Visceral Adiposity Index,Triglyceride/High-Density Lipoprotein Ratio,and Lipid Accumulation Product Index to Discriminate Metabolic Syndrome Among Adult Type 1 Diabetes Patients

Abstract

Background:

Obesity and metabolic syndrome (MetS) are growing problems in type 1 diabetic patients; these can influence clinical complications and also treatment regimens. Visceral adipose tissue inflammation plays an important role in cardiovascular complications. Visceral adiposity index (VAI), lipid accumulation product index (LAP), and triglyceride (TG)/high-density lipoprotein (HDL) ratio have been strongly correlated with insulin resistance and visceral adipose tissue amount in previous studies. Therefore, this study aimed to investigate and compare the usefulness of these indices to detect MetS in patients with type 1 diabetes mellitus (T1DM).

Materials and Methods:

Patients with T1DM and gender- and age-matched controls were included in this cross-sectional study. MetS was defined using both International Diabetes Federation (IDF), World Health Organization (WHO), and National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III) criteria. T1DM patients were divided into two groups according to the IDF criteria. VAI, LAP, and TG/HDL ratio were calculated for all patients. Groups were compared accordingly.

Results:

One hundred twenty-six patients with T1DM were included in the study. Increased VAI was observed in association with MetS. Patients with MetS (32.2%) had the highest VAI than healthy controls (8.21 ± 8.86; 3.49 ± 2.73, respectively, P < 0.01). For determining MetS in type 1 diabetes, the cutoff value of VAI was 2.65 [area under the curve (AUC) = 0.837, sensitivity 80.0%, specificity 72.8%], LAP was 27.57 (AUC = 0.842, sensitivity 80.0%, specificity74.0%), TG/HDL ratio was 2.18 (AUC = 0.826, sensitivity 75.0%, specificity 74.0%), each P < 0.001.

Conclusions:

MetS becomes increasingly common in T1DM. VAI, LAP, and TG/HDL ratio were useful for predicting MetS in patients with T1DM.

Introduction

Obesity, as a growing pandemic, affects a significant proportion of the entire population. Concurrently, its prevalence is increased in patients with type 1 diabetes mellitus (T1DM), ranging from 14 to 47.8%.^1,2 T1DM is recognized as a chronic autoimmune disease with destruction of autoimmune beta cells. Metabolic syndrome (MetS), which includes abdominal obesity as its most common component, is increasingly diagnosed at younger ages, and this increased prevalence has been found to be associated with increased microvascular and macrovascular complications^3,4

MetS in T1DM has been shown to be important because it increases cardiovascular risk and other diabetic complications.³ Visceral adipose tissue plays an important role in the underlying pathophysiology. Previous studies have associated increased cardiovascular risk with visceral adipose tissue.^4,5 Therefore, although measuring visceral adipose tissue is challenging in clinical practice, several indices have been developed to estimate visceral adipose tissue and cardiovascular risk.

Visceral adiposity index (VAI), which has been used to predict insulin resistance and related diseases, is strongly associated with insulin resistance and visceral adipose tissue deposition calculated by magnetic resonance imaging (MRI).⁶ VAI has been shown to be a better parameter than other anthropometric indices. It has been also a simple and early indicator of metabolic abnormalities that can lead to cardiovascular complications.^7,8 Lipid accumulation product index (LAP), an index based on triglyceride (TG) and waist circumference (WC), had been shown to be an indicator of insulin resistance.^9,10 Similarly, TG/high-density lipoprotein (HDL) has been associated with MetS and insulin resistance.¹¹ However, there are insufficient studies comparing these three indices in patients with T1DM.

Therefore, we aimed to investigate the frequency, characteristics of MetS in T1DM patients and VAI, LAP, TG/HDL ratio, and compare their predictability of MetS in type 1 diabetes.

Materials and Methods

Study design

T1DM patients (n = 126) and age- and gender-matched control subjects (n = 58) were enrolled in this study. All individuals were regularly followed up at endocrinology and metabolism department, Istanbul Research and Education Hospital, Turkey. Patients between 18 and 65 years and previously confirmed as type 1 diabetes were included. Patients >65 years, pregnant, who have incomplete records, and co-morbidities such as liver disease, active infections, and cancers were excluded. After exclusion criteria, 118 patients were included. All patients were on intensive insulin therapy. Subjects aged 18–65 years, from routine screening programs, euthyroid, and who do not have any chronic disease such as liver failure, renal failure, active infection, or cancer were included in the age- and gender-matched control group of the study. The study was performed in accordance with Declaration of Helsinki guideline. Ethical approval for this study was granted by the Ethics Committee of Istanbul Research and Education Hospital (2021/2667).

