Metabolic syndrome (MetS) is a clustering of abdominal obesity, atherogenic dyslipidaemia, hypertension, insulin resistance and disturbed glucose metabolism that identifies individuals at increased risk for type 2 diabetes and progression of CVD(Reference Grundy, Cleeman and Daniels1). MetS has become a global health problem and a substantial economic burden in both developing and developed countries(Reference Steinberger, Daniels and Eckel2, Reference Gu, Reynolds and Wu3). Over the past two decades, Tunisia, a developing country in the Eastern Mediterranean Region, has undergone a sharp socio-economic and demographic transition. Rapid changes in urbanization and socio-economic circumstances, related to the nutrition transition, are contributing to major epidemiological changes with the emergence of chronic diseases like obesity, diabetes, hypertension, CVD and other disorders(Reference Popkin4–Reference Ntandou, Delisle and Agueh6). The Tunisian epidemiological transition has been compounded by powerful environmental and behavioural changes. In particular, the adoption of new dietary habits and sedentary lifestyles, and the stress of urbanization and of working conditions, all may lead to increased prevalence of MetS and its risk factors(Reference Ben Romdhane, Habib and Ali7). Although modification of lifestyle-associated risk factors is known to be essential for preventing and managing MetS, there is currently insufficient information available on the prevalence of MetS and associated factors in North Africa and especially in Tunisia. In the Tunisian population, few studies on MetS have been conducted(Reference Harzallah, Alberti and Ben Khalifa8–Reference Allal-Elasmi, Haj Taieb and Hsairi10). In addition, there is only one study conducted in the population of Greater Tunis which has investigated the implication of socio-economic status (SES) as assessed by education level in the prevalence of MetS(Reference Allal-Elasmi, Haj Taieb and Hsairi10). An inverse relationship was found between education level and MetS only in women; however, this association is possibly confounded by factors other than age, which are strongly related to MetS. The present study was conducted in a nationally representative population to estimate the prevalence of MetS and its components among Tunisian adults and to evaluate the association of this syndrome with cardiovascular risk factors, demographic and socio-economic variables.
Materials and methods
Sampling
A large, nationally representative survey was conducted in the entire population of Tunisia. This survey was integrated into a collaborative project funded by the European Commission to study epidemiological Transition and Health Impact in North Africa (TAHINA). The survey was cross-sectional from April 2004 to September 2005 and the target population was adult men and women between the ages of 35 and 74 years. A nationally representative, stratified, two-tier cluster sample of households was selected according to the seven administrative regions of Tunisia. The sampling frame was derived by the Tunisian National Institute of Statistics from the database of the 2004 census of the population; in each stratum forty-seven census districts were selected, with a probability proportional to size in number of eligible households (i.e. featuring at least one 35–74-year-old household resident). At the second stage, twenty-five eligible households were sampled in each district; then for each household, all household residents from the targeted age range were to be included during the implementation of the field survey. The overall response rate was 79·5 %, rates were generally lower in urban than in rural areas and in men than in women. The study protocol was carried out according to the Declaration of Helsinki and has been ethically approved by the Tunisian Ministry of Health and the Tunisian National Council of Statistics (visa n°5/2005). All participants gave their free informed consent, after being thoroughly informed of the purpose, requirements and procedures of the survey.
A total of 8007 people were enrolled. Of these, 3353 individuals who either had missing anthropometric measurements or did not fast properly prior to the blood test were excluded. The remaining 4654 participants (1840 men and 2814 women) constituted the sample used. The mean age of the 4654 individuals (50·2 years for men, 50·3 years for women) was similar to that of the initial 8007 individuals recruited for the survey (49·6 years for men, 49·5 years for women). Excluded men had a higher prevalence of rural residents compared with included men (P < 0·05). Excluded men had also a greater proportion of lower education levels (P < 0·05). With respect to women, comparison between excluded and included groups showed no significant differences.
Data collection
Demographic and socio-economic information, smoking, menopausal status and taking of relevant medications (especially antidiabetic agents, antihypertensive agents and hormone replacement therapy) were obtained with a structured questionnaire pre-tested on a small group of non-participants. A family history of CVD was defined as having at least one parent or sibling diagnosed with diabetes, hypertension, stroke or CHD.
