Clinical Significance of the Lipid Profile Ratios and Triglyceride Glucose Index in the Diagnosis of Metabolic Syndrome

Abstract

Introduction:

Metabolic syndrome (MetS) is a pathophysiological condition defined by a set of metabolic alterations such as hypertriglyceridemia, hyperglycemia, hypertension, low HDL-c levels, and visceral obesity. Its presence identifies people with an increased risk of developing cardiovascular diseases and type 2 diabetes; however, the lack of practical and reliable methods for its diagnosis limits the identification of people with this condition. In this sense, the objective of this study was to analyze the diagnostic utility of markers derived from the lipid profile [triglyceride–glucose (TyG) index and the ratios total cholesterol (TC)/high-density lipoprotein cholesterol (HDL-c), triglyceride (TG)/HDL-c, low-density lipoprotein cholesterol/HDL-c, fasting blood glucose (FBG)/HDL-c, and white blood cell/HDL-c] in the determination of MetS.

Methods:

A retrospective study was designed that included 619 individuals. A logistic regression model was used to evaluate the associations of the different markers with MetS, and the cutoff points of the markers were determined through an analysis of receiver operating characteristic curves and the Youden Index.

Results:

A positive and significant association was observed between all markers and the presence of MetS. The cutoff values for the markers that best predicted MetS were TyG ≥ 4.8 (sensitivity = 91.4%, specificity = 74.3%), TC/HDL-c ≥ 3.7 (sensitivity = 74.3%, specificity = 75.7%), TG/HDL-c ≥ 3.3 (sensitivity = 82.5%, specificity = 84.0%), and FBG/HDL-c ≥ 2.0 (sensitivity = 85.1%, specificity = 79.7%).

Conclusion:

Our study demonstrated the diagnostic relevance of the different markers in detecting MetS, suggesting that these ratios may be useful in clinical practice for the opportune and accurate diagnosis of MetS.

Introduction

Metabolic syndrome (MetS) is a pathophysiological condition in which four main characteristics are distinguished: insulin resistance (IR), central obesity, atherogenic dyslipidemia, and endothelial dysfunction.¹ The MetS is defined by a set of metabolic alterations, according to the third report of the National Cholesterol Education Program Adult Treatment Panel (NCEP ATP-III), the diagnosis of this condition is granted if three or more of the following five criteria are met: blood pressure greater than 130/85 mmHg, waist circumference (WC) ≥40 inches in men and ≥35 inches in women, fasting blood glucose (FBG) levels ≥100 mg/dL, fasting triglyceride (TG) levels ≥150 mg/dL, and fasting high-density lipoprotein cholesterol (HDL-c) levels <40 mg/dL in men and <50 mg/dL in women.² Its presence discriminates between a specific group of patients with a shared pathophysiology, those with an increased risk of developing cardiovascular disease (CVD) and type 2 diabetes (T2D). However, the lack of practical methods for its diagnostic implementation limits its application in the field of preventive medicine. In this context, different markers derived from the lipid profile have been proposed for the opportune and accurate diagnosis of different metabolic pathologies; for example, the following have been evaluated: the triglyceride–glucose (TyG) index as a marker of IR,³ MetS⁴ and coronary events in patients with T2D, and in patients with acute coronary syndrome;⁵ TG/HDL-c ratio as a marker of IR,^6
–8 MetS,^9,10 diabetes,¹¹ development of CVD,^12,13 and nonalcoholic fatty liver;¹⁴ total cholesterol (TC)/HDL-c ratio as a predictor of premature myocardial infarction¹⁵ and CVD;^16,17 low-density lipoprotein cholesterol (LDL-c)/HDL-c ratio as a marker of nonalcoholic fatty liver¹⁸ and as a predictor of coronary artery disease subsequent to acute myocardial infarction;¹⁹ likewise, FBG/HDL-c and white blood cell (WBC) count/HDL-c ratios have been evaluated as predictors of mortality resulting from coronary artery disease.^20,21 However, previous studies have shown that the cutoff points for determining people at risk can vary depending on their ethnic origin;^22,23 therefore, the objective of this study was to determine and compare the accuracy diagnosis of the different markers derived from the lipid profile (TyG, TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c) in the diagnosis of MetS in the adult population of Mexico.