Clinical and biochemical analysis

All physical measurements (body weight, height, body mass index (BMI), WC, hip circumference, and laboratory examinations were performed at the same clinic. WC was measured between the lower costal margin and iliac crest. BMI was calculated by formula as body weight (kg)/height (m²). Blood pressure was measured using a mercury manometer after 15 min of resting. Diagnosis of hypertension was made according to Joint National Committee (JNC) 7 guideline.

Biochemical parameters, including fasting plasma glucose, serum hemoglobin A1c (HbA1c) (measured by spectrophotometry), TG, HDL-cholesterol (HDL-c), and low-density lipoprotein-cholesterol (LDL-c), were performed at the same hospital laboratory. All the laboratory data were reported from the patients' last visit to the clinic. Urine albumin creatinine ratio was measured with immunoturbidimetric method.

MetS frequency was calculated using the National Cholesterol Education Program Adult Treatment Panel III (NCEP- ATP III), WHO, and International Diabetes Federation (IDF) criteria. WHO criteria included (1) hypertension: systolic blood pressure ≥140 mmHg, and/or diastolic blood pressure ≥90 mmHg, and/or receiving antihypertensive medication; (2) dyslipidemia: plasma TGs >1.7 mmol/L (150 mg/dL) and/or decreased HDL-c (<35 for men, <39 mg/dL for women), (3) waist/hip ratio >0.90 or BMI >30 kg/m²; (4) microalbuminuria: spot urine albumin >30 mg/L; and (5) fasting blood glucose >110 mg/dL (absolutely required). Two or more of 1–4 criteria plus fasting glucose >100 mg/dL positive was defined as MetS.^8,9 NCEP ATP III criteria included (1) WC >88 for women, >102 for men; (2) fasting blood glucose >100 mg/dL or antihyperglycemic medication; (3) TGs >1.7 mmol/L (150 mg/dL) and/or any antihypertriglyceridemia medication; (4) decreased HDL-c (<40 mg/dL for men, <50 mg/dL for women); and (5) >130 mmHg systolic or >85 mmHg diastolic blood pressure or antihypertensive treatment. Three of these criteria were defined as MetS.¹² IDF criteria included (1) central obesity men >94 cm, women >80 cm (absolutely required); (2) fasting blood glucose >100 mg/dL or antihyperglycemic medication; (3) TGs >1.7 mmol/L (150 mg/dL) and/or any antihypertriglyceridemia medication; (4) decreased HDL-c (<40 mg/dL for men, <50 mg/dL for women); and (5) >130 mmHg systolic or >85 mmHg diastolic blood pressure or antihypertensive treatment.¹³

VAI was calculated for each person using the following gender-specified formula developed by Amato et al.⁶ VAI = waist circumference (cm)/[39,68+(1.88*BMI) *(TG/1.03) *(1.31/HDL-c) for male] and VAI = waist circumference (cm)/[36,58+(BMI *1.89) *(TG/0.81) *(1.52/HDL-c) for female]. LAP index was calculated by the formulation for women: [WC (cm) −58] × TG (mmol/L), and for men: [WC (cm) −65] × TG (mmol/L).¹⁴

Statistical analysis

Statistical evaluations were performed using SPSS 22.0 (Statistical Package for the Social Sciences software version 22.0) (SPSS, Inc., Chicago, IL). Descriptive analyses were expressed as mean ± standard deviation, percentages (%), odds ratios, beta (β), and 95% confidence intervals (CIs). Kolmogorov–Smirnov or Shapiro–Wilk W was used for normality. The chi-squared test or Fisher's exact test, where appropriate, was used for categorical variables. Student's t-test was used for comparison of normality distributed continuous variables of two groups. The Mann–Whitney U test was used for comparisons of continuous variables that were not normally distributed between two groups. In logistic regression analyses, dependent variables: neuropathy, nephropathy, retinopathy; independent variables: adjustments for age, gender, diabetes duration, HbA1c were carried out. One-way analysis of variance was used for comparison of continuous variables of three different groups. Logarithmic transformation was used to continuous variables that were not normally distributed. The capacity of VAI, LAP, and HDL/TG ratio in predicting the presence of MetS was analyzed using receiver operating characteristic (ROC) curve analysis with the area under the curve (AUC) value. Sensitivity and specificity were examined. Statistical significance was accepted as P < 0.05.

