Association of visceral fat with coronary risk factors in a population-based sample of postmenopausal women

Abstract

OBJECTIVE: To investigate in a population-based random sample of postmenopausal women the adjusted association of visceral adipose tissue (VAT) with coronary risk factors.

DESIGN: Cross-sectional population-based random sample study.

SUBJECTS: Ninety-eight postmenopausal women (age 50–65 y).

MEASUREMENTS: Visceral and subcutaneous fat areas by computer axial tomography, anthropometry, lipid profile, fasting glucose and insulin, diet, physical activity, smoking status and alcohol intake.

RESULTS: Compared to women with low VAT, women with high VAT (>117.8 cm2) had a less favorable metabolic profile with significantly higher fasting glucose (120±50 vs 98±39), insulin (7.9±10 vs 5±8), triglycerides (172±69 vs 127±72), apolipoprotein B (119±24 vs 98±32) and significantly lower HDL-C (38±10 vs 46±14) values in the whole sample (n=98). A similar profile was found in women without diabetes and hypertension (n=39). In multiple regression models, VAT explained a portion of the variance of TG (6.2%) in the entire sample and of total cholesterol (12.4%), LDL-C (15.8%), triglycerides (16.3%), apolipoprotein B (11.6%), and fasting glucose (28.4%) in the group of non-diabetic or hypertensive women. Our VAT cut-off point of 117.8 cm2 corresponded to a waist circumference of 84 cm.

CONCLUSION: Our results in a random population-based sample of postmenopausal women confirm the association of VAT with most coronary risk factors. These associations persisted after adjusting for diet, physical activity, smoking status and alcohol intake.

Introduction

Central obesity has been associated with increased risk for cardiovascular disease.1 Imaging methods such as computer tomography have found that the higher risk is primarily due to an increased accumulation of visceral adipose tissue (VAT), which has been associated with glucose tolerance impairment2 and dyslipidemia.3 Few studies have investigated the relationship between VAT and the metabolic profile in postmenopausal women. In addition, most of these studies have been made only in selected samples4,5,6,7,8 and have investigated extremely obese subjects7,8 or women with advanced age.9,10 Recently, the association of visceral fat with coronary risk factors has been questioned, because most studies have been performed in selected groups of obese subjects, without an adequate control for potential confounders.11 In this study we investigated in a population-based random sample of postmenopausal women the association of VAT, measured by computer axial tomography, with coronary risk factors. The protocol controlled variables know to affect VAT, including diet, physical activity, smoking status and alcohol intake.

Subjects and methods

A random sample of 98 participants aged 50–65 y was obtained from 17 587 women registered to the Mexican Institute of Social Security in the northeastern section of Mexico City. Women with the following diseases were excluded: hepatic cirrhosis, chronic renal failure, cancer and rheumatoid arthritis. The Scientific Investigation Committee of the Mexican Institute of Social Security approved the study protocol and all participants gave informed consent.

Subjects were recruited at their homes where the type and intensity of physical activity was assessed with Baecke's questionnaire.12 Diet was evaluated with a prospective 24-h-recall diet history. Body weight was measured to the nearest 0.1 kg and height measured to the nearest 0.1 cm. Waist circumference was measured midway between the lower rib margin and the iliac crest, and hip circumference was measured at the widest circumference over the great trochanters. Both measurements were made twice and the average was used for the analysis. Systolic (SBP; first phase) and diastolic blood pressure (DBP; fifth phase) were measured with a mercury sphygmomanometer after the patient had remained seated for at least 5 min. The average of the second and third determinations were used for the analysis. Abdominal fat was assessed with a single 10 mm scan taken at the L4–L5 disk space by computer axial tomography (CAT) on a General Electric ST Sytec 3000 Scanner as previously described by Kvist.13 An intratest variation coefficient of 1.9% was obtained when the scanner calculated adipose tissue areas twice on the same image. When a small group of these women were measured twice, the test–retest coefficient of variation was of 3.9%. Lipids and lipoproteins were determined by conventional enzymatic methods.14,15 Low-density lipoprotein cholesterol (LDL-C) concentrations were calculated by the Friedewald formula modified by DeLong.16 Our laboratory participates in the Lipid Standardization Program of the Center for Disease Control in Atlanta, GA. Plasma glucose was determined by the glucose oxidase method and fasting insulin by a double antibody ELISA method. Lipoprotein(a) (Lp(a)), apolipoprotein B (apoB) and apolipoprotein A-I (apoA-I) measurements were made by kinetic nephelometry.

