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Diabetes Care 28:409-415, 2005
© 2005 by the American Diabetes Association, Inc.

Metabolic Syndrome/Insulin Resistance Syndrome/Pre-Diabetes
Original Article

Household Income Is Associated With the Risk of Metabolic Syndrome in a Sex-Specific Manner

Jean Dallongeville, MD, PHD1, Dominique Cottel, MD1, Jean Ferrières, MD, PHD2, Dominique Arveiler, MD, PHD3, Annie Bingham, MSC4, Jean Bernard Ruidavets, MD, PHD2, Bernadette Haas, MD3, Pierre Ducimetière, PHD4 and Philippe Amouyel, MD, PHD1,5

1 Institut Pasteur de Lille, Institut National de la Santé et de la Recherche Médicale, Lille, France
2 Faculté de Médecine Purpan, Institut National de la Santé et de la Recherche Médicale, Toulouse, France
3 Laboratoire d’Epidémiologie et de Santé Publique, Strasbourg, France
4 Hôpital Paul Brousse, Institut National de la Santé et de la Recherche Médicale, Villejuif, France
5 Faculté de Médecine, Université Lille II, Lille, France

Address correspondence and reprint requests to Dr. Jean Dallongeville, Institut National de la Santé et de la Recherche Médicale U 508, Institut Pasteur de Lille, 1 rue du Pr Calmette, 59019 Lille Cedex, France. E-mail: jean.dallongeville{at}pasteur-lille.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
OBJECTIVE—To assess the relationship between household income and metabolic syndrome in men and women.

RESEARCH DESIGN AND METHODS—A total of 1,695 men and 1,664 women, aged 35–64 years, from three distinct geographical areas of France were investigated. Waist girth, plasma triglycerides, HDL cholesterol, glucose, and systolic blood pressure were used to define metabolic syndrome according to the National Cholesterol Education Program (NCEP)/Adult Treatment Panel III (ATPIII) guidelines. Household income, educational level, occupational category, working status, consumption of psychotropic drugs, accommodation status, household composition, physical activity at work and during leisure time, alcohol consumption, and smoking habits were recorded with a standardized questionnaire.

RESULTS—There were 390 (23.0%) men and 381 (16.9%) women who satisfied NCEP/ATPIII criteria for metabolic syndrome. Household income (P < 0.0001) and consumption of psychotropic drugs (P = 0.0005) were associated with metabolic syndrome in women but not in men. In contrast, educational level, occupational category, working status, and accommodation status were associated with metabolic syndrome in both men and women. After adjustment on lifestyle variables, household income (interaction P < 0.004) remained inversely associated with metabolic syndrome in women but not in men.

CONCLUSIONS—These data suggest that limited household income, which reflects a complex unfavorable social and economic environment, may increase the risk of metabolic syndrome in a sex-specific manner.

Abbreviations: ATPIII, Adult Treatment Panel III • Monitoring Trends and Determinants in Cardiovascular Disease • NCEP III, National Cholesterol Education Program III


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
The metabolic syndrome is characterized by the clustering of several metabolic disorders (1,2). The latter are influenced by nutritional habits and physical activity (3–6). Several working definitions have been proposed for metabolic syndrome (7), including increased body weight, insulin resistance, elevated plasma triglyceride levels, low HDL cholesterol, high blood pressure, and altered glucose homeostasis. These factors independently and in combination increase the risk of cardiovascular disease and diabetes (8–11).

In the U.S., the prevalence of metabolic syndrome has been estimated to be 22.8 and 22.6% in men and women, respectively (12). The distribution of the syndrome varies among different categories of the population. Increasing evidence (13–21) indicates that social indicators and psychological factors are strongly associated with the risk of insulin resistance, hypertriglyceridemia, hypertension, obesity, and metabolic syndrome. People from the lowest social categories are more likely to develop several metabolic disorders or metabolic syndrome. The mechanisms involved in these associations are not totally elucidated. Social factors, educational level, and economic indicators are strongly interrelated. These factors influence nutritional habits, physical activity, and healthy behaviors possibly affecting the clustering of metabolic disorders (22,23).

Very little is known about the influence of household income on the risk of metabolic syndrome. The reason is the limited number of studies that recorded information on this indicator. Earlier studies (24–26) have reported an inverse relationship between household income and obesity that is compatible with a higher risk of metabolic syndrome in people with limited economic resources. In the present study, we hypothesized that household income might influence the risk of metabolic syndrome. Therefore, we investigated the relationship between household income and metabolic syndrome in a large sample of men and women in which social indicators and lifestyle variables were recorded.