Results

Mean age, gender, and BMI did not differ between groups ((P > 0.05). T1DM patients were classified as MetS (n = 38, 32.2%) and non-MetS (n = 80, 67.8%) according to IDF criteria. Mean age of T1DM-MetS(+) was higher than in T1D-MetS(−) (37.47 ± 8.58 vs. 32.81 ± 13.01 years, P < 0.047) (Table 1).

Table 1.

Properties of Type 1 Diabetes Groups and Healthy Subjects

	Control (n = 58)	T1D-MetS(−) (n = 80)	T1D-MetS(+) (n = 38)	P^*	P^**	P^***
Age (years)	36.34 ± 13.16	32.81 ± 13.01	37.47 ± 8.58	0.119	0.642	0.047
Systolic BP (mmHg)	122.25 ± 11.81	120.25 ± 13.58	125.92 ± 13.89	0.262	0.235	0.038
Diastolic BP (mmHg)	69.22 ± 9.81	71.16 ± 10.07	73.94 ± 11.3	0.260	0.031	0.178
Body weight (kg)	74.60 ± 14.97	69.58 ± 12.24	77.39 ± 18.33	0.032	0.416	0.007
WC (cm)	89.39 ± 14.23	82.32 ± 9.99	91.76 ± 11.68	0.001	0.433	0.001
BMI (kg/m²)	25.50 ± 3.39	24.14 ± 3.27	27.47 ± 5.10	0.019	0.026	0.010
HbA1c (%)	5.62 ± 0.38	9.03 ± 1.89	9.73 ± 1.89	<0.01	<0.01	0.065
Fasting glucose (mg/dL)	93.92 ± 12.60	186.23 ± 75.47	215.97 ± 66.17	<0.01	<0.01	0.040
Postprandial glucose (mg/dL)	108.01 ± 33.60	251.01 ± 59.22	286.11 ± 54.05	<0.01	<0.01	0.044
Triglyceride (mg/dL)	121.98 ± 76.05	99.81 ± 77.01	199.33 ± 117.83	0.139	0.002	<0.01
HDL (mg/dL)	52.25 ± 12.55	55.00 ± 10.87	44.53 ± 10.84	0.172	0.001	<0.01
LDL (mg/dL)	126.91 ± 44.28	109.63 ± 34.81	125.53 ± 38.15	0.012	0.877	0.033
Total insulin dose (U/day)	—	66.12 ± 19.15	69.90 ± 22.15			0.722
Diabetes duration (years)		11.02 ± 7.96	12.50 ± 9.25			0.374
Lipid accumulation product	41.81 ± 39.81	24.42 ± 27.11	65.90 ± 51.09	<0.01	<0.01	<0.01
TG/HDL ratio	2.51 ± 1.81	1.89 ± 1.37	4.66 ± 3.33	0.081	<0.01	<0.01
VAI	3.49 ± 2.73	2.49 ± 1.72	8.21 ± 8.86	0.013	<0.01	<0.01

P ^*control vs. T1DM-MetS(−), P ^**control vs. T1DM-MetS(+), P ^*** T1DM-MetS(−) vs. T1DM-MetS(+).

BMI, body mass index; BP, blood pressure; HbA1c, hemoglobin A1c; LDL, low-density lipoprotein; MetS, metabolic syndrome; T1DM, type 1 diabetes mellitus; TG/HDL, triglyceride/high-density lipoprotein; VAI, visceral adiposity index; WC, waist circumference.

Body weight and WC of T1DM-MetS(+) patients (77.39 ± 18.33 kg, 91.76 ± 11.68 cm) and control group (74.60 ± 14.97 kg, 89.39 ± 14.23 cm) did not significantly differ (P > 0.05), whereas T1DM-MetS(−) patients were leaner (69.58 ± 12.24 kg, 91.76 ± 11.68 cm).