Participants and Methods

Study population

This retrospective study included the participation of 619 subjects (228 men and 391 women) aged 44.0 ± 13.0 years, from the metropolitan area of the city of Zacatecas, Mexico. None of the individuals had vascular complications, pregnancy, hypothyroidism, or clinical infections disease. In addition, the individuals were not regular smokers, and they did not ingest alcohol on regular basis. People under regular pharmacological treatment for metabolic disorders (e.g., statins, hypoglycemic agents, and insulin) were included and people under hormonal treatment (e.g., corticosteroids and levothyroxine), chemotherapy, as well as lactating women were excluded. All participants were informed about the study and signed an informed consent. The protocol was approved by the Bioethics Committee of the Mexican Institute of Social Security (IMSS), with the registration numbers R-2018-785-072 and SALUD-2012-01-182554.

Anthropometric and biochemical characteristics

Anthropometric measurements were obtained by trained personnel. Body mass index (BMI, kg/m²) and waist–hip ratio (WHR, waist cm/hip cm) were determined; a BMI <25 was considered normal weight, a BMI ≥25 and <30 was considered overweight, and a BMI ≥30 was considered obese. After fasting for 10–12 h, a blood sample was taken by venipuncture for the determination of WBC and levels of FBG, glycated hemoglobin (Hb1Ac), TC, HDL-c, LDL-c, and TG, in accordance with the conventional protocols of the IMSS Zone 1 General Hospital. The TyG index was used as a surrogate marker for the determination of TG-driven IR; a TyG index ≥4.6 indicates IR. This index was calculated as Ln [fasting triglycerides (mg/dL) × fasting glucose (mg/dL)]/2 ³. For their part, the ratios TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c were calculated by dividing the levels of TC (mg/dL), TG (mg/dL), LDL-c (mg/dL), FBG (mg/dL), and WBC (×10⁷/dL) between the levels of HDL-c (mg/dL), respectively. The diagnosis of MetS was established according to the NCEP ATP-III criteria,² with values adjusted to the Mexican population.²⁴

Statistical analysis

Statistical analysis was performed using SPSS software (IBM Statistics version 20.0). The Shapiro–Wilk test was used to determine the distribution of quantitative variables; because all variables presented a non-normal distribution, quantitative variables were compared using the nonparametric Mann–Whitney U test, whereas the chi-squared test (χ ²) was used for qualitative variables. The Spearman rank test was used to analyze the correlations between the TyG index and the TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c ratios with the different quantitative variables established. The association between the TyG index and the TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c ratios with MetS was analyzed using a logistic regression analysis. To define the cutoff point at which the greatest sensitivity and specificity of the index and the ratios evaluated is obtained, the receiver operating characteristic (ROC) curve analysis and the Youden Index were performed, and an area under the curve (AUC) ≥0.7 was considered acceptable. A value of p < 0.05 was considered significant.

Results

Anthropometric and biochemical characteristics

A total of 619 people participated in this study, of whom 36.8% were men and 63.2% were women, whose average age was 44 ± 13.0 years. The individuals consisted in Mexican Mestizo population, which is defined as people born in the country having a Spanish-derived last name, with family antecedents of Mexican ancestors.²⁵ Participants were classified according to the presence of MetS (43.5%, 94 males; 175 females) or its absence (control group) (56.5%, 134 males; 216 females). Participants diagnosed with MetS presented values of the TyG index and ratios of TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c, significantly higher compared with the control group (p < 0.001). Both groups differ in obesity indicators such as BMI, WC, and WHR, whose values were higher in the group with MetS (p < 0.001) compared with the control group. Likewise, blood levels of FBG, Hb1Ac, TC, LDL-c, and TG were found to be statistically higher in the MetS group compared with the control group; however, HDL-c blood levels were higher in the control group compared with people diagnosed with MetS (p < 0.001) (Table 1).

Table 1.

Anthropometric and Biochemical Characteristics of the Study Groups According to the MetS