SES was assessed using the following measures obtained from the questionnaire: education level and occupation. Education was classified into four categories: level 0, illiterate; level 1, low-level education (≤6 years of schooling); level 2, intermediate-level education (7–13 years of schooling); and level 3, higher education (≥14 years of schooling). Occupation was classified into four categories: not working/retired; employee/ worker; intermediate grade (civil servants with >6 years of education); and upper grade (university graduates). Marital status was categorized as single, married, widowed or divorced. Concerning smoking status, a smoker was defined as a person who smoked any number of cigarettes regularly or who had any history of smoking in the past. A never smoker was defined as someone who had never smoked.
Measurements
Anthropometric measurements including weight and height were taken with the participant barefoot and wearing light clothing. Waist circumference (WC) was measured in the erect position at the middle between the tenth rib and the iliac crest. BMI (kg/m2) was calculated as the weight (in kilograms) divided by the square of the height (in metres). Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were measured twice by a mercury sphygmomanometer in the sitting position after the participant had been quietly seated for more than 15 min. The mean of the two measurements was used in the analyses. Blood samples were collected after a 12 h overnight fast. Fasting blood glucose (FBG) was determined by the glucose oxidase enzymatic method. Serum TAG was measured enzymatically after hydrolysis of glycerol and total cholesterol (TC) was measured by the cholesterol oxidase enzymatic method. All biochemical analyses were done using a Beckman reagent kit on a Beckman SYNCHRON CX7 analyser (Beckman Instruments, Inc., Fullerton, CA, USA).
Definition of the metabolic syndrome
According to the National Cholesterol Education Program, Adult Treatment Panel III (NCEP-ATPIII), MetS is defined as the presence of three or more of the following criteria: (i) WC ≥ 102 cm in men or ≥88 cm in women; (ii) TAG ≥ 1·7 mmol/l; (iii) HDL cholesterol (HDL-C)<1·03 mmol/l in men or <1·29 mmol/l in women; (iv) SBP ≥ 130 mmHg and/or DBP ≥ 85 mmHg; and (v) FBG ≥ 6·1 mmol/l(11). In the present study HDL-C was not determined because at the time of the survey the method used was the precipitation method, which is known for its large variability, and serum was not kept to measure it. We used TC instead of HDL-C as previously reported(Reference Bouguerra, Ben Salem and Alberti9, Reference Rguibi and Belahsen12, Reference Fezeu, Balkau and Kengne13). The cut-off point used was TC ≥ 5·2 mmol/l in men and women. Participants who reported taking hypertension or diabetes medications were considered to have elevated blood pressure (BP) or high FBG, respectively.
Statistical analysis
All statistical analyses were conducted using the SPSS statistical software package version 15·0 (SPSS Inc.). Continuous variables are presented as means and standard deviations, and categorical variables are presented as absolute and relative frequencies. Differences in baseline characteristics between groups were assessed using the independent t test or the χ 2 test, as appropriate. We describe the data stratified by gender because there was an interaction between gender and socio-economic factors in the association with MetS and in order to reduce the bias between the genders caused by the variation in response rate. We calculated the odds ratios together with their 95 % approximate confidence intervals as estimators of the relative risk of MetS and its components for demographic characteristics and SES indicators of the study population. Univariate logistic regression analyses were used to determine crude odds ratios. To study the association of SES indicators and other factors with the prevalence of the MetS, we performed a multivariate logistic regression model with MetS as the dependent variable and with age, residence area, marital status, smoking, family history of CVD, education and occupation as the independent variables. The sampling design, i.e. stratification, clustering and sampling weights (accounting for differential probabilities of selection and also a post-stratification on gender, age and urban v. rural), was taken into account in all estimates and analyses using the specific SVY series of Stata commands. We added menopausal status to the model when analyses were done for women. The significance threshold was set at P < 0·05.
Results
The basic characteristics of the study population, stratified by gender, are listed in Table 1. The overall prevalence of MetS was 30·0 %, and was significantly higher in women than in men (36·1 % v. 20·6 %, P < 0·0 0 1). High WC, high BP and high TC were significantly more prevalent in women than in men (P < 0·001, P < 0·05 and P < 0·001, respectively), while high FBG and high TAG were more prevalent in men (P < 0·05 for both; Table 2). The prevalence of MetS increased with age for both men and women (P < 0·001 for both), but the increase with age was more important in women. In the age group 35–44 years, 14·6 % of men and 20·7 % of women had MetS. In those over 64 years of age, the prevalence was 24·1 % and 51·5 % for men and women, respectively (Fig. 1).
