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Published in: Diabetology & Metabolic Syndrome 1/2019

Open Access 01-12-2019 | Insulins | Research

Differential role of insulin resistance and β-cell function in the development of prediabetes and diabetes in middle-aged and elderly Chinese population

Authors: Xueli Cai, Lili Xia, Yuesong Pan, Dian He, Huiping Zhu, Tiemin Wei, Yan He

Published in: Diabetology & Metabolic Syndrome | Issue 1/2019

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Abstract

Background

The prevalence of diabetes and prediabetes were estimated to be 10.9% and 35.7% in the Chinese adult population, respectively, and the middle-aged and elderly Chinese are at even higher risk of diabetes and prediabetes than younger population. With the increasing trend of aging in China, the burden of diabetes and related complications will be aggravated.

Objectives

Through comparing the indices of insulin resistance and β-cell function between subjects with different glucose metabolic status, to analyze the differential role of insulin resistance and β-cell function in the development of prediabetes and type 2 diabetes (T2DM) in the middle-aged and elderly Chinese population.

Methods

In this cross-sectional study, we enrolled 512 participants aged 50 and over. The indices of insulin resistance (homoeostasis model assessment of insulin resistance (HOMA-IR) and adipose tissue insulin resistance (Adipo-IR), and indices of β-cell function [HOMA-β), fasting C-peptide to glucose ratio (FCPRI) and postprandial C-peptide to glucose ratio (PCPRI)] were calculated. Association of insulin resistance and β-cell function with prediabetes or T2DM were evaluated by multivariate logistic regression analysis, in which potential confounding factors were adjusted.

Results

Of the 509 participants with complete information, 263 (51.7%) had normal glucose tolerance (NGT), 161 (31.6%) were in prediabetic status and 85 (16.7%) were overt T2DM. With the advancing of unfavorable glucose metabolism, the insulin resistance (HOMA-IR and Adipo-IR) and β-cell function (FCPRI, PCPRI) deteriorated (Ptrend < 0.05 for all indices). We found that increase in insulin resistance expressed by Adipo-IR and HOMA-IR is associated with increased risk of prediabetes, whereas decrease in β-cell function expressed by HOMA-β and PCPRI is associated with increased risk of T2DM. We also demonstrated that Adipo-IR was more closely associated with developing prediabetes than HOMA-IR, and PCPRI was most closely related with developing T2DM among the indices of β-cell function used in this study.