Variable	Control group	MetS	P
n	350	269	—
Sex (M:F)^a	134:216	94:175	0.402
Age^b	45.50 (35.00–54.25)	43.00 (32.00–52.00)	<0.05
BMI (kg/m²)^b	26.36 (23.62–29.80)	30.06 (27.01–33.16)	<0.001
WC (cm)^b	91.00 (83.00–101.0)	100.0 (95.00–108.0)	<0.001
WHR^b	0.895 (0.842–0.952)	0.933 (0.894–0.980)	<0.001
WBC (×10⁹/L)^b	5.400 (4.475–6.525)	5.300 (4.200–6.600)	0.442
FBG (mg/dL)^b	89.00 (81.75–98.00)	121.0 (103.0–174.0)	<0.001
Hb1Ac (%)^b	5.90 (5.40–6.60)	7.00 (6.20–8.85)	<0.001
TC (mg/dL)^b	182.0 (161.5–205.0)	194.0 (168.0–217.8)	<0.001
HDL-c (mg/dL)^b	56.40 (50.60–65.95)	44.90 (39.53–52.38)	<0.001
LDL-c (mg/dL)^b	97.60 (76.55–117.9)	104.5 (84.33–122.5)	<0.05
TG (mg/dL)^b	125.0 (92.00–154.3)	206.5 (168.0–268.8)	<0.001
TyG^b	4.685 (4.504–4.854)	5.105 (4.942–5.274)	<0.001
TC/HDL-c^b	3.196 (2.723–3.680)	4.229 (3.657–4.807)	<0.001
TG/HDL-c^b	2.171 (1.481–2.959)	4.329 (3.535–6.152)	<0.001
LDL-c/HDL-c^b	1.719 (1.304–2.116)	2.222 (1.756–2.769)	<0.001
FBG/HDL-c^b	1.566 (1.320–1.917)	2.631 (2.183–3.773)	<0.001
WBC/HDL-c^b	93.44 (71.34–121.8)	114.5 (90.85–149.7)	<0.001

Data are presented as median (interquartile range) or proportions.

The p value was calculated using the χ² test or the Mann–Whitney U test.

χ² test.

Mann–Whitney U test.

BMI, body mass index; F, female; FBG, fasting blood glucose; Hb1Ac, glycated hemoglobin; HDL-c, high-density lipoprotein cholesterol; LDL-c, low-density lipoprotein cholesterol; M, male; METs, metabolic syndrome; TC, total cholesterol; TG, triglycerides; WBC, white blood cell count; WC, waist circumference; WHR, waist-to-hip ratio.

Bivariate correlation analysis

The results of the bivariate correlation analysis demonstrated a statistically significant relationship between the TyG index and the TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c ratios with the MetS components: WC (rho = 0.360, p < 0.001; rho = 0.288, p < 0.001; rho = 0.355, p < 0.001; rho = 0.210, p < 0.001; rho = 0.360, p < 0.001; rho = 0.135, p < 0.01, respectively); FBG (rho = 0.735, p < 0.001; rho = 0.333, p < 0.001; rho = 0.344, p < 0.001; 0.264, p < 0.001; rho = 0.834, p < 0.001; rho = 0.059, p = 0.144, respectively); HDL-c (rho = −0.356, p < 0.001; rho = −0.704, p < 0.001; rho = −0.688, p < 0.001; rho = −0.551, p < 0.001; rho = −0.662, p < 0.001; rho = −0.535, p < 0.001, respectively); and TG (rho = 0.850, p < 0.001; rho = 0.589, p < 0.001; rho = 0.919, p < 0.001; rho = 0.319, p < 0.001; rho = 0.439, p < 0.001; rho = 0.227, p < 0.001, respectively). Likewise, significant correlations with the other established variables were observed (Table 2).

Table 2.

Correlations of the Study Variables: TyG, TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c with the MetS Components and the Anthropometric and Biochemical Characteristics of the Study Subjects

	TyG		TC/HDL-c		TG/HDL-c		LDL-c/HDL-c		FBG/HDL-c		WBC/HDL-c
Variable	rho	P	rho	P	rho	P	rho	P	rho	P	rho	P
Age	–0.078	0.054	–0.001	0.988	–0.037	0.352	–0.007	0.858	–0.072	0.072	–0.007	0.856
BMI (kg/m²)	0.337	<0.001	0.292	<0.001	0.359	<0.001	0.216	<0.001	0.301	<0.001	0.147	<0.001
WC (cm)	0.360	<0.001	0.288	<0.001	0.355	<0.001	0.210	<0.001	0.360	<0.001	0.135	<0.01
WHR	0.290	<0.001	0.272	<0.001	0.278	<0.001	0.233	<0.001	0.345	<0.001	0.132	<0.01
WBC (×10⁹/L)	–0.050	0.215	–0.080	<0.05	–0.030	0.456	–0.083	<0.05	–0.089	<0.05	0.768	<0.001
FBG (mg/dL)	0.735	<0.001	0.333	<0.001	0.344	<0.001	0.264	<0.001	0.834	<0.001	0.059	0.144
Hb1Ac (%)	0.577	<0.001	0.262	<0.001	0.256	<0.001	0.208	<0.001	0.642	<0.001	0.040	0.317
TC (mg/dL)	0.361	<0.001	0.514	<0.001	0.211	<0.001	0.576	<0.001	0.051	0.203	–0.136	<0.01
HDL-c (mg/dL)	–0.356	<0.001	–0.704	<0.001	–0.688	<0.001	–0.551	<0.001	–0.662	<0.001	–0.535	<0.001
LDL-c (mg/dL)	0.191	<0.001	0.575	<0.001	0.115	<0.01	0.776	<0.001	0.108	<0.01	–0.051	0.202
TG (mg/dL)	0.850	<0.001	0.589	<0.001	0.919	<0.001	0.319	<0.001	0.439	<0.001	0.227	<0.001

Spearman’s rank correlation coefficient.

