Predictive value of simplified insulin resistance assessment indicators for metabolic syndrome in middle-aged and elderly Chinese without established diabetes

doi:10.21203/rs.3.rs-5195777/v1

Objective To investigate the predictive value of simplified insulin resistance (IR) assessment indicators for metabolic syndrome (MetS) in middle-aged and elderly Chinese individuals without established diabetes.

Methods A total of 16,621 subjects from Shijingshan District, Beijing, China, were recruited for the study from November 2011 to August 2012. Data on demographic information, lifestyle, history of diabetes mellitus, hypertension, dyslipidemia, anthropometric indices, and biomarkers were recorded. MetS was diagnosed based on the diagnostic standards of the Chinese Diabetes Society (CDS) MetS (2020 edition). The receiver operating characteristic (ROC) curve was used to analyze the predictive power of different simplified IR assessment indicators, including the triglyceride-glucose index (TyG), plasma TG-to-HDL concentration ratio (TG/HDL-C), TyG-body mass index (TyG-BMI), TyG-waist circumference (TyG-WC), and TyG-waist-to-height ratio (TyG-WHtR) for MetS, and the area under the curve (AUC) was calculated.

Results Among men, the area under the curve of the simplified IR surrogate index for MS was as follows: TyG-WC > TyG-WHtR > TyG-BMI > TyG = TG/HDL-C. Among women, the ranking was TyG-WC > TyG-WHtR > TyG-BMI > TyG > TG/HDL-C ratio. The AUC for TyG-WC were 0.900 and 0.905 for men and women, respectively. The optimal TyG-WC was 779.8 in men and 746.3 in women.

Conclusions TyG, TG/HDL-C ratio, TyG-BMI, TyG-WC, and TyG-WHtR can be used to predict MetS risk. Among them, TyG-WC was a more powerful predictor of MetS than the other four indexes.

Health sciences/Endocrinology

Health sciences/Medical research

insulin resistance

metabolic syndrome

triglyceride- glucose index

TG/HDL-C

TyG-body mass index

TyG-waist circumference index

TyG-waist-to-height ratio index

Metabolic syndrome (MetS) is a cluster of metabolic disorders characterized by insulin resistance (IR), abdominal obesity, impaired glucose and lipid metabolism, and elevated blood pressure. It is closely correlated with a higher risk of type 2 diabetes mellitus (T2DM) and atherosclerotic cardiovascular disease (ASCVD) ^1-3.The prevalence of MetS is increasing worldwide, along with the increasing incidence of overweight and obesity⁴. Excess energy intake and sedentary lifestyle are major contributors to the development of MetS, leading to the accumulation of visceral adiposity, which activates most MetS pathways. IR, chronic inflammation, and neurohormonal activation appear to play important roles in the progression of MetS and its subsequent transition to ASCVD and T2DM^5,6.

IR refers to a pathological status in which the sensitivity of peripheral tissues to insulin is reduced, the ability to utilize glucose is weakened, and the lipogenesis of triglyceride (TG) lipoproteins is enhanced^7,8. IR underpins many metabolic disorders such as T2DM, MetS, and ASCVD, which are recognized as major risk factors. Therefore, the early detection of IR is vital to prevent these conditions. It is well known The hyperinsulinemic-euglycemic clamp (HEC) is regarded as the gold standard method for IR assessment; however, its complexity, invasiveness, and high cost impede its routine use in practise⁹. Thus, it is necessary to use simple alternatives to assess IR to predict MetS risk. In clinical settings, homeostasis model assessment of IR (HOMA-IR) is considered a surrogate for HEC to evaluate the degree of IR¹⁰. However, challenges of insulin measurement availability and standardization have limited the widespread application of HOMA-IR. Recently, simplified IR biomarkers and anthropometric parameters have been widely adopted, such as the triglyceride-glucose index (TyG), plasma TG-to-HDL concentration ratio (TG/HDL-C), body mass index (BMI), waist circumference (WC), and waist-height ratio (WHtR). Previous studies have shown that TyG has a good correlation with HEC and HOMA-IR and can be used to estimate IR^11,12. Therefore, we explored the relationship between TyG, TG/HDL, and TyG-related parameters, such as TyG-BMI, TyG-WC, TyG-WHtR, and MetS, in a middle-aged and elderly Chinese population, in which previously diagnosed diabetic subjects were excluded.