Fasting glucose, postprandial glucose, and TG levels were highest in T1D-MetS(+) and lowest in the control group. There were significant differences between the three groups (Table 1). HDL-c was lowest (44.07 ± 11.28 mg/dL) in T1DM MetS(+) group and highest (55.50 ± 10.41 mg/dL) in T1DM-MetS(−) group (P < 0.01).

Total insulin dose was 69.90 ± 22.15 U/day for T1DM-MetS(+) and 66.12 ± 19.15 U/day for T1DM-MetS(−) group, and did not significantly differ (P > 0.05). Diabetes duration was 12.50 ± 9.25 years for T1DM-MetS(+) and 11.02 ± 7.96 years for T1DM-MetS(−) group (P > 0.05) (Table 1).

Hypertension (according to IDF criteria), obesity (BMI >30 kg/m²), and MS positivity (according to WHO and NCEP ATP III criteria) frequencies are given in Table 2.

Table 2.

Metabolic Syndrome Frequency, Hypertension, and Obesity Ratio for Groups

	Control (n = 58)	T1DM-MetS(−) (n = 80)	T1DM-MetS(+) (n = 38)	P^*	P^**	P^***
IDF (%)	8.8	0	100	0.007	<0.01	<0.01
WHO (%)		2.6	62.2			<0.01
NCEP (%)	7.0	0	70.3	0.018	<0.01	<0.01
Women (%)	46.6% (n = 27)	37.5% (n = 30)	47.4% (n = 18)	0.286	0.937	0.308
Hypertension (%)	13.8	15.0	42.1	0.842	0.002	0.010
Obese (BMI ≥30 kg/m²)	13.8	6.2	31.6	0.134	0.036	0.001

P ^*control vs. T1DM MetS(−).

P ^**control vs. T1DM MetS(+).

P ^***T1DM MetS(−) vs. T1DMMetS(+).

IDF, International Diabetes Federation; NCEP, National Cholesterol Education Program; WHO, World Health Organization.

When IDF criteria were applied, 32.2% of type 1 diabetes patients had MetS. It was 8.8% for the control group. Increased WC (29.9%) was the most common MetS criteria after diabetes followed by increased TG (27.3%), decreased HDL-c (23.1%), and elevated blood pressure (21.3) in all T1D patients (Table 3).

Table 3.

Characteristics of Metabolic Syndrome Criteria Fulfilling Among Type 1 Diabetes Patients

MetS criteria^a	All T1DM patients (n = 117)	Female (n = 48)	Male (n = 69)	P value for gender groups	Age 18–34 (n = 55)	Age 35–60 (n = 62)	P value for age groups
WC	29.9% (n = 35)	37.5% (n = 18)	24.6% (n = 17)	0.135	22.1% (n = 14)	38.2% (n = 21)	0.066
Decreased HDL	23.1% (n = 27)	25.0% (n = 12)	21.7% (n = 15)	0.680	20.9% (n = 13)	25.4% (n = 14)	0.565
Increased TG or on treatment for TG levels	27.3% (n = 32)	27.0% (n = 13)	27.5% (n = 19)	0.957	25.8% (n = 16)	29.1% (n = 16)	0.691
Elevated BP or hypertension story	21.3% (n = 25)	18.7% (n = 9)	23.1% (n = 16)	0.565	14.1% (n = 10)	31.6% (n = 19)	0.016

IDF 2005 criteria, important P values (<0.005) are shown in bold.

VAI was significantly higher in the T1DM-MetS(+) group (8.21 ± 8.86) when compared with the T1DM-MetS(−) group (2.4 9 ± 1.72) (P < 0.01). The cutoff value of ROC for determining Met S was 2.65(P < 0.001, 95% CI 0.764–0.927) with AUC value 0.846 (specificity 81.8%, and sensitivity 75.7%) (Fig. 1).

FIG. 1.

ROC curve of visceral adiposity index in metabolic syndrome. ROC, receiver operating characteristic.

Cutoff point for LAP was 27.57 (ROC: 0.842, P < 0.001, sensitivity 80.0%, and specificity 74.0%). Cutoff point for TG/HDL ratio was 2.18 (ROC: 0.826, P < 0.001, sensitivity 74.3%, and specificity 74.0%) (Table 4).

Table 4.