Conclusions

Insulin resistance is the main determinant of developing prediabetes, whereas β-cell function is the main determinant of developing T2DM.
Literature
1.
go back to reference Wang L, Gao P, Zhang M, et al. Prevalence and ethnic pattern of diabetes and prediabetes in China in 2013. JAMA. 2017;317:2515–23.CrossRef Wang L, Gao P, Zhang M, et al. Prevalence and ethnic pattern of diabetes and prediabetes in China in 2013. JAMA. 2017;317:2515–23.CrossRef
2.
go back to reference Zhao Y, Crimmins EM, Hu P, et al. Prevalence, diagnosis, and management of diabetes mellitus among older Chinese: results from the China health and retirement longitudinal study. Int J Public Health. 2016;61:347–56.CrossRef Zhao Y, Crimmins EM, Hu P, et al. Prevalence, diagnosis, and management of diabetes mellitus among older Chinese: results from the China health and retirement longitudinal study. Int J Public Health. 2016;61:347–56.CrossRef
3.
go back to reference Bragg F, Holmes MV, Iona A, et al. Association between diabetes and cause-specific mortality in rural and urban areas of China. JAMA. 2017;317:280–9.CrossRef Bragg F, Holmes MV, Iona A, et al. Association between diabetes and cause-specific mortality in rural and urban areas of China. JAMA. 2017;317:280–9.CrossRef
5.
go back to reference Kanaya AM, Herrington D, Vittinghoff E, et al. Understanding the high prevalence of diabetes in US south Asians compared with four racial/ethnic groups: the MASALA and MESA studies. Diabetes Care. 2014;37:1621–8.CrossRef Kanaya AM, Herrington D, Vittinghoff E, et al. Understanding the high prevalence of diabetes in US south Asians compared with four racial/ethnic groups: the MASALA and MESA studies. Diabetes Care. 2014;37:1621–8.CrossRef
6.
go back to reference Hulman A, Simmons RK, Brunner EJ, et al. Trajectories of glycaemia, insulin sensitivity and insulin secretion in South Asian and white individuals before diagnosis of type 2 diabetes: a longitudinal analysis from the Whitehall II cohort study. Diabetologia. 2017;60:1252–60.CrossRef Hulman A, Simmons RK, Brunner EJ, et al. Trajectories of glycaemia, insulin sensitivity and insulin secretion in South Asian and white individuals before diagnosis of type 2 diabetes: a longitudinal analysis from the Whitehall II cohort study. Diabetologia. 2017;60:1252–60.CrossRef
7.
go back to reference Gastaldelli A, Gaggini M, DeFronzo RA. Role of adipose tissue insulin resistance in the natural history of type 2 diabetes: results from the San Antonio metabolism study. Diabetes. 2017;66:815–22.CrossRef Gastaldelli A, Gaggini M, DeFronzo RA. Role of adipose tissue insulin resistance in the natural history of type 2 diabetes: results from the San Antonio metabolism study. Diabetes. 2017;66:815–22.CrossRef
8.
go back to reference Yue Y, He H, Yang XJ, et al. Pancreatic beta-cell functions measured by continuous glucose monitoring in Han Chinese with varied degree of glucose tolerance. Sichuan da xue xue bao Yi xue ban = J Sichuan Univ Med Sci Ed. 2016;47:790–5. Yue Y, He H, Yang XJ, et al. Pancreatic beta-cell functions measured by continuous glucose monitoring in Han Chinese with varied degree of glucose tolerance. Sichuan da xue xue bao Yi xue ban = J Sichuan Univ Med Sci Ed. 2016;47:790–5.
9.
go back to reference Rhee SY, Kim JY, Chon S, et al. The changes in early phase insulin secretion in newly diagnosed, drug naive korean prediabetes subjects. Korean Diabetes J. 2010;34:157–65.CrossRef Rhee SY, Kim JY, Chon S, et al. The changes in early phase insulin secretion in newly diagnosed, drug naive korean prediabetes subjects. Korean Diabetes J. 2010;34:157–65.CrossRef
10.
go back to reference Onishi Y, Hayashi T, Sato KK, et al. Fasting tests of insulin secretion and sensitivity predict future prediabetes in Japanese with normal glucose tolerance. J Diabetes Investig. 2010;1:191–5.CrossRef Onishi Y, Hayashi T, Sato KK, et al. Fasting tests of insulin secretion and sensitivity predict future prediabetes in Japanese with normal glucose tolerance. J Diabetes Investig. 2010;1:191–5.CrossRef
11.
go back to reference Festa A, Williams K, D’Agostino R Jr, et al. The natural course of beta-cell function in nondiabetic and diabetic individuals: the insulin resistance atherosclerosis study. Diabetes. 2006;55:1114–20.CrossRef Festa A, Williams K, D’Agostino R Jr, et al. The natural course of beta-cell function in nondiabetic and diabetic individuals: the insulin resistance atherosclerosis study. Diabetes. 2006;55:1114–20.CrossRef
12.
go back to reference Tabak AG, Jokela M, Akbaraly TN, et al. Trajectories of glycaemia, insulin sensitivity, and insulin secretion before diagnosis of type 2 diabetes: an analysis from the Whitehall II study. Lancet (London, England). 2009;373:2215–21.CrossRef Tabak AG, Jokela M, Akbaraly TN, et al. Trajectories of glycaemia, insulin sensitivity, and insulin secretion before diagnosis of type 2 diabetes: an analysis from the Whitehall II study. Lancet (London, England). 2009;373:2215–21.CrossRef
13.