   RESEARCH DESIGN AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
RESULTS
 CONCLUSIONS
 References
 
Participants were recruited in the framework of the World Health Organization Monitoring Trends and Determinants in Cardiovascular Disease (MONICA) population survey conducted from 1995 to 1997 in three distinct geographical areas in France: the urban community of Lille in the north, the district of Bas-Rhin in the east, and the district of Haute-Garonne in the south of France. The sample included representative subjects aged 35–64 years, stratified by town size, randomly selected from the electoral rolls to obtain 200 participants for each sex and 10-year age-group (World Health Organization MONICA project protocol [27]). A total of 1,778 men and 1,730 women completed the recruitment procedure. The local ethical committee approved the protocol.

After signing an informed consent, participants were administered a standard questionnaire, and physical measurements were made by a specially trained nurse. The questionnaire covered questions on socioeconomic factors, physical activity at work and during leisure activities, alcohol consumption, smoking status, personal medical history, family history, attitudes and knowledge concerning several diseases, and current drug therapy.

The level of physical activity during leisure time was self-reported as no physical activity, light (light physical activity almost every week), and intense (at least 20 min more than once a week). Physical activity at work was divided into four groups: sedentary, regular walking and handling of <10-kg parcels (light), handling of 10- to 24-kg parcels (average), and handling of >25-kg loads (heavy). Current cigarette smokers were defined as subjects reporting at least one cigarette per day. Total alcohol intake was expressed as the sum of milliliters of alcohol per week from wine, beer, cider, and spirits. Household income was estimated by family income tax classified in four categories: no income tax, <760 euros, 760–2,300 euros, and >2,300 euros. These cut points approximately corresponded to the tertile of family income in France at the time of the study. The educational level was assessed by counting the number of years of schooling and classified in three categories: primary, secondary or technical, and university. Occupational categories were classified according the French National Institute of Statistics and Economic Studies in five categories: unskilled manual workers, company clerks, middle executives, and senior executives. Working status included retired and no professional activity, working full or part time, disability, and unemployed. Psychotropic drug consumption included tranquillizer, antidepressant, and hypnotic. The number of people living in the household was assessed. Accommodation status was either owner or living in a rented accommodation.

The anthropometric measurements included body weight (rounded to the nearest even decimal), waist girth (at a level midway between lower rib margin and iliac crest; to the nearest 0.5 cm), and height (to the nearest centimeter) and were taken on subjects in light clothing without shoes. BMI was calculated according to the Quetelet equation. Blood pressure was measured on the right arm, with the subject in a sitting position and after a minimum 5-min rest, using a standard mercury sphygmomanometer. Two consecutive measures of systolic and diastolic blood pressure were recorded to the nearest 2 mmHg. The second blood pressure record was taken at least 1 min after the first one. The mean value of the two blood pressure readings was taken into account.

Metabolic syndrome was defined, according to the National Cholesterol Education Program (NCEP)/Adult Treatment Panel III (ATPIII) recommendations (28), by the presence of at least three or more of the following abnormalities: waist girth >102 cm in men and >88 cm in women, triglycerides ≥150 mg/dl, HDL cholesterol <40 mg/dl in men and <50 mg/dl in women, blood pressure ≥130/85 mmHg or treatment with blood pressure–lowering medications, and fasting glucose ≥110 mg/dl or treatment for diabetes. Eighty-two subjects with triglycerides <150 mg/dl could not be classified because of fibrate treatment. These subjects were excluded from the analyses.

After the subjects had fasted for at least 10 h, a 20-ml blood sample was drawn on disodium EDTA, kept at room temperature, and centrifuged within 4 h. Lipid and lipoprotein levels were measured centrally at the Purpan Hospital Biochemical Laboratory (Toulouse, France). The quality of biological measurements was assessed within the framework of the MONICA project. Glucose was measured by the glucose oxidase method (DuPont Dimension). Plasma insulin was measured by radioimmunoassay (BiInsuline; Eria Pasteur). Serum triglyceride and HDL cholesterol levels were measured enzymatically (DuPont Dimension).

Statistical analyses
Statistical analyses were performed with the SAS System for Windows (SAS Institute, Cary, NC). The general linear model procedure and logistic regression analyses were used to compare continuous and categorical variables, respectively. Logistic regression analyses was used to assess the association between household income and metabolic syndrome using age and center as covariables. To compare the association in men and women, an interaction term for sex and the social variable of interest, separately, was fitted to the model together with age, center, physical activity, alcohol consumption, smoking habits, and household composition. The Wald statistic was used to test the statistical significance of the interaction term.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
CONCLUSIONS
 References
 
At total of 23% of men and 16.9% of women, aged 35–64 years, satisfied NCEP/ATPIII criteria for metabolic syndrome (Table 1). The prevalence increased across age categories and was lower in southern France (Toulouse) than in the east (Strasbourg) or the north (Lille). Physical activity during leisure time was inversely associated with metabolic syndrome in both sexes (P < 0.0001). Physical activity at work was positively correlated with metabolic syndrome in women (P < 0.0002) but not in men. Smoking and alcohol consumption were associated with metabolic syndrome in men (P < 0.011, P < 0.0003, respectively) and women (P < 0.0001, P < 0.04, respectively). BMI, waist circumference, insulin, glucose, triglycerides, and blood pressure were higher, and HDL cholesterol was lower in both men and women (all variables P < 0.0001) with metabolic syndrome than in control subjects (Table 1).