BMI, body mass index; FBG, fasting blood glucose; Hb1Ac, glycated hemoglobin; HDL-c, high-density lipoprotein cholesterol; LDL-c, low-density lipoprotein cholesterol; METs, metabolic syndrome; TC, total cholesterol; TG, triglycerides; WBC, white blood cells; WC, waist circumference; WHR, waist-to-hip ratio.

Multivariable association analysis

After observing that the study variables were correlated with the MetS components and, to investigate their association as risk factors for the development of this condition, a logistic regression analysis was performed. It was found that the association between MetS and the study variables remained significant, even after adjustment for sex and age: TyG [odds ratio (OR) = 2.504, confidence interval (CI) = 1.131–5.544, p < 0.05]; TC/HDL-c (OR = 2.449, CI = 1.245–4.818, p < 0.01); TG/HDL-c (OR = 7.383, CI = 3.428–15.90, p < 0.001); LDL-c/HDL-c (OR = 2.164, CI = 1.024–4.573, p < 0.05); FBG/HDL-c (OR = 23.53, CI = 10.02–55.24, p < 0.001); and WBC/HDL-c (OR = 1.867, CI = 1.109-3.144, p < 0.05) (Table 3).

Table 3.

Associations Between the Study Variables: TyG, TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c with the MetS

Variable	OR	CI (95%)	P
TyG	2.504	1.131–5.544	<0.05
TC/HDL-c	2.449	1.245–4.818	<0.01
TG/HDL-c	7.383	3.428–15.90	<0.001
LDL-c/HDL-c	2.164	1.024–4.573	<0.05
FBG/HDL-c	23.53	10.02–55.24	<0.001
WBC/HDL-c	1.867	1.109–3.144	<0.05

Values adjusted for sex and age. Binomial logistic regression test (the model considers the relationships with WC, BMI, FBG, TC, HDL-c, LDL-c, and TG).

CI, confidence interval; FBG, fasting blood glucose; HDL-c, high-density lipoprotein cholesterol; LDL-c, low-density lipoprotein cholesterol; METs, metabolic syndrome; OR, odds ratio; TC, total cholesterol; TG, triglycerides; WBC, white blood cells.

ROC curve analysis

According to the Youden Index of the ROC curves, the optimal cutoff values of the TyG index and the ratios of the lipid profile in which the greatest joint sensitivity and specificity are obtained were the following: TyG (≥4.823), TC/HDL-c (≥3.701), TG/HDL-c (≥3.311), LDL-c/HDL-c (≥2.007), FBG/HDL-c (≥2.001), and WBC/HDL-c (≥101.06). Furthermore, the AUC was significant for TyG (0.904), TC/HDL-c (0.812), TG/HDL-c (0.903), LDL-c/HDL-c (0.713), FBG/HDL-c (0.885), and WBC/HDL-c (0.660), with a significance value of p < 0.001 in all cases. The TyG index (sensitivity = 91.40%, specificity = 74.30%) and the TC/HDL-c (sensitivity = 74.3%, specificity = 75.7%), TG/HDL-c (sensitivity = 82.50%, specificity = 84.00%), and FBG/HDL-c (sensitivity = 85.10%, specificity = 79.70%) ratios were the markers that demonstrated the highest diagnostic accuracy (Table 4, Fig. 1).

FIG. 1.

Receiver operating characteristic curves of the different markers derived from the lipid profile. Receiver operating characteristic curves for TyG index and TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c ratios as indicators of high risk of MetS. FBG, fasting blood glucose; HDL-c, high-density lipoprotein cholesterol; LDL-c, low-density lipoprotein cholesterol; TC, total cholesterol; TG, triglyceride; TyG, triglyceride–glucose; WBC, white blood cell.

Table 4.