go back to reference Liu J, Wu YY, Huang XM, et al. Ageing and type 2 diabetes in an elderly Chinese population: the role of insulin resistance and beta cell dysfunction. Eur Rev Med Pharmacol Sci. 2014;18:1790–7.PubMed Liu J, Wu YY, Huang XM, et al. Ageing and type 2 diabetes in an elderly Chinese population: the role of insulin resistance and beta cell dysfunction. Eur Rev Med Pharmacol Sci. 2014;18:1790–7.PubMed
14.
go back to reference Cnop M, Vidal J, Hull RL, et al. Progressive loss of beta-cell function leads to worsening glucose tolerance in first-degree relatives of subjects with type 2 diabetes. Diabetes Care. 2007;30:677–82.CrossRef Cnop M, Vidal J, Hull RL, et al. Progressive loss of beta-cell function leads to worsening glucose tolerance in first-degree relatives of subjects with type 2 diabetes. Diabetes Care. 2007;30:677–82.CrossRef
15.
go back to reference Qian L, Xu L, Wang X, et al. Early insulin secretion failure leads to diabetes in Chinese subjects with impaired glucose regulation. Diabetes/Metab Res Rev. 2009;25:144–9.CrossRef Qian L, Xu L, Wang X, et al. Early insulin secretion failure leads to diabetes in Chinese subjects with impaired glucose regulation. Diabetes/Metab Res Rev. 2009;25:144–9.CrossRef
16.
go back to reference Morimoto A, Tatsumi Y, Deura K, et al. Impact of impaired insulin secretion and insulin resistance on the incidence of type 2 diabetes mellitus in a Japanese population: the Saku study. Diabetologia. 2013;56:1671–9.CrossRef Morimoto A, Tatsumi Y, Deura K, et al. Impact of impaired insulin secretion and insulin resistance on the incidence of type 2 diabetes mellitus in a Japanese population: the Saku study. Diabetologia. 2013;56:1671–9.CrossRef
17.
go back to reference Alberti KG, Zimmet PZ. 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. 1998;15:539–53.CrossRef Alberti KG, Zimmet PZ. 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. 1998;15:539–53.CrossRef
18.
go back to reference Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22:1462–70.CrossRef Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22:1462–70.CrossRef
19.
go back to reference Abu-Farha M, Behbehani K, Elkum N. Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs. Cardiovasc Diabetol. 2014;13:76.CrossRef Abu-Farha M, Behbehani K, Elkum N. Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs. Cardiovasc Diabetol. 2014;13:76.CrossRef
20.
go back to reference Barchetta I, Angelico F, Del Ben M, et al. Phenotypical heterogeneity linked to adipose tissue dysfunction in patients with type 2 diabetes. Clin Sci. 2016;130:1753–62.CrossRef Barchetta I, Angelico F, Del Ben M, et al. Phenotypical heterogeneity linked to adipose tissue dysfunction in patients with type 2 diabetes. Clin Sci. 2016;130:1753–62.CrossRef
21.
go back to reference Hershkop K, Besor O, Santoro N, et al. Adipose insulin resistance in obese adolescents across the spectrum of glucose tolerance. J Clin Endocrinol Metab. 2016;101:2423–31.CrossRef Hershkop K, Besor O, Santoro N, et al. Adipose insulin resistance in obese adolescents across the spectrum of glucose tolerance. J Clin Endocrinol Metab. 2016;101:2423–31.CrossRef
22.
go back to reference Saponaro C, Gaggini M, Carli F, et al. The subtle balance between lipolysis and lipogenesis: a critical point in metabolic homeostasis. Nutrients. 2015;7:9453–74.CrossRef Saponaro C, Gaggini M, Carli F, et al. The subtle balance between lipolysis and lipogenesis: a critical point in metabolic homeostasis. Nutrients. 2015;7:9453–74.CrossRef
23.
go back to reference Ferrannini E, Barrett EJ, Bevilacqua S, et al. Effect of fatty acids on glucose production and utilization in man. J Clin Investig. 1983;72:1737–47.CrossRef Ferrannini E, Barrett EJ, Bevilacqua S, et al. Effect of fatty acids on glucose production and utilization in man. J Clin Investig. 1983;72:1737–47.CrossRef
24.
go back to reference Mundi MS, Koutsari C, Jensen MD. Effects of increased free fatty acid availability on adipose tissue fatty acid storage in men. J Clin Endocrinol Metab. 2014;99:E2635–42.CrossRef Mundi MS, Koutsari C, Jensen MD. Effects of increased free fatty acid availability on adipose tissue fatty acid storage in men. J Clin Endocrinol Metab. 2014;99:E2635–42.CrossRef
25.
go back to reference Gyllenhammer LE, Alderete TL, Toledo-Corral CM, et al. Saturation of subcutaneous adipose tissue expansion and accumulation of ectopic fat associated with metabolic dysfunction during late and post-pubertal growth. Int J Obes. 2005;2016(40):601–6. Gyllenhammer LE, Alderete TL, Toledo-Corral CM, et al. Saturation of subcutaneous adipose tissue expansion and accumulation of ectopic fat associated with metabolic dysfunction during late and post-pubertal growth. Int J Obes. 2005;2016(40):601–6.
26.
go back to reference Morelli M, Gaggini M, Daniele G, et al. Ectopic fat: the true culprit linking obesity and cardiovascular disease? Thromb Haemost. 2013;110:651–60.CrossRef Morelli M, Gaggini M, Daniele G, et al. Ectopic fat: the true culprit linking obesity and cardiovascular disease? Thromb Haemost. 2013;110:651–60.CrossRef
27.
go back to reference Ter Horst KW, van Galen KA, Gilijamse PW, et al. Methods for quantifying adipose tissue insulin resistance in overweight/obese humans. Int J Obes. 2005;2017(41):1288–94. Ter Horst KW, van Galen KA, Gilijamse PW, et al. Methods for quantifying adipose tissue insulin resistance in overweight/obese humans. Int J Obes. 2005;2017(41):1288–94.
