Sex-specific clinical outcomes of impaired glucose status: A long follow-up from the Tehran Lipid and Glucose Study

Abstract

Aims

To investigate the sex-specific associations of prediabetes with major clinical outcomes including incident type 2 diabetes, chronic kidney disease, hypertension, coronary heart disease, stroke and all-cause mortality.

Methods

Among 8498 Iranian adults from the Tehran Lipid and Glucose Study, aged ≥30 years and without diagnosed type 2 diabetes, gender-interactions were assessed for each outcome, followed by sex-separated multivariate-adjusted Cox proportional hazard models to calculate hazard ratios and 95% confidence intervals (CIs) of different prediabetes categories, including impaired fasting glucose (IFG), defined by the American Diabetes Association (ADA) and World Health Organization (WHO), as fasting plasma glucose of 5.6–6.9 mmol/L and 6.1–6.9 mmol/L, respectively, and impaired glucose tolerance, defined as 2-h post challenge plasma glucose of 7.8–11 mmol/L.

Results

Sex-specific associations existed for men between IFG-ADA and chronic kidney disease (hazard ratio: 1.28, 95% CI 0.99–1.65; p_interaction = 0.008) and between IFG-WHO and stroke (hazard ratio: 2.15, 95% CI 1.08–4.27; p_interaction = 0.21); and for women between IFG-ADA and hypertension (hazard ratio: 1.24, 95% CI 1.04–1.48; p_interaction = 0.06) and between impaired glucose tolerance and coronary heart disease (hazard ratio: 1.57, 95% CI 1.14–2.16; p_interaction = 0.05). Among both genders, all prediabetes definitions were associated with type 2 diabetes but none with mortality.

Conclusions

The hazards of prediabetes definitions may differ between genders depending on the outcome of interest. IFG-WHO among men and impaired glucose tolerance among women are particularly important because of their association with incident stroke and coronary heart disease, respectively. Considering these sex differences could improve personalized management of prediabetes.

Keywords

Prediabetic state impaired fasting glucose impaired glucose tolerance hypertension renal insufficiency cardiovascular disease

Get full access to this article

View all access options for this article.

References

World Health Organization. WHO Guidelines approved by the Guidelines Review Committee. Use of glycated haemoglobin (HbA1c) in the diagnosis of diabetes mellitus: Abbreviated report of a WHO consultation. Geneva: World Health Organization, 2011.

The American Diabetes Association. Standards of medical care in diabetes—2018 abridged for primary care providers. Clin Diabetes 2017; 41: 160.

Hadaegh

Derakhshan

Zafari

et al.

Pre-diabetes tsunami: Incidence rates and risk factors of pre-diabetes and its different phenotypes over 9 years of follow-up. Diabet Med 2017; 34: 69–78.

Echouffo-Tcheugui

Narayan

Weisman

et al.

Association between prediabetes and risk of chronic kidney disease: A systematic review and meta-analysis. Diabet Med 2016; 33: 1615–1624.

Levin

Kestenbaum

Ida Chen

Y-D

et al.

Glucose, insulin, and incident hypertension in the multi-ethnic study of atherosclerosis. Am J Epidemiol 2010; 172: 1144–1154.

Lee

Lim

N-K

Kim

H-C

et al.

Impaired fasting glucose and impaired glucose tolerance do not predict hypertension: A community cohort study. Am J Hypertens 2015; 28: 493–500.

Huang

Cai

Mai

et al.

Association between prediabetes and risk of cardiovascular disease and all cause mortality: Systematic review and meta-analysis. BMJ 2016; 355: i5953.

Faerch

Vistisen

Johansen

et al.

Cardiovascular risk stratification and management in pre-diabetes. Curr Diab Rep 2014; 14: 493.

Rannelli

MacRae

Mann

et al.

Sex differences in associations between insulin resistance, heart rate variability, and arterial stiffness in healthy women and men: A physiology study. Can J Physiol Pharmacol 2017; 95: 349–355.

10.

Arshi

Tohidi

Derakhshan

et al.

Sex-specific relations between fasting insulin, insulin resistance and incident hypertension: 8.9 years follow-up in a Middle-Eastern population. J Hum Hypertens 2015; 29: 260–267.

11.

Kautzky-Willer

Harreiter

Pacini

. Sex and gender differences in risk, pathophysiology and complications of type 2 diabetes mellitus. Endocr Rev 2016; 37: 278–316.

12.

Warren

Pankow

Matsushita

et al.

Comparative prognostic performance of definitions of prediabetes: A prospective cohort analysis of the Atherosclerosis Risk in Communities (ARIC) study. Lancet Diabetes Endocrinol 2017; 5: 34–42.

13.

Tohidi

Hasheminia

Mohebi

et al.

Incidence of chronic kidney disease and its risk factors, results of over 10 year follow up in an Iranian cohort. PLoS One 2012; 7: e45304.

14.

Turk-Adawi

Sarrafzadegan

Fadhil

et al.

Cardiovascular disease in the Eastern Mediterranean region: Epidemiology and risk factor burden. Nat Rev Cardiol 2017; 15: 106–119.