Study population

This study used a cross-sectional cluster sampling survey based on community population. From November 2011 to August 2012, we conducted this survey in three communities in the Shijingshan District, Beijing, China. A total of 19,274 subjects participated in the survey and all subjects involving in the study signed informed consent before data collection. A total of 2,653 individuals with incomplete demographic information, no availability of fasting blood glucose or 2-hour blood glucose data, or previously diagnosed diabetes were excluded. Ultimately, 16,621 individuals (men 5,665; women 10,956) were recruited for the study. The enrolled subjects were aged 40–91 years, with an average age of 58 years. This study was approved by the Chinese PLA General Hospital Ethics Committee (NO.EC2012-046). The enrollment process was described in detail in a previously published study¹³.

Clinical Data and Biochemical Indicators

Trained physicians administered a standard questionnaire to collect baseline data including demographics, lifestyle, previous history of cardiovascular disease (CVD), stroke, hypertension, diabetes, and dyslipidemia. All participants underwent physical examination by trained physicians according to established standard methods, including height, weight, waist circumference (WC), hip circumference (HC), blood pressure (BP), and heart rate. Body mass index (BMI; kg/m²) was calculated as weight/height². The waist-to-hip ratio (WHR) was calculated as the WC/HC. The waist-to-height ratio (WHtR) was calculated as the WC/height. A 75 g oral glucose tolerance test was performed according to a routine method. Blood glucose was measured using the hexokinase method on a fully automatic biochemical analyzer (Modular P800; Roche, Basel, Switzerland). Fasting triglyceride (TG), total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), and low-density lipoprotein cholesterol (LDL-C) levels were measured by chemiluminescence using an automatic analyzer (Modular E170; Roche). Glycated hemoglobin (HbA1c) levels were measured using high-pressure liquid chromatography.

Definition

The diagnostic criteria for MetS were as follows: diagnosis can be made if three or more of the following items are met¹⁴.

(1). Central obesity: WC ≥ 90cm in men, ≥85cm in women;

(2). Hyperglycemia: fasting plasma glucose (FPG) ≥ 6.1 mmol/L or 2h-plasma glucose (PG2h) ≥ 7.8 mmol/L;

(3). Hypertension was defined as average systolic blood pressure (SBP) ≥ 130 mmHg, average diastolic blood pressure (DBP) ≥ 85 mmHg, or use of antihypertensive medication.

(4). Elevated TG: fasting TG level ≥ 1.7mmo1/L;

(5). Reduced HDL-C level, fasting HDL-C level <1.04 mmol/L.

Simplified IR indices and the calculation formulas were listed below.

(1). TyG = Ln（TG (mg/dL)×FPG (mg/dL)/2）；

(2). TG (mg/dL)/HDL-C (mg/dL)；

(3). TyG‑BMI=TyG×BMI;

(4). TyG‑WC=TyG×WC；

(5). TyG‑WHtR=TyG×WHtR

4. SPSS (version 25.0; SPSS Inc., USA) was used for statistical analysis. Normally distributed measurement data are expressed as mean ± standard deviation (SD), skewed distribution measurement data are expressed as median (interquartile range), and count data or prevalence are expressed as percentages. Continuous variables were compared between the two groups using t-test, and the rates between the two groups were compared using chi-square test. The receiver operating characteristic (ROC) curve was used to analyze the diagnostic efficacy of the five simplified IR indices for MetS, and the areas under the ROC curve (AUCs) were calculated. The 2-tailed test was used, and statistical significance was set at P < 0.05.