Diagnostic Accuracy of the Study Variables: TyG, TC/HDL-c, TG/HDL-c, LDL-c/HDL-c, FBG/HDL-c, and WBC/HDL-c in MetS

Variable	AUC	CI (95%)	P	Cutoff	Sensitivity	Specificity
TyG	0.904	0.881–0.927	<0.001	≥4.823	91.40	74.30
TC/HDL-c	0.812	0.779–0.846	<0.001	≥3.701	74.30	75.70
TG/HDL-c	0.903	0.880–0.926	<0.001	≥3.311	82.50	84.00
LDL-c/HDL-c	0.713	0.673–0.754	<0.001	≥2.007	63.20	70.00
FBG/HDL-c	0.885	0.859–0.911	<0.001	≥2.001	85.10	79.70
WBC/HDL-c	0.660	0.617–0.703	<0.001	≥101.06	66.20	58.00

Receiver operating characteristic curve analysis.

AUC, area under the curve; CI, confidence interval; FBG, fasting blood glucose; HDL-c, high-density lipoprotein cholesterol; LDL-c, low-density lipoprotein cholesterol; METs, metabolic syndrome; TC, total cholesterol; TG, triglycerides; WBC, white blood cells.

Discussion

In this study, we analyzed the association of different markers of the lipid profile with MetS, and our results demonstrated the diagnostic accuracy of the TyG index and the TC/HDL-c, TG/HDL-c, and FBG/HDL-c ratios to identify individuals at high risk of developing MetS in the Mexican Mestizo population. The cutoff values for the markers that best predicted MetS were TyG index ≥4.8, TC/HDL-c ratio ≥3.7, TG/HDL-c ratio ≥3.3, and FBG/HDL-c ratio ≥2.0. Previous studies have established different cutoff points for some of these markers for the diagnosis of MetS. For example, in a study carried out in an adult population between 18 and 59 years of age in Brazil, the cutoff value for the TyG index ≥4.52 (sensitivity = 84.3%, specificity = 75.7%) was proposed,⁴ and compared with the cutoff point that we propose in our study (≥4.8), we obtained greater sensitivity and specificity. Likewise, cutoff values have been established for the TG/HDL-c ratio in the diagnosis of MetS; in a study carried out in Mexican Mestizo adults, a value of ≥3.0 was proposed (sensitivity = 86.9%, specificity = 66.8%),⁹ which was similar to that observed in our analyzes (≥3.3), however, we obtained greater specificity and similar sensitivity with the cutoff point that we propose, likewise, cutoff points have also been established for this same ratio in the population of Germany,⁸ Argentina,²⁶ and China;¹⁰ however, as mentioned, the cutoff points must be established for each specific population because of the impact generated by ethnic origin on the distribution of the variables.^22,23 Otherwise, it is important to mention that our study is the first to consider the FBG/HDL-c ratio as a diagnostic marker for MetS; our results demonstrated its high diagnostic accuracy at the cutoff point ≥2.0 (sensitivity = 85.1%, specificity = 79.7%; OR = 23.53) in our study population. From a clinical point of view, physicians and patients can benefit from establishing practical diagnostic methods that accurately identify individuals with MetS, facilitating the approach to pharmacological treatment, and recommending preventive lifestyle changes.

The main strength of our study is the participation of people in a risk state who were overweight or obese but did not have MetS, which allowed us to demonstrate the robustness of the different markers as diagnostic tests. In contrast, our study proposes novel markers as diagnostic tests for MetS. Some of the limitations of our work is that our analysis model only adjusts for age, sex, and presence of obesity and does not consider other variables that could influence (physical activity, diet, and hereditary family history).

Conclusion

In conclusion, our study demonstrated that the relative ratios of lipid profile are positively associated with the high risk of presenting MetS in Mexican Mestizo adults. The cutoff values for the markers that best predict MetS and in which the highest diagnostic accuracy was presented were TyG index ≥4.8 and TC/HDL-c ≥3.7, TG/HDL-c ≥3.3, and FBG/HDL-c ≥2.0 ratios; these values maintained their significant association even after adjustment for age, sex, and presence of overweight or obesity, suggesting that these ratios may be useful in clinical practice for a timely, accurate, and reproducible diagnosis of MetS.

Footnotes

Authors’ Contributions

The authors confirm contribution to the article as follows: Material preparation, data collection, and analysis were performed by A.C.-J. The first draft of the manuscript was written by A.C.-J., and all authors commented on the previous versions of the article. Study conception and design were performed by M.H.G.-H. and A.C.-J. Draft manuscript preparation was performed by A.C.-J., and D.P.P.-PO. and B.R.-S. reviewed and approved the final version of the article. All authors read and approved the final article.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

The research reported in this article did not receive any financial support.

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