Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-05-27T22:31:14.229Z Has data issue: false hasContentIssue false

Association of the short-chain fatty acid levels and dietary quality with type 2 diabetes: a case–control study based on Henan Rural Cohort

Published online by Cambridge University Press:  12 February 2024

Jia Li
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Yuqian Li
Affiliation:
Department of Clinical Pharmacology, School of Pharmaceutical Science, Zhengzhou University, Zhengzhou, Henan, People’s Republic of China
Shuhua Zhang
Affiliation:
Comprehensive Laboratory, Puyang Quality and Technical Supervision, Inspection and Testing Center, Puyang, Henan, People’s Republic of China
Chongjian Wang
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Zhenxing Mao
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Wenqian Huo
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Tianyu Yang
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Yan Li
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Wenguo Xing
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
Linlin Li*
Affiliation:
Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, People’s Republic of China
*
*Corresponding author: Linlin Li, email 13623850209@163.com

Abstract

Evidence of the relationship between fecal short-chain fatty acids (SCFA) levels, dietary quality and type 2 diabetes mellitus (T2DM) in rural populations is limited. Here, we aimed to investigate the association between fecal SCFA levels and T2DM and the combined effects of dietar quality on T2DM in rural China. In total, 100 adults were included in the case–control study. Dietary quality was assessed by the Alternate Healthy Eating Index 2010 (AHEI-2010), and SCFA levels were analysed using the GC-MS system. Generalised linear regression was conducted to calculate the OR and 95 % CI to evaluate the effect of SCFA level and dietary quality on the risk of T2DM. Finally, an interaction was used to study the combined effect of SCFA levels and AHEI-2010 scores on T2DM. T2DM participants had lower levels of acetic and butyric acid. Generalised linear regression analysis revealed that the OR (95 % CI) of the highest acetic and butyric acid levels were 0·099 (0·022, 0·441) and 0·210 (0·057, 0·774), respectively, compared with the subjects with the lowest tertile of level. We also observed a significantly lower risk of T2DM with acetic acid levels > 1330·106 μg/g or butyric acid levels > 585·031 μg/g. Moreover, the risks of higher acetic and butyric acid levels of T2DM were 0·007 (95 % CI: 0·001, 0·148), 0·005 (95 % CI: 0·001, 0·120) compared with participants with lower AHEI-2010 scores (all P < 0·05). Acetate and butyrate levels may be important modifiable beneficial factors affecting T2DM in rural China. Improving dietary quality for body metabolism balance should be encouraged to promote good health.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of the Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Sun, H, Saeedi, P, Karuranga, S, et al. (2022) IDF Diabetes Atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract 183, 109119.CrossRefGoogle ScholarPubMed
Rittiphairoj, T, Pongpirul, K, Mueller, NT, et al. (2019) Probiotics for glycemic control in patients with type 2 diabetes mellitus: protocol for a systematic review. Syst Rev 8, 227.CrossRefGoogle ScholarPubMed
Kautzky-Willer, A, Harreiter, J & Pacini, G (2016) Sex and gender differences in risk, pathophysiology and complications of type 2 diabetes mellitus. Endocr Rev 37, 278316.CrossRefGoogle ScholarPubMed
Zmora, N, Suez, J & Elinav, E (2019) You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol 16, 3556.CrossRefGoogle ScholarPubMed
He, J, Zhang, P, Shen, L, et al. (2020) Short-chain fatty acids and their association with signalling pathways in inflammation, glucose and lipid metabolism. Int J Mol Sci 21, 6356.CrossRefGoogle ScholarPubMed
Hou, D, Zhao, Q, Chen, B, et al. (2021) Dietary supplementation with mung bean coat alleviates the disorders in serum glucose and lipid profile and modulates gut microbiota in high-fat diet and streptozotocin-induced prediabetic mice. J Food Sci 86, 41834196.CrossRefGoogle ScholarPubMed
Macho-Gonzalez, A, Garcimartin, A, Redondo, N, et al. (2021) Carob fruit extract-enriched meat, as preventive and curative treatments, improves gut microbiota and colonic barrier integrity in a late-stage T2DM model. Food Res Int 141, 110124.CrossRefGoogle Scholar