28.
go back to reference Sondergaard E, Espinosa De Ycaza AE, Morgan-Bathke M, et al. How to measure adipose tissue insulin sensitivity. J Clin Endocrinol Metab. 2017;102:1193–9.CrossRef Sondergaard E, Espinosa De Ycaza AE, Morgan-Bathke M, et al. How to measure adipose tissue insulin sensitivity. J Clin Endocrinol Metab. 2017;102:1193–9.CrossRef
29.
go back to reference Butler AE, Janson J, Bonner-Weir S, et al. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52:102–10.CrossRef Butler AE, Janson J, Bonner-Weir S, et al. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52:102–10.CrossRef
30.
go back to reference Saisho Y. Beta-cell dysfunction: its critical role in prevention and management of type 2 diabetes. World J Diabetes. 2015;6:109–24.CrossRef Saisho Y. Beta-cell dysfunction: its critical role in prevention and management of type 2 diabetes. World J Diabetes. 2015;6:109–24.CrossRef
31.
go back to reference Okuno Y, Komada H, Sakaguchi K, et al. Postprandial serum C-peptide to plasma glucose concentration ratio correlates with oral glucose tolerance test- and glucose clamp-based disposition indexes. Metab Clin Exp. 2013;62:1470–6.CrossRef Okuno Y, Komada H, Sakaguchi K, et al. Postprandial serum C-peptide to plasma glucose concentration ratio correlates with oral glucose tolerance test- and glucose clamp-based disposition indexes. Metab Clin Exp. 2013;62:1470–6.CrossRef
32.
go back to reference Meier JJ, Menge BA, Breuer TG, et al. Functional assessment of pancreatic beta-cell area in humans. Diabetes. 2009;58:1595–603.CrossRef Meier JJ, Menge BA, Breuer TG, et al. Functional assessment of pancreatic beta-cell area in humans. Diabetes. 2009;58:1595–603.CrossRef
33.
go back to reference Peacock I, Tattersall RB. The difficult choice of treatment for poorly controlled maturity onset diabetes: tablets or insulin? Br Med J. 1984;288:1956–9.CrossRef Peacock I, Tattersall RB. The difficult choice of treatment for poorly controlled maturity onset diabetes: tablets or insulin? Br Med J. 1984;288:1956–9.CrossRef
34.
go back to reference Funakoshi S, Fujimoto S, Hamasaki A, et al. Utility of indices using C-peptide levels for indication of insulin therapy to achieve good glycemic control in Japanese patients with type 2 diabetes. J Diabetes Investig. 2011;2:297–303.CrossRef Funakoshi S, Fujimoto S, Hamasaki A, et al. Utility of indices using C-peptide levels for indication of insulin therapy to achieve good glycemic control in Japanese patients with type 2 diabetes. J Diabetes Investig. 2011;2:297–303.CrossRef
35.
go back to reference Saisho Y, Kou K, Tanaka K, et al. Postprandial serum C-peptide to plasma glucose ratio as a predictor of subsequent insulin treatment in patients with type 2 diabetes. Endocr J. 2011;58:315–22.CrossRef Saisho Y, Kou K, Tanaka K, et al. Postprandial serum C-peptide to plasma glucose ratio as a predictor of subsequent insulin treatment in patients with type 2 diabetes. Endocr J. 2011;58:315–22.CrossRef
36.
go back to reference Goto A, Takaichi M, Kishimoto M, et al. Body mass index, fasting plasma glucose levels, and C-peptide levels as predictors of the future insulin use in Japanese type 2 diabetic patients. Endocr J. 2010;57:237–44.CrossRef Goto A, Takaichi M, Kishimoto M, et al. Body mass index, fasting plasma glucose levels, and C-peptide levels as predictors of the future insulin use in Japanese type 2 diabetic patients. Endocr J. 2010;57:237–44.CrossRef
37.
go back to reference Fujiwara D, Takahashi K, Suzuki T, et al. Postprandial serum C-peptide value is the optimal index to identify patients with non-obese type 2 diabetes who require multiple daily insulin injection: analysis of C-peptide values before and after short-term intensive insulin therapy. J Diabetes Investig. 2013;4:618–25.CrossRef Fujiwara D, Takahashi K, Suzuki T, et al. Postprandial serum C-peptide value is the optimal index to identify patients with non-obese type 2 diabetes who require multiple daily insulin injection: analysis of C-peptide values before and after short-term intensive insulin therapy. J Diabetes Investig. 2013;4:618–25.CrossRef
38.
go back to reference Lee EY, Hwang S, Lee SH, et al. Postprandial C-peptide to glucose ratio as a predictor of beta-cell function and its usefulness for staged management of type 2 diabetes. J Diabetes Investig. 2014;5:517–24.CrossRef Lee EY, Hwang S, Lee SH, et al. Postprandial C-peptide to glucose ratio as a predictor of beta-cell function and its usefulness for staged management of type 2 diabetes. J Diabetes Investig. 2014;5:517–24.CrossRef
Metadata
Title
Differential role of insulin resistance and β-cell function in the development of prediabetes and diabetes in middle-aged and elderly Chinese population
Authors
Xueli Cai
Lili Xia
Yuesong Pan
Dian He
Huiping Zhu
Tiemin Wei
Yan He
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2019
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/s13098-019-0418-x

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