Menopausal status was defined as no natural menses for at least 12 months and serum follicle-stimulating hormone (FSH) levels≥40 IU/l. Hypertension was defined by the WHO criteria DBP>90 mmHg and/or SBP>140 mmHg) or the current use of antihypertensive drugs. Diabetes mellitus was diagnosed by the criteria of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (fasting glucose>126 mg/dl).17 Women with a previous diagnosis of diabetes and that were treated with diet, oral hypoglycemic drugs and/or insulin, were also considered as diabetics. Body mass index (BMI) was calculated as weight (kg)/height (m2). General obesity was defined as BMI ≥27 kg/m2. Receiver-operator-curve (ROC) analysis was done for each coronary risk factor by identifying the relative frequency of individuals with and without the elevated risk factor for each level of VAT. Likelihood ratios for positive and negative results were calculated for each level of VAT, and specific cut-off points were identified as those with the highest likelihood ratio for positive results or with the lowest ratio for negative results.4 Depending on the studied risk factor, cut-off points ranged from 158 to 102.7 cm2. Therefore, a VAT value of 117.8 cm2 was considered the best cut-off point to identify women with an increased cardiovascular risk profile, as this was the value within the ROC calculated cut-off points, where most risk factors showed an important increase in mean values. Smoking was considered positive in women who smoked more than five cigarettes a day.18

Statistical analysis

Lp(a) and triglycerides (TG) values were logarithmically transformed for parametric analyses but their non-transformed values are shown. Mean values were compared with Student's t-test in the groups defined by the VAT cut-off point. Simple correlations were computed between VAT and other variables. Partial correlation analyses were used to assess the effect of potentially confounding variables on simple correlations. Stepwise multiple regression analysis was performed to evaluate the variance in coronary risk factors that could be explained by anthropometric and tomographic variables. Statistical significance was considered when P<0.05.

Results

The study included 98 women with a mean age of 56.7±4.3 y. Of these women, 19.4% had received hormone replacement therapy (HRT), mostly as cyclic-use of conjugated estrogens (13.3%). However, 63.2% of these women used HRT for less than a year and only four women were taking HRT at the time of the study. Hypertension and type 2 diabetes were present in 50 and 23.5% of these women, respectively. These findings are similar to those of a nationwide survey conducted by the National Health Department where hypertension was found in 46.7% and diabetes in 19.3% in subjects aged 55–59 y.19,20 Among the nine women with diabetes only, and the 14 women with diabetes and hypertension, 33 and 14.3% were treated with diet; 33 and 14.3% were taking oral agents; 0.0 and 7.09% were taking insulin; 33.3 and 28,5%, respectively, had no treatment as they did not know they were diabetic. When our sample was divided by the presence of hypertension and/or diabetes (Table 1), women who had both diseases showed the highest value of VAT (P=0.013), a tendency towards a higher waist circumference and total cholesterol–high density lipoprotein cholesterol ratio (TC/HDL-C), and significantly higher intake of fat compared to healthy women (31.7 vs 25.3%; P=0.01). There were no significant differences in physical activity among groups. We further studied the effect of VAT by comparing the metabolic and physiologic profile of women with low and high VAT. High VAT women had a less favorable metabolic profile consisting of significantly higher fasting plasma glucose (120±50 vs 98±39; P<0.05), insulin (7.9±10 vs 5±8; P<0.05), TG (172±69 vs 127±72; P<0.05), apoB (119±24 vs 98±32; P<0.05), and significantly lower HDL-C levels (38±10 vs 46±14; P<0.05), when compared to low VAT women. There were no statistical differences in physical activity or dietary variables. Correlation coefficients between VAT and variables associated to coronary risk are shown in Table 2. VAT was positively correlated with BMI, waist and hip circumference, waist–hip ratio (WHR), SBP, heart rate, TG, glucose, insulin, dietary fat, saturated fatty acid intake and negatively with leisure time physical activity. After adjusting for BMI, the correlation of VAT with apo B, TC/HDL-C and LDL-C/HDL-C ratios became significant but significance was lost with SBP, subcutaneous adipose tissue (SAT), fasting insulin and dietary variables. Adjusting for BMI and leisure time physical activity produced a non-significant association between VAT and TC/HDL-C and LDL-C/HDL-C ratios.