Zhang, Y, Peng, Y, Zhao, L, et al. (2021) Regulating the gut microbiota and SCFAs in the faeces of T2DM rats should be one of antidiabetic mechanisms of mogrosides in the fruits of Siraitia grosvenorii. J Ethnopharmacol 274, 114033.CrossRefGoogle ScholarPubMed
Han, L, Li, T, Du, M, et al. (2019) Beneficial effects of potentilla discolor bunge water extract on inflammatory cytokines release and gut microbiota in high-fat diet and streptozotocin-induced type 2 diabetic mice. Nutrients 11, 670.CrossRefGoogle ScholarPubMed
Lee, YS, Lee, D, Park, GS, et al. (2021) Lactobacillus plantarum HAC01 ameliorates type 2 diabetes in high-fat diet and streptozotocin-induced diabetic mice in association with modulating the gut microbiota. Food Funct 12, 63636373.CrossRefGoogle ScholarPubMed
Maldonado-Contreras, A, Noel, SE, Ward, DV, et al. (2020) Associations between diet, the gut microbiome, and short-chain fatty acid production among older Caribbean Latino adults. J Acad Nutr Dietetics 120, 20472060.e2046.CrossRefGoogle Scholar
Ren, M, Zhang, H, Qi, J, et al. (2020) An almond-based low carbohydrate diet improves depression and glycometabolism in patients with type 2 diabetes through modulating gut microbiota and GLP-1: a randomized controlled trial. Nutrients 12, 3036.CrossRefGoogle ScholarPubMed
Medawar, E, Haange, SB, Rolle-Kampczyk, U, et al. (2021) Gut microbiota link dietary fiber intake and short-chain fatty acid metabolism with eating behavior. Transl Psychiatry 11, 500.CrossRefGoogle ScholarPubMed
Zhao, L, Lou, H, Peng, Y, et al. (2020) Elevated levels of circulating short-chain fatty acids and bile acids in type 2 diabetes are linked to gut barrier disruption and disordered gut microbiota. Diabetes Res Clin Pract 169, 108418.CrossRefGoogle ScholarPubMed
Wang, H, Gou, W, Su, C, et al. (2022) Association of gut microbiota with glycaemic traits and incident type 2 diabetes, and modulation by habitual diet: a population-based longitudinal cohort study in Chinese adults. Diabetologia 65, 11451156.CrossRefGoogle Scholar
Xu, Y, Wang, L, He, J, et al. (2013) Prevalence and control of diabetes in Chinese adults. JAMA 310, 948959.CrossRefGoogle ScholarPubMed
Karlsson, FH, Tremaroli, V, Nookaew, I, et al. (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498, 99103.CrossRefGoogle ScholarPubMed
Singh, RK, Chang, HW, Yan, D, et al. (2017) Influence of diet on the gut microbiome and implications for human health. J Transl Med 15, 73.CrossRefGoogle ScholarPubMed
Vangay, P, Johnson, AJ, Ward, TL, et al. (2018) US immigration westernizes the human gut microbiome. Cell 175, 962972.e910.CrossRefGoogle Scholar
Yang, JJ, Lipworth, LP, Shu, XO, et al. (2020) Associations of choline-related nutrients with cardiometabolic and all-cause mortality: results from 3 prospective cohort studies of blacks, whites, and Chinese. Am J Clin Nutr 111, 644656.CrossRefGoogle ScholarPubMed
Liu, X, Mao, Z, Li, Y, et al. (2019) Cohort profile: the Henan Rural Cohort: a prospective study of chronic non-communicable diseases. Int J Epidemiol 48, 17561756j.CrossRefGoogle ScholarPubMed
Wallace, TM, Levy, JC & Matthews, DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27, 14871495.CrossRefGoogle ScholarPubMed
Zhang, S, Wang, H & Zhu, MJ (2019) A sensitive GC/MS detection method for analyzing microbial metabolites short chain fatty acids in fecal and serum samples. Talanta 196, 249254.CrossRefGoogle ScholarPubMed
Hsu, YL, Chen, CC, Lin, YT, et al. (2019) Evaluation and optimization of sample handling methods for quantification of short-chain fatty acids in human fecal samples by GC-MS. J Proteome Res 18, 19481957.CrossRefGoogle ScholarPubMed
Xue, Y, Yang, K, Wang, B, et al. (2020) Reproducibility and validity of an FFQ in the Henan Rural Cohort Study. Public Health Nutr 23, 3440.CrossRefGoogle ScholarPubMed
Chiuve, SE, Fung, TT, Rimm, EB, et al. (2012) Alternative dietary indices both strongly predict risk of chronic disease. J Nutr 142, 10091018.CrossRefGoogle ScholarPubMed
American Diabetes Association (2013) Diagnosis and classification of diabetes mellitus. Diabetes Care 36, S6774.CrossRefGoogle Scholar
Alberti, KG & Zimmet, PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15, 539553.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Wu, H, Tremaroli, V, Schmidt, C, et al. (2020) The gut microbiota in prediabetes and diabetes: a population-based cross-sectional study. Cell Metab 32, 379390.e373.CrossRefGoogle Scholar