Baseline characteristics of the sample population

In this study, the overall prevalence of MetS was 29.4%. The prevalence of MetS was 36.4% and 25.8% in the men and women, respectively. Baseline patient characteristics are shown in Table 1. Among participants with MetS, age, WC, HC, BMI, WHR, WHtR, SBP, DBP, TC, TG, LDL-C, FPG, PG2h, TyG, TG/HDL-C, TyG-BMI, TyG-WC, and TyG-WHtR were significantly higher than those without MetS. Serum HDL-C levels were lower in the MetS group than in the non-MetS group (P< 0.001).

Table 1 The baseline characteristics of the population

Variables	MetS group	Non-MetS group	p-value
Men/women	2063/2824	3602/8132	<0.001
age (years)	59.3±8.3	56.8±7.9	<0.001
WC（cm）	90.4±7.6	80.8±8.0	<0.001
HC（cm）	98.1±6.9	93.0±6.4	<0.001
BMI（Kg/m²）	27.9±3.2	24.8±3.2	<0.001
WHR	0.92±0.06	0.87±0.06	<0.001
WHtR	0.56±0.05	0.50±0.05	<0.001
SBP（mmHg）	140.1±15.8	127.9±16.0	<0.001
DBP（mmHg）	79.8±10.0	74.2±9.3	<0.001
T-CHO（mmol/L）	5.37±1.06	5.20±0.97	<0.001
TG（mmol/L）	2.01（1.56-2.72）	1.13（0.85-1.49）	<0.001
HDL-C（mmol/L）	1.21±0.30	1.53±0.36	<0.001
LDL-C（mmol/L）	3.31±0.88	3.18±0.79	<0.001
HbA1c（%）	6.2±0.9	5.8±0.6	<0.001
FPG（mmol/L）	6.2±1.5	5.4±0.9	<0.001
PG2h（mmol/L）	9.6±3.7	7.0±2.5	<0.001
TyG	9.20±0.54	8.49±0.47	<0.001
TG/HDL-C	5.07±4.70	2.09±1.86	<0.001
TyG-BMI	256.16±31.55	210.42±30.80	<0.001
TyG-WC	831.43±80.07	686.95±82.61	<0.001
TyG-WHtR	5.13±0.49	4.28±0.51	<0.001

Abbreviations: WC, waist circumference; HC, hip circumference; BMI, body mass index; WHR, waist-to-hip ratio; WHtR, waist-to-height ratio; SBP, systolic blood pressure; DBP, diastolic blood pressure; T-CHO, total cholesterol; TG, triglyceride; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; HbA1c, hemoglobin Alc; FPG, fasting plasma glucose; PG2h, plasma glucose tested 2 hours after oral glucose tolerance test; TyG, triglyceride-glucose index; TG/HDL-C, plasma TG-to-HDL concentration ratio.

Five IR indices and MetS components

The mean values of the five different IR indices for Table 2 in four groups with 0, 1, 2, 3, or more MetS components, respectively. In both men and women, TyG, TG/HDL-C, TyG-BMI, TyG-WC, and TyG-WHtR increased significantly with an increase in the number of MetS components. The average values of all five IR indicators were greater in participants with three or more MetS components than in the residual groups.

Table 2 The alteration of five IR indices with the increase of MetS components

	0	1	2	≥3
men
TyG	8.22±0.34	8.41±0.42	8.70±0.49	9.23±0.59
TG/HDL-C	1.53±0.64	1.98±1.37	2.84±2.89	5.66±5.50
TyG-BMI	190.21±22.64	205.24±24.76	225.43±27.42	254.34±29.77
TyG-WC	658.07±59.37	701.53±67.02	760.63±71.21	856.34±80.29
TyG-WHtR	3.90±0.36	4.17±0.40	4.52±0.42	5.06±0.47
women
TyG	8.23±0.35	8.47±0.42	8.75±0.45	9.19±0.50
TG/HDL-C	1.39±0.61	1.91±1.91	2.69±1.88	4.63±3.96
TyG-BMI	190.95±24.17	208.79±28.46	228.51±30.12	257.48±32.74
TyG-WC	616.46±58.41	667.67±68.67	728.31±72.66	813.20±74.84
TyG-WHtR	3.91±0.39	4.25±0.45	4.64±0.47	5.19±0.49

Abbreviations: TyG, triglyceride-glucose index; TG/HDL-C, plasma TG-to-HDL concentration ratio; TyG-BMI, TyG-body mass index; TyG-WC, TyG-waist circumference index; TyG-WHtR, TyG-waist-to-height ratio index.