Table 1 Anthropometric and metabolic characteristics of a random sample of 98 population-based postmenopausal women by the presence of hypertension and/or diabetes mellitus
Table 2 Simple and partial correlations between visceral adipose tissue and anthropometric, metabolic and dietary variables in population-based postmenopausal women

Because hypertension and diabetes may modify the association of VAT and coronary risk factors, we further studied the subgroup without these two diseases; this subgroup will be referred to as healthy participants. Healthy women with increased VAT showed significantly higher mean values of TG (176±63 vs 112±81), apoB (119±24 vs 98±32), fasting glucose (120±49 vs 98±39) and fasting insulin (7.9±10 vs 5±8), when compared to women with lower VAT. Pearson's and partial correlation coefficients between VAT and coronary risk factors in these healthy women are shown in Table 3. Similar to the entire sample, VAT had a significant correlation with waist circumference, hip circumference, WHR, heart rate, total adipose tissue (TAT), VAT/SAT ratio, TG, and fasting insulin and glucose. In addition, in these healthy women, VAT did have significant correlations with TC, LDL-C and apo B. When adjusting for BMI, the correlation of VAT with leisure time physical activity became significant but the correlation with both hip circumference and fasting insulin was no longer significant.

Table 3 Simple and partial correlations between visceral adipose tissue and anthropometric, metabolic and dietary variables in population-based postmenopausal women

Multiple regression analyses were performed in the entire sample (n=98) and in healthy women (n=39) to quantify the independent contribution of anthropometric and tomographic variables to the variance of coronary risk variables. Each coronary risk factor was analysed in a model that included as independent variables BMI, waist circumference, VAT and SAT. Results indicated that VAT area explained a portion of the variance of TG in the original sample and of TC, LDL-C, TG, apoB, fasting glucose and fasting insulin in the group of healthy women (Table 4).

Table 4 Multiple regression analysis of anthropometric and tomographic variables contributing to the variance of coronary risk factors

Discussion

Current imaging methods such as CAT allow the quantification of VAT and the assessment of its participation in metabolic abnormalities. However, all studies that have evaluated VAT have been done in selected groups of subjects, and it has been questioned if these associations persist in population-based samples.11 This is the first study in which VAT has been associated with coronary risk factors in a random population-based sample of postmenopausal women. Care was taken to control for potentially confounding variables, including diet, smoking status and physical activity.

It is desirable to identify what VAT levels are associated with an increased coronary risk. A VAT cut-off point of 130 cm2 was reported both in Canadian men and premenopausal women.21,22 Using ROC analysis, Williams et al4 determined a value of 110 cm2 in white American pre- and postmenopausal women. In our postmenopausal women, 118 cm2 was the best cut-off point. Therefore, the amount of VAT, from which metabolic abnormalities associated with central obesity appear or become significant, has not shown large differences among several studies.

High levels of VAT were associated with a higher risk profile in the entire sample (n=98) of postmenopausal women. This was not unexpected, as the group with high levels of VAT had a greater percentage of diabetic (28.4 vs 8.3%, P=NS) and hypertensive (54.1 vs 41.7%, P=NS) women. The unexpected finding was the abscence of statistical differences in lipid values between healthy and diabetic women. A possible explanation could be that many healthy women had increased visceral obesity. This explanation is supported by the fact that healthy women with low VAT had significantly lower mean VAT (82±29 vs 142±19; P<0.001) and TG (111±42 vs 165±26; P=0.023) values than diabetic-only women. Healthy women with high VAT had significantly higher concentrations of TG and ApoB and non-significant higher levels of TC and LDL-C, when compared to healthy women with low VAT. This is similar to what has been noted in men23 and in premenopausal women,24 but different from older10 or more obese postmenopausal women with high VAT25 in whom TC and LDL-C have been significantly higher. However, TC and LDL-C had significant univariate and multivariate correlation with VAT in our healthy women, which persisted after adjusting for confounding variables. According to what has been found by Després and colleagues24 in premenopausal women, by Zamboni and colleagues in a heterogeneous group of pre- and postmenopausal women,25 and by DiPietro et al in older women,10 our healthy women with high VAT showed lower HDL-C values, but the difference did not reach statistical significance, probably because of the small number of subjects. Although we did not find significantly higher LDL-C levels in healthy women with high VAT, these women may still have an increased coronary risk due to significantly higher Apo B levels in the presence of normal LDL-C values, suggesting an increase in small, dense LDL particles which are considered a more atherogenic lipoproteic fraction.26 Therefore, our postmenopausal women with high VAT have lipoprotein abnormalities associated with a higher risk for coronary heart disease.