Zhao, L, Lou, H, Peng, Y, et al. (2019) Comprehensive relationships between gut microbiome and faecal metabolome in individuals with type 2 diabetes and its complications. Endocrine 66, 526537.CrossRefGoogle ScholarPubMed
Mueller, NT, Differding, MK, Zhang, M, et al. (2021) Metformin affects gut microbiome composition and function and circulating short-chain fatty acids: a randomized trial. Diabetes Care 44, 14621471.CrossRefGoogle ScholarPubMed
Sanna, S, van Zuydam, NR, Mahajan, A, et al. (2019) Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat Genet 51, 600605.CrossRefGoogle ScholarPubMed
Ojo, O, Feng, QQ, Ojo, OO, et al. (2020) The role of dietary fibre in modulating gut microbiota dysbiosis in patients with type 2 diabetes: a systematic review and meta-analysis of randomised controlled trials. Nutrients 12, 3239.CrossRefGoogle ScholarPubMed
Li, J, Li, Y, Ivey, KL, et al. (2022) Interplay between diet and gut microbiome, and circulating concentrations of trimethylamine N-oxide: findings from a longitudinal cohort of US men. Gut 71, 724733.CrossRefGoogle ScholarPubMed
Huang, F, Nilholm, C, Roth, B, et al. (2018) Anthropometric and metabolic improvements in human type 2 diabetes after introduction of an Okinawan-based Nordic diet are not associated with changes in microbial diversity or SCFA concentrations. Int J Food Sci Nutr 69, 729740.CrossRefGoogle ScholarPubMed
Valdes, DS, So, D, Gill, PA, et al. (2021) Effect of dietary acetic acid supplementation on plasma glucose, lipid profiles, and body mass index in human adults: a systematic review and meta-analysis. J Acad Nutr Diet 121, 895914.CrossRefGoogle ScholarPubMed
Yu, D, Zhang, X, Xiang, YB, et al. (2014) Adherence to dietary guidelines and mortality: a report from prospective cohort studies of 134 000 Chinese adults in urban Shanghai. Am J Clin Nutr 100, 693700.CrossRefGoogle ScholarPubMed
Merino, J, Guasch-Ferré, M, Li, J, et al. (2022) Polygenic scores, diet quality, and type 2 diabetes risk: an observational study among 35 759 adults from 3 US cohorts. PLoS Med 19, e1003972.CrossRefGoogle ScholarPubMed
Fung, TT, Li, Y, Bhupathiraju, SN, et al. (2021) Higher global diet quality score is inversely associated with risk of type 2 diabetes in US women. J Nutr 151, 168s175s.CrossRefGoogle ScholarPubMed
Jiang, Z, Sun, TY, He, Y, et al. (2020) Dietary fruit and vegetable intake, gut microbiota, and type 2 diabetes: results from two large human cohort studies. BMC Med 18, 371.CrossRefGoogle ScholarPubMed
Yu, D, Nguyen, SM, Yang, Y, et al. (2021) Long-term diet quality is associated with gut microbiome diversity and composition among urban Chinese adults. Am J Clin Nutr 113, 684694.CrossRefGoogle ScholarPubMed
Qian, F, Liu, G, Hu, FB, et al. (2019) Association between plant-based dietary patterns and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA Intern Med 179, 13351344.CrossRefGoogle ScholarPubMed
Schwingshackl, L, Bogensberger, B & Hoffmann, G (2018) Diet quality as assessed by the healthy eating index, alternate healthy eating index, dietary approaches to stop hypertension score, and health outcomes: an updated systematic review and meta-analysis of cohort studies. J Acad Nutr Diet 118, 74100.e111.CrossRefGoogle Scholar
Wang, G, Li, X, Zhao, J, et al. (2017) Lactobacillus casei CCFM419 attenuates type 2 diabetes via a gut microbiota dependent mechanism. Food Funct 8, 31553164.CrossRefGoogle Scholar
Zhang, C, Ma, S, Wu, J, et al. (2020) A specific gut microbiota and metabolomic profiles shifts related to antidiabetic action: the similar and complementary antidiabetic properties of type 3 resistant starch from Canna edulis and metformin. Pharmacol Res 159, 104985.CrossRefGoogle ScholarPubMed
Li, X, Sui, Y, Xie, B, et al. (2021) Diabetes diminishes a typical metabolite of litchi pericarp oligomeric procyanidins (LPOPC) in urine mediated by imbalanced gut microbiota. Food Funct 12, 53755386.CrossRefGoogle ScholarPubMed
Canfora, EE, Hermes, GDA, Müller, M, et al. (2022) Fiber mixture-specific effect on distal colonic fermentation and metabolic health in lean but not in prediabetic men. Gut Microbes 14, 2009297.CrossRefGoogle ScholarPubMed
Cronin, P, Joyce, SA, O’Toole, PW, et al. (2021) Dietary fibre modulates the gut microbiota. Nutrients 13, 1655.CrossRefGoogle ScholarPubMed
Canfora, EE, Jocken, JW & Blaak, EE (2015) Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol 11, 577591.CrossRefGoogle ScholarPubMed
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material
Download Li et al. supplementary material(File)
File 30 KB