15.

Wang

Han

. Fasting insulin, insulin resistance and risk of hypertension in the general population: A meta-analysis. Clin Chim Acta 2017; 464: 57–63.

16.

Azizi

Ghanbarian

Momenan

et al.

Prevention of non-communicable disease in a population in nutrition transition: Tehran Lipid and Glucose Study phase II. Trials 2009; 10: 5–19.

17.

Levey

Stevens

Schmid

et al.

A new equation to estimate glomerular filtration rate. Ann Intern Med 2009; 150: 604–612.

18.

Althouse

. Adjust for multiple comparisons? It's not that simple. Ann Thorac Surg 2016; 101: 1644–1645.

19.

Bender

Lange

. Adjusting for multiple testing – when and how?. J Clin Epidemiol 2001; 54: 343–349.

20.

Rothman

. No adjustments are needed for multiple comparisons. Epidemiology 1990; 1: 43–46.

21.

Morris

Khunti

Achana

et al.

Progression rates from HbA1c 6.0–6.4% and other prediabetes definitions to type 2 diabetes: A meta-analysis. Diabetologia 2013; 56: 1489–1493.

22.

Song

Qiu

Zhang

et al.

Gender-related affecting factors of prediabetes on its 10-year outcome. BMJ Open Diabetes Res Care 2016, pp. 4.

23.

Neugarten

Acharya

Silbiger

. Effect of gender on the progression of nondiabetic renal disease: A meta-analysis. J Am Soc Nephrol 2000; 11: 319–329.

24.

Shen

Cai

Sun

et al.

Diabetes mellitus as a risk factor for incident chronic kidney disease and end-stage renal disease in women compared with men: A systematic review and meta-analysis. Endocrine 2017; 55: 66–76.

25.

Maric

Sullivan

. Estrogens and the diabetic kidney. Gend Med 2008; 5: S103–S113.

26.

Jadhakhan

Marshall

Gill

. A systematic review of the effects of impaired glucose tolerance (IGT) on the incidence of chronic kidney disease (CKD) in young adults. Br J Diabetes 2016; 16: 162–167.

27.

Tapp

Shaw

Zimmet

et al.

Albuminuria is evident in the early stages of diabetes onset: Results from the Australian Diabetes, Obesity, and Lifestyle Study (AusDiab). Am J Kidney Dis 2004; 44: 792–798.

28.

Nelson

Tan

Beck

et al.

Changing glomerular filtration with progression from impaired glucose tolerance to Type II diabetes mellitus (Short Communications). Diabetologia 1999; 42: 90–93.

29.

Suematsu C, Hayashi T, Fujii S, et al. Impaired fasting glucose and the risk of hypertension in Japanese men between the 1980s and the 1990s. The Osaka Health Survey. Diabetes Care 1999; 22: 228–232.

30.

Giltay

Lambert

Gooren

LJG

et al.

Sex steroids, insulin, and arterial stiffness in women and men. Hypertension 1999; 34: 590.

31.

Sung

Song

Y-M

Ebrahim

et al.

Fasting blood glucose and the risk of stroke and myocardial infarction. Circulation 2009; 119: 812.

32.

DECODE Study Group, the European Diabetes Epidemiology Group. Glucose tolerance and cardiovascular mortality: Comparison of fasting and 2-hour diagnostic criteria. Arch Intern Med 2001; 161: 397–405.

33.

Tai

Goh

Lee

JJM

et al.

Lowering the criterion for impaired fasting glucose. Diabetes Care 2004; 27: 1728.

34.

Rutter

Parise

Benjamin

et al.

Impact of glucose intolerance and insulin resistance on cardiac structure and function. Circulation 2003; 107: 448.

35.

Peters

Huxley

Woodward

. Diabetes as risk factor for incident coronary heart disease in women compared with men: A systematic review and meta-analysis of 64 cohorts including 858,507 individuals and 28,203 coronary events. Diabetologia 2014; 57: 1542–1551.

36.

Sui

Lavie

Hooker

et al.

A prospective study of fasting plasma glucose and risk of stroke in asymptomatic men. Mayo Clin Proc 2011; 86: 1042–1049.

37.

Kim

H-K

Kim

C-H

Kim

et al.

Impaired fasting glucose and risk of cardiovascular disease in Korean men and women. Diabetes Care 2013; 36: 328.

38.

Iso

Imano

Kitamura

et al.

Type 2 diabetes and risk of non-embolic ischaemic stroke in Japanese men and women. Diabetologia 2004; 47: 2137–2144.

39.

Doi

Ninomiya

Hata

et al.

Impact of glucose tolerance status on development of ischemic stroke and coronary heart disease in a general Japanese population: The Hisayama study. Stroke 2010; 41: 203–209.

40.

Hirata

Okamura

Sugiyama

et al.

Impacts of chronic kidney disease and diabetes on cardiovascular mortality in a general Japanese population: A 20-year follow-up of the NIPPON DATA90 study. Eur J Prev Cardiol 2017; 24: 505–513.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.61 MB