AUCs of five simplified IR parameters for MetS

The AUCs, sensitivity, specificity, and optimal cutoff values of the five different IR indices for predicting the risk of MetS are listed in Table 3. All five indicators showed a good diagnostic efficacy for MetS. Among men, the ranking of AUCs of all five IR indicators for MetS was TyG-WC > TyG-WHtR > TyG-BMI > TyG=TG/HDL-C. Among women, the ranking was TyG-WC > TyG-WHtR > TyG-BMI > TyG > TG/HDL-C ratio. Among both men and women, TyG-WC had the largest AUC (0.900 for men and 0.905 for women). The optimal cutoff values for TyG-WC was 779.8 in men and 746.3 in women.ROC curves of five IR indicators to predict the risk of MetS among men and women were shown in Figure 1.

Table 3AUCs of five simplified IR parameters for MetS

	AUC （95%CI）	Sensitivity （%）		specificity（%）	Cut-off value
Men
TyG	0.844（0.834,0.855）		80.5	73.6	8.76
TG/HDL-C	0.844（0.833,0.855）		80.5	73.5	2.65
TyG-BMI	0.856（0.846,0.866）		81.2	73.6	228.8
TyG-WC	0.900（0.892,0.908）		84.5	79.3	779.8
TyG-WHtR	0.892（0.884,0.900）		82.8	79.3	4.65
Women
TyG	0.859（0.851,0.867）		79.3	78.9	8.82
TG/HDL-C	0.836（0.827,0.845）		77.3	76.7	2.49
TyG-BMI	0.856（0.849,0.864）		81.9	74.1	229.2
TyG-WC	0.905（0.900,0.911）		84.3	83.1	746.3
TyG-WHtR	0.901（0.895,0.907）		84.7	80.2	4.71

Abbreviations see table 2

Fig.1 ROC curves of five IR indicators to predict the risk of MetS. A ROC curves in men. B ROC curves in women.

MetS is a cluster of cardiovascular risk factors that promotes the occurrence of T2DM and ASCVD. Therefore, the early identification and management of MetS could prevent the development of diabetes and ASCVD. IR plays an important role in MetS development of MetS^15,16. Therefore, this study evaluated and compared the predictive ability of simple IR surrogate markers such as TyG, TG/HDL-C, TyG-BMI, TyG-WC, and TyG-WHtR for MetS. We found that all five investigated IR indices demonstrated excellent predictive power for future MetS risk and that the TyG-WC index had the largest AUC in both men and women.

The liver is a major metabolic organ that plays a vital role in the regulation of glucose and lipid metabolism. IR causes excessive intrahepatic triglyceride levels by stimulating de novo hepatic lipogenesis (DNL) and gluconeogenesis. Activated hepatic gluconeogenesis also increases the blood glucose level¹⁷. The TyG index, calculated from fasting glucose and triglyceride levels, has a strong association with HEC and HOMA-IR and has been widely applied to evaluate the degree of IR^{11, 12}. Furthermore, an investigation conducted in American adults showed that the TyG index was superior to the HOMA-IR index in predicting MetS risk¹⁸. Owing to the simple measurement and low cost of the TyG index, it has become a surrogate for IR estimation and is widely used to predict the risks of T2DM, MetS and ASCVD¹⁹. The present study showed that the TyG index was associated with MetS risk. Among men, the AUC of TyG was 0.844, with a sensitivity of 80.5%, specificity of 73.6%, and cut-off point of 8.76. Among women, the AUC of TyG was 0.859, with a sensitivity of 79.3%, specificity of 78.9%, and a cutoff point of 8.82. These results are similar to those of two previous studies conducted in China^{20, 21}. Our research further confirmed the predictive value of the TyG index for MetS.