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  		Table 1— Characteristics of the subjects with metabolic syndrome and control subjects according to sex

 
The household income was inversely associated with metabolic syndrome in women (P < 0.0001) but not in men (Table 2). Educational level was inversely associated with metabolic syndrome in both men and women (both P < 0.0001). Similarly, the mean duration of schooling was lower in men and women with metabolic syndrome than in control subjects (P < 0.0001). Both men (P < 0.0005) and women (P < 0.0012) living in rented accommodations were more likely to be affected by metabolic syndrome than owners. Occupational category was associated with metabolic syndrome in both sexes (P = 0.0003 in men and P < 0.0001 in women). Unskilled manual workers were more likely to present a metabolic syndrome than control subjects. Consumption of psychotropic drugs was associated with metabolic syndrome in women (P < 0.0005) but not in men. Number of individuals in the household was inversely associated with metabolic syndrome in men (P < 0.03) but not in women. Finally, working status was associated to metabolic syndrome in men (P = 0.0003) and women (P < 0.0001). There were less active workers among the metabolic syndrome group than in the control group (Table 2).


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  		Table 2— Household income, education, social status and psychotropic drug use distribution in subjects with metabolic syndrome and control subjects according to sex

 
To compare the impact of economic and social factors on metabolic syndrome in men and women, logistic regression analyses were performed with an interaction term for sex and the variable of interest, adjusting for age, center, physical activity, alcohol consumption, smoking habits, and household composition (Table 3). Household income remained inversely associated with metabolic syndrome in women (trend P < 0.0001) but not in men (trend P < 0.12, interaction between sex and household income P = 0.0004). Educational level was inversely associated with metabolic syndrome in men (trend P < 0.0003) and women (trend P < 0.0001, interaction P < 0.011). Accommodation status was associated with metabolic syndrome in men (trend P < 0.0023) and women (trend P < 0.0045, interaction was nonsignificant P = 0.89). Occupational category was associated with metabolic syndrome in men (trend P < 0.0071) and women (trend P < 0.0004, interaction P = 0.056). Psychotropic drug use was associated with metabolic syndrome in women (trend P < 0.0009) but not in men (trend P < 0.22, interaction P = 0.18).


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  		Table 3— Age- and center-adjusted odds ratios of metabolic syndrome for household income, educational level, and accommodation status by sex

 
To gain further insight to the relationship between household income and metabolic syndrome, logistic regression analyses were performed with household income and each metabolic disorder separately, adjusting for age, center, physical activity, alcohol consumption, smoking habits, and household composition (Fig. 1). In women, household income was inversely associated with increased waist girth (P < 0.001), HDL levels (P < 0.04), blood pressure (P < 0.01), and glycemia (P < 0.02). In men, there was no evidence for significant associations between household income and any of the metabolic disorders separately.



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  		Figure 1— Adjusted odds ratio of metabolic disorders for a 1-unit increase in household income in men and women. Metabolic disorders were defined according to the NCEP III definition. Logistic regression analyses was used to assess the odds ratio of metabolic disorders using age, center, physical activity, alcohol consumption, smoking habits, and household composition as covariables.

 

   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
References
 
The principal finding of the present study is that household income is inversely associated with the risk of metabolic syndrome in women. After adjustment on lifestyle factors, the relationship remained statistically significant. These data suggest that limited household income, which reflects a complex unfavorable social and economic environment, may increase the risk of metabolic syndrome in a sex-specific manner.

The observation of an inverse association between metabolic syndrome and household income in women, but not in men, suggests that economic constraints may increase the risk of metabolic syndrome in women. These data are consistent with previous reports (24–26) that had shown stronger association between household income and waist girth in women than in men. Our study further extends this observation to metabolic syndrome. One possible explanation to this finding is that limited resources bring people to choose low-cost, energy-dense food, which favors the development of insulin resistance, hypertriglyceridemia, and body weight gain (23). In support of this hypothesis, it has been shown that foods composed of fat, refined grain, and added sugar are the lowest-cost options for consumers in France (29). Limited resources may also affect the ability to practice leisure activity, resulting in a higher risk of metabolic syndrome. However, these hypotheses do not clearly explain the sex difference, since both men and women from the lower household income category should be similarly affected by inappropriate food choice and lack of leisure activity. Therefore, another explanation could be that women in the lowest household income category are likely unemployed and bothered by limited resources, resulting in reduced physical activity and/or increased stress. This in turn may favor body weight gain and insulin resistance (25). In agreement with this hypothesis, women in the bottom income group were more often unemployed and consume more psychotropic drugs than women in the upper household income category.

