting action. Diabetes Res Clin Pract. 2010;87(1):2–3.
Ejtahed HS, Soroush AR, Angoorani P, Larijani B, Hasani-Ranjbar S. Gut Microbiota as a Target in the Pathogenesis of Metabolic Disorders: A New Approach to Novel Therapeutic Agents. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme. 2016;48(6):349–58.
Tilg H, Moschen AR. Microbiota and diabetes: an evolving relationship. Gut. 2014;63(9):1513–21.
Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012;336(6086):1262–7.
Ejtahed HS, Hasani-Ranjbar S, Larijani B. Human microbiome as an approach to personalized medicine. Altern Ther Health Med. 2017;23(6):8–9.
Ejtahed HS, Soroush AR, Siadat SD, Hoseini-Tavassol Z, Larijani B, Hasani-Ranjbar S. Targeting obesity management through gut microbiota modulation by herbal products: a systematic review. Complementary therapies in medicine. 2019;42:184–204.
Ejtahed HS, Angoorani P, Hasani-Ranjbar S, Siadat SD, Ghasemi N, Larijani B, et al. Adaptation of human gut microbiota to bariatric surgeries in morbidly obese patients: a systematic review. Microb Pathog. 2018;116:13–21.
Everard A, Cani PD. Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol. 2013;27(1):73–83.
Erejuwa O, Sulaiman S, Wahab M. Modulation of gut microbiota in the management of metabolic disorders: the prospects and challenges. Int J Mol Sci. 2014;15(3):4158–88.
Ejtahed HS, Hasani-Ranjbar S. Neuromodulatory effect of microbiome on gut-brain axis; new target for obesity drugs. 2019;18(1):263–5.
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.
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.
Gulden E, Wong FS, Wen L. The gut microbiota and Type 1 Diabetes. Clinical immunology (Orlando, Fla). 2015;159(2):143–53.
Brown CT, Davis-Richardson AG, Giongo A, Gano KA, Crabb DB, Mukherjee N, et al. Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PLoS One. 2011;6(10):e25792.
Gérard C, Vidal H. Impact of gut microbiota on host glycemic control. Front Endocrinol. 2019;10:29.
Bartosch S, Fite A, Macfarlane GT, McMurdo ME. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol. 2004;70(6):3575–81.
Fitzgerald CB, Shkoporov AN. Comparative analysis of Faecalibacterium prausnitzii genomes shows a high level of genome plasticity and warrants separation into new species-level taxa 2018;19(1):931.
Gregory KE, LaPlante RD, Shan G, Kumar DV, Gregas M. Mode of birth influences preterm infant intestinal colonization with Bacteroides over the early neonatal period. Advances in neonatal care : official journal of the National Association of Neonatal Nurses. 2015;15(6):386–93.
Kanno T, Matsuki T, Oka M, Utsunomiya H, Inada K, Magari H, et al. Gastric acid reduction leads to an alteration in lower intestinal microflora. Biochem Biophys Res Commun. 2009;381(4):666–70.
Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5(2):e9085.
Payne AN, Chassard C, Banz Y, Lacroix C. The composition and metabolic activity of child gut microbiota demonstrate differential adaptation to varied nutrient loads in an in vitro model of colonic fermentation. FEMS Microbiol Ecol. 2012;80(3):608–23.
Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol. 2004;97(6):1166–77.
Schneeberger M, Everard A, Gómez-Valadés AG, Matamoros S, Ramírez S, Delzenne NM, et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5:16643.
Karlsson FH, Tremaroli V, Nookaew I, Bergström G, Behre CJ, Fagerberg B, et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498:99.
Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60.
Leiva-Gea I, Sanchez-Alcoholado L, Martin-Tejedor B, Castellano-Castillo D, Moreno-Indias I, Urda-Cardona A, et al. Gut Microbiota Differs in Composition and Functionality Between Children With Type 1 Diabetes and MODY2 and Healthy Control Subjects: A Case-Control Study. 2018;41(11):2385–95.
Mejia-Leon ME, Petrosino JF, Ajami NJ, Dominguez-Bello MG, de la Barca AM. Fecal microbiota imbalance in Mexican children with type 1 diabetes. Sci Rep. 2014;4:3814.
Murri M, Leiva I, Gomez-Zumaquero JM, Tinahones FJ, Cardona F, Soriguer F, et al. Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case-control study. BMC Med. 2013;11:46.
Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–80.
Hjorth MF, Blædel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P, et al. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes. 2019;43(1):149–57.
Tamanai-Shacoori Z, Smida I, Bousarghin L, Loreal O, Meuric V, Fong SB, et al. Roseburia spp.: a marker of health? Future Microbiol. 2017;12:157–70.
Huang Y, Li SC, Hu J, Ruan HB, Guo HM, Zhang HH, et al. Gut microbiota profiling in Han Chinese with type 1 diabetes. Diabetes Res Clin Pract. 2018;141:256–63.
Zhang X, Shen D, Fang Z, Jie Z, Qiu X, Zhang C, et al. Human gut microbiota changes reveal the progression of glucose intolerance. PLoS One. 2013;8(8):e71108.
Endesfelder D, Engel M, Davis-Richardson AG, Ardissone AN, Achenbach P, Hummel S, et al. Towards a functional hypothesis relating anti-islet cell autoimmunity to the dietary impact on microbial communities and butyrate production. Microbiome. 2016;4:17.
Siljander H, Honkanen J, Knip M. Microbiome and type 1 diabetes. EBioMedicine. 2019;46:512–21.
Sedighi M, Razavi S, Navab-Moghadam F, Khamseh ME, Alaei-Shahmiri F, Mehrtash A, et al. Comparison of gut microbiota in adult patients with type 2 diabetes and healthy individuals. Microb Pathog. 2017;111:362–9.
Ordiz MI, May TD, Mihindukulasuriya K, Martin J, Crowley J, Tarr PI, et al. The effect of dietary resistant starch type 2 on the microbiota and markers of gut inflammation in rural Malawi children. Microbiome. 2015;3:37.
Halawa MR, El-Salam MA, Mostafa BM, Sallout SS. The gut microbiome, Lactobacillus acidophilus; relation with type 2 diabetes mellitus. Curr Diabetes Rev. 2019.
Soyucen E, Gulcan A, Aktuglu-Zeybek AC, Onal H, Kiykim E, Aydin A. Differences in the gut microbiota of healthy children and those with type 1 diabetes. Pediatrics international: official journal of the Japan Pediatric Society. 2014;56(3):336–43.
Ejtahed H-S, Tito RY, Siadat S-D, Hasani-Ranjbar S, Hoseini-Tavassol Z, Rymenans L, et al. Metformin induces weight loss associated with gut microbiota alteration in non-diabetic obese women: a randomized double-blind clinical trial. European journal of endocrinology. 2018;1(aop).
Forslund K, Hildebrand F, Nielsen T, Falony G, Le Chatelier E, Sunagawa S, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature. 2015;528(7581):262–6.
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This work was supported by the National Institute for Medical Research Development (NIMAD) (grant number: 940604).
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Ejtahed, HS., Hoseini-Tavassol, Z., Khatami, S. et al. Main gut bacterial composition differs between patients with type 1 and type 2 diabetes and non-diabetic adults. J Diabetes Metab Disord 19, 265–271 (2020). https://doi.org/10.1007/s40200-020-00502-7
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DOI: https://doi.org/10.1007/s40200-020-00502-7