Atherogenic dyslipidemia, characterized by elevated TG and reduced HDL-C levels, is a prominent feature of MetS. The TG/HDL-C index, which combines TG and HDL-C levels, provides a more comprehensive indication of the pathogenicity and specificity of lipid abnormalities than high TG or low HDL-C levels alone²². Previous evidence has shown a strong association between the TG/HDL-C ratio and IR; therefore, the TG/HDL index is also regarded as a surrogate of IR assessment for predicting the risk of MetS^{23, 24}. In this study, we explored the predictive capacity of TG/HDL-C index for MetS. In men, the AUC of the TG/HDL-C index was 0.844, which was similar to that of the TyG index for MetS. In women, the area under the curve of the TG/HDL-C index was 0.836, which was slightly lower than that of the TyG index for MetS. Two previous studies involving Chinese and Argentine populations showed that the TyG index was better than the TG/HDL index for predicting MetS in both men and women^21,25.

Being overweight or obese, especially abdominal obesity, is closely related to IR, which promotes the development of MetS²⁶. Two studies from different regions of China showed that WC and WHtR of the anthropometric indicators, which represent abdominal obesity, could better predict the risk of MetS than BMI^27,28. Therefore, we further analyzed the diagnostic efficacy of TyG combined with three anthropometric indicators (TyG-BMI, TyG-WC, and TyG-WHtR) for MetS. The TyG-WC index had the largest AUC for MetS in both men and women (0.900 in men and 0.905 in women). The optimal cutoff points for TyG-WC was 779.8 in men and 746.3 in women. In this study, TyG-WC and TyG-WHtR outperformed TyG, TG/HDL-C ratio, and TyG-BMI in predicting MetS. These results are consistent with those of a study conducted in Nigerian population²⁹. Our study suggests that TyG levels combined with anthropometric indices representing abdominal obesity could enhance the sensitivity and accuracy of identifying MetS.

In this study, we also analyzed the changes in five different IR indices in four groups with 0, 1, 2, 3, or more MetS components. These results showed that all five IR indicators increased significantly with the number of MetS components. The results demonstrated that the more severe the IR, the more severe was the metabolic disorder.

The strengths of our study include its large sample size and good representativeness. We excluded individuals with established diabetes because the use of antidiabetic medicines may reduce fasting plasma glucose levels. However, our study has some limitations. The population enrolled in this study was residents of Beijing; therefore, the results cannot be generalized to other regions of China. In addition, individuals who had been diagnosed with hypertriglyceridemia and treated with anti-triglyceride medication were not excluded, which may have reduced the TyG index value.

In summary, all five simplified IR surrogate indices predicted MetS risk. Among the five IR parameters, TyG-WC index had the highest predictive efficacy for MetS in both men and women. Therefore, to prevent the occurrence of T2DM and ASCVD, the TyG-WC index can be used for the early screening and identification of MetS.

Ethical Approval and Informed Consent

This study complies with the Declaration of Helsinki and was approved by the First Medical Centre of Chinese PLA General Hospital Ethics Committee.

Acknowledgments

This study was supported by the National Key New Drug Creation and Manufacturing Program of the Ministry of Science and Technology (2011ZX09307001-08). We would like to thank all authors for their contributions.

Disclosure

The authors declare no conflicts of interest in this work.

Availability of Data and Materials

Our data cannot be shared openly in order to protect study participant privacy. The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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No competing interests reported.

Predictive value of simplified insulin resistance assessment indicators for metabolic syndrome in middle-aged and elderly Chinese without established diabetes

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Abstract

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Introduction

Methods

Results

Discussion

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References

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