As has been reported in men23 and in premenopausal women,25 in the present study, healthy women with high VAT had significantly higher fasting insulin and glucose levels, suggesting insulin resistance.27 This finding is in agreement with a recent study by Brochu et al,8 where by using hyperinsulinemic/euglucemic clamp technique it was demonstrated that VAT is an important and independent predictor of glucose disposal in apparently healthy postmen-opausal women. Since insulin resistance has been associated with higher coronary mortality,28 these apparently healthy high VAT hyperinsulinemic women are at increased coronary risk.

It has been suggested that VAT changes in response to modifications in caloric intake29 or in physical activity30 are under genetic control. Our study did not show differences between high and low VAT women in mean dietary values. Further, significant univariate correlations between dietary variables and VAT in healthy women disappeared after adjusting for BMI. These findings support a previous cross-sectional study31 in which VAT had no association with diet. Follow-up studies are needed to evaluate if dietary composition alone can modify VAT accumulation.

The effect of daily physical activity in VAT deposits has not been assessed in population-based studies, but an inverse association between physical activity and WHR has been reported.32 In our entire sample, leisure time physical activity had a significantly inverse association with VAT. Additionally, in healthy women, when adjusting for BMI and leisure time physical activity, correlation coefficients decreased for waist circumference, and increased for LDL-C, TG and apoB. Finally, when comparing VAT mean values between sedentary and non-sedentary groups (using as a cut-off point the leisure index 50th percentile), the sedentary group had higher values of VAT than the non-sedentary group in both the entire sample (166.9±66 vs 140.33±42; P=0.023) and in healthy women (144.9±50 vs 131.57±51; P=NS). Taken together, these findings suggest that VAT is influenced by daily physical activity in women from a population-based sample. The reduction of VAT in response to physical exercise when used as an intervention,33 supports our observations.

We did not find a significant association between smoking status and VAT. However, when dividing by smoking status, there was a tendency towards lower VAT values in smokers both in the entire sample (134.6±45 vs 156.6±57; P=NS) and in healthy women (112.9±25 vs 142.4±53; P=NS). A similar tendency was found with the VAT/SAT ratio in all (0.51±0.29 vs 0.53±0.29; P=NS) and in healthy women (0.41±0.13 vs 0.56±0.35; P=NS). Additionally, BMI and hip circumference had statistically lower mean values in smokers. These results are in agreement with the finding that female smokers had decreased abdominal obesity evaluated by waist circumference and densitometry.34 Since only one woman smoked more than 20 cigarettes per day, statistical differences in VAT values may perhaps be found in groups with an increased amount of cigarettes smoked per day.

A number of studies have found that waist circumference is the best anthropometric predictor of VAT, with correlation coefficients greater that 0.70.21 In our study, the correlation between VAT and waist circumference was 0.73. In the Canadian population, a VAT area of 130 cm2 corresponded to a waist circumference of 100 cm in 40-y-old premenopausal women.22 In our study of older, postmenopausal women, the cut-off point of 118 cm2 of VAT corresponded to a waist circumference of 84 cm. This supports the notion that VAT increases in a greater proportion than SAT with advancing age. Based on this, Després has proposed a cut-off point in waist circumference of only 90 cm in both men and women between 40 and 60 y of age.22

In summary, our results in a random population-based sample of postmenopausal women confirm the association of VAT with most coronary risk factors. These associations persisted after adjusting for potentially confounding variables including diet, physical activity and smoking status. Women with hypertension and diabetes showed higher VAT values and, as expected, greater metabolic abnormalities. A waist circumference greater than 84 cm corresponded to a VAT value associated to metabolic abnormalities. Since this anthropometric measurement can be useful in clinical and epidemiological settings to identify high-risk subjects, similar studies in different ethnic groups are warranted to identify their own cut-off points.

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Correspondence to C Posadas-Romero.

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Hernández-Ono, A., Monter-Carreola, G., Zamora-González, J. et al. Association of visceral fat with coronary risk factors in a population-based sample of postmenopausal women. Int J Obes 26, 33–39 (2002). https://doi.org/10.1038/sj.ijo.0801842

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Keywords

  • visceral fat
  • computed tomography
  • menopause
  • coronary heart disease
  • physical activity

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