Comparison of Visceral Adiposity Index, Lipid Accumulation Product Index, and Triglyceride/High-Density Lipoprotein Index

	Cutoff	AUC	Sensitivity (%)	Specificity (%)	P	95% CI
VAI	2.65	0.837	80.0	72.8	<0.001	0.752–0.923
TG/HDL	2.18	0.826	74.3	74.0	<0.001	0.740–0.913
LAP	27.57	0.842	80.0	74.0	<0.001	0.758–0.927

AUC, area under the curve; CI, confidence interval; LAP, lipid accumulation product index.

Discussion

In this study, the frequency of MetS in T1DM patients was found to be 32.2%, according to the IDF criteria. The ratio of MetS frequency was compatible with other recent studies.^15,16 In contrast, the MetS ratio in the age-matched control group was 8.8%. This nearly fourfold higher proportion of MetS in the T1DM group compared with healthy subjects may indicate that MetS is common in T1DM patients even at such a young average age.

In the analysis of MetS criteria, central obesity (increased WC) was the most common (33%) IDF criterion after diabetes. 31.8% of the T1DM patient group were overweight and obese. A similar ratio was also found in other studies.¹⁷ In a study of adolescent or young adult T1DM patients, a higher prevalence of overweight and/or obesity (50%) was found; central obesity was found to be more common in female patients and patients aged 35 years.¹⁸ As a possible mechanism of increased obesity, elevated leptin and high resistin have been shown in studies to promote immune destruction in pancreatic beta cells.¹⁵ Interestingly, in a Danish cohort study of 75,008 women, BMI was found to increase the risk of autoimmune disease. The associations were particularly pronounced in T1DM, with a 2.7-fold increase.¹⁶ Therefore, multiple mechanisms should account for the increased body weight in a proportion of T1DM patients.

The second more common component was hypertriglyceridemia, which was found with varying frequencies in other studies depending on the cutoff values. In the EURODIAB study, a frequency of 8% and 12% was found for female and male T1DM patients, respectively.¹⁷ In another study of 181 patients, the frequency of high TGs was 11.2%.¹⁸ The mean TG level in this study was significantly higher in T1DM with MetS.

Low HDL-c was the third most common component of MetS, lowest in the MetS(+) T1DM group, whereas we found a higher HDL-c concentration in MetS(−) T1DM patients compared with healthy controls. In another study, low HDL-c lipid abnormality was the most common lipid abnormality in inadequately controlled T1DM patients,¹⁹ and in some other studies, HDL-c levels were elevated in T1DM patients.²⁰

We found a significantly higher hypertension frequency as an IDF criterion for MetS in T1DM patients. This prevalence was highest in the MetS group. Male patients and older patients (35 years) also had a higher prevalence of hypertension. These findings were compatible with other prevalence studies.^21,22

All three indices had similar sensitivity and specificity ratios in this study. LAP index constitutes TG level and WC, and it was proposed as a marker of insulin resistance, cardiovascular risk, and visceral adipose tissue.^23,24 Also TG/HDL ratio was associated adverse cardiovascular risk, decreased insulin sensitivity, and MetS.^25,26

VAI, a formula created by Amato et al., demonstrated a significant association between visceral adipose tissue volume and superficial area.⁶ The formula VAI includes three of the MetS criteria (TG, HDL-c, and WC). It has been shown in a large cohort study to be the most outstanding discriminating factor for MetS in men and women.²⁷

In this study, VAI was significantly higher (8.21 ± 8.86) in MetS(+) T1DM group compared with MetS(−) T1DM and control group. We found that VAI >2.65 had the highest sensitivity for MetS prediction. In another study of 88 T1DM patients, the group with insulin resistance had a mean VAI score of 2.61.²⁸ In another study of diabetic patients, VAI provided a better estimate of atherosclerosis than insulin resistance.⁸ Recently, an analysis of computed tomography scans of 460 subjects found that VAI was also associated with coronary calcium score.²⁹ Therefore, measurement of VAI should be beneficial to predict cardiovascular risk in T1DM patients.

This study was cross-sectional. This was the limitation of our study. However, we studied all the criteria of MetS in T1DM patients.

Conclusions

MetS was detected in patients with T1DM with a significant proportion. VAI, LAP score, and TG/HDL ratio were highest in patients with MetS in T1DM. These three scores can be practically useful to estimate MetS and cardiovascular risk in patients with T1DM.

Footnotes

Authors' Contributions

Both authors have contributed to in all stages of the study.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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