In contrast with women, household income was not associated with metabolic syndrome or any of its components separately in men. Interestingly, the prevalence of metabolic syndrome tended to be higher in men from the upper than the lower income category, whereas the opposite was observed in women. Therefore, one explanation could be that men from the top income category, because of cultural and personal beliefs, care less for healthy food choices and physical activity than women from the same income range. Furthermore, men in the bottom income group have a more physical occupation that might protect them from developing metabolic syndrome. Altogether, household income is a social and economic indicator associated with health behaviors that result in a higher risk of metabolic syndrome in women.

Educational level is an important cofactor of the relationship between household income and metabolic syndrome. In the present study, the level of education was inversely related to metabolic syndrome in both men and women; however, it was more strongly inversely related in women than in men (interaction P < 0.011). This is consistent with previous studies (16–20) that reported more pronounced inverse associations between educational level and features of metabolic syndrome in women than in men. The reasons for this association might be related to the influence of education in predicting food choices (22,30–33) and healthy behaviors (30,34), both of which are related to metabolic syndrome. Since education facilitates the understanding and acquisition of healthy lifestyles and since women are generally more health conscious than men, the combination of both factors might explain the greater protection against metabolic syndrome in educated women.

Housing status is an indicator of social position that is linked to household income. In this study, living in a rented accommodation is associated with metabolic syndrome in men and women. The mechanism through which housing status influences metabolic syndrome is speculative. Living in a rented accommodation might reflect a lower social position, which might generate chronic stress resulting in insulin resistance and hypertriglyceridemia (35–37). Consistent with this hypothesis, previous works (17,18) have reported that the risk of insulin resistance and obesity is related to the neighborhood characteristics and accommodation status. Therefore, accommodation status might aggregate several indicators of social position that influence the risk of metabolic syndrome.

This study has several strengths and limitations. It was conducted in three representative samples of men and women from different regions of France, therefore providing a large variety of social and economical situations. However, indicators of social position, wealth, and educational level are highly interrelated, which makes it difficult to determine the precise individual contribution of each factor. Furthermore, due to the strong interrelations among social indicators, there is always a possibility that unmeasured factors may confound the observations. Another study limitation is the cross-sectional nature of the study, which does not allow inferring a causal relationship. Moreover, reverse causation, the extent of which metabolic syndrome and poor health lead to low income, could be of some concern. In addition, we used family income tax as a proxy of household income despite well-identified conceptual difficulties.

In conclusion, household income is a social and economic indicator that aggregates several indicators of social position. In the present study, household income is inversely associated with metabolic syndrome in women. These data suggest that low social position, reflected by limited familial income, may increase the risk of metabolic syndrome in a sex-specific manner.


   Acknowledgments
 
The World Health Organization MONICA population survey developed in the north of France was supported by unrestricted grants from the Conseil Régional du Nord-Pas de Calais, the Office National de Interprofessionnel des Vins, Parke-Davies Laboratory, the Mutuelle Générale de l’Education Nationale (MGEN), Groupe Fournier, the Réseau National de Santé Publique, the Direction Générale de la Santé, the Institut National de la Santé et de la Recherche Médicale (INSERM), and the Institut Pasteur de Lille and the Unité d’Evaluation du Centre Hospitalier et Universitaire de Lille.


   Footnotes
 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

Received for publication June 29, 2004. Accepted for publication November 3, 2004.


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 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 

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 Am. J. Physiol. Endocrinol. Metab.Home page
P. Darmon, F. Dadoun, S. Boullu-Ciocca, M. Grino, M.-C. Alessi, and A. Dutour
Insulin resistance induced by hydrocortisone is increased in patients with abdominal obesity
Am J Physiol Endocrinol Metab, November 1, 2006; 291(5): E995 - E1002.
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J. Dallongeville, M.-C. Grupposo, D. Cottel, J. Ferrieres, D. Arveiler, A. Bingham, J.-B. Ruidavets, B. Haas, P. Ducimetiere, and P. Amouyel
Association between the metabolic syndrome and parental history of premature cardiovascular disease
Eur. Heart J., March 2, 2006; 27(6): 722 - 728.
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