Baseline characteristics of the study participants and by gender: representative sample of Tunisian adults aged 35–74 years, Transition and Health Impact in North Africa (TAHINA) project, 2004–2005
WC, waist circumference.
Continuous variables are presented as means and standard deviations and were compared by the t test. Categorical variables are presented as absolute and relative frequencies and were compared by the χ 2 test.
Prevalence of MetS and its components among the study participants and by gender: representative sample of Tunisian adults aged 35–74 years, Transition and Health Impact in North Africa (TAHINA) project, 2004–2005
MetS, metabolic syndrome; WC, waist circumference; BP, blood pressure; FBG, fasting blood glucose; TC, total cholesterol; NCEP-ATPIII, National Cholesterol Education Program, Adult Treatment Panel III.
Values were significantly different from those in men: *P < 0·05, ***P < 0·001.
Prevalence of metabolic syndrome (MetS) stratified by age group and gender (—⧫—, men, n 1840; —▪—, women, n 2814): representative sample of Tunisian adults aged 35–74 years, Transition and Health Impact in North Africa (TAHINA) project, 2004–2005. MetS prevalence increased significantly with age for both genders: P < 0·001
The OR for MetS and its components according to demographic and socio-economic indicators are shown in Tables 3 and 4 for men and women, respectively. In men, the odds for high WC (OR = 1·31; P < 0·05), high FBG (OR = 1·85; P < 0·0 0 1), high TC (OR = 1·52; P < 0·05) and high TAG (OR = 1·26; P < 0·05) were significantly higher in urban residents. Urban area was significantly associated with a higher odds for MetS, even after adjusting for covariates (OR = 1·51; P < 0·05). Higher levels of education were significantly associated with higher odds for high WC (P < 0·05 for low, intermediate and higher v. illiterate), high TC (P < 0·05 for intermediate and higher v. illiterate) and high TAG (P < 0·05 for low, intermediate and higher v. illiterate) and with lower odds for high BP (P < 0·05 for low and intermediate v. illiterate). The odds for MetS increased linearly as education level increased, and this result was unchanged in multiple logistic regression analysis. Men with a family history of CVD showed higher odds for high WC (P < 0·05), high BP (P < 0·05) and high FBG (P < 0·001). The odds for MetS was significantly higher in men with a family history of CVD before and after adjusting for confounding variables (P < 0·05 for both). The odds increased for high TC (P < 0·05) and high TAG (P < 0·001) and decreased for high WC (P < 0·05) and high BP (P < 0·05) in smokers compared with non-smokers. There was no significant effect of smoking, marital status and occupation on the risk of the MetS in univariate and multivariate logistic regression analyses (Table 3).
The odds for MetS and its components according to demographic and socio-economic indicators in men: representative sample of Tunisian adults aged 35–74 years, Transition and Health Impact in North Africa (TAHINA) project, 2004–2005
MetS, metabolic syndrome; WC, waist circumference; BP, blood pressure; FBG, fasting blood glucose; TC, total cholesterol.
Odds ratios were significant compared with the referent category: *P < 0·05, ***P < 0·001.
†Univariate logistic regression.
‡Multivariate logistic regression analysis including MetS as the dependent variable and age, residence area, marital status, smoking, family history of CVD, educational level and occupation as independent variables.
§Referent category.
The odds for MetS and its components according to demographic and socio-economic indicators in women: representative sample of Tunisian adults aged 35–74 years, Transition and Health Impact in North Africa (TAHINA) project, 2004–2005
MetS, metabolic syndrome; WC, waist circumference; BP, blood pressure; FBG, fasting blood glucose; TC, total cholesterol.
Odds ratios were significant compared with the referent category: *P < 0·05, ***P < 0·001.
†Univariate logistic regression.
‡Multivariate logistic regression analysis including MetS as the dependent variable and age, residence area, marital status, smoking, family history of CVD, educational level and occupation as independent variables.
§Referent category.
In women, urban residents showed higher odds for high WC (OR = 2·06; P < 0·001), high FBG (OR = 2·04; P < 0·001) and high TC (OR = 1·14; P < 0·001). The OR for MetS was significantly higher in urban residents before and after adjusting for risk factors (P < 0·001 for both). Postmenopausal women had higher odds for high WC (OR = 1·26; P < 0·05), high BP (OR = 3·25; P < 0·001), high FBG (OR = 2·51; P < 0·001) and high TC (OR = 1·88; P < 0·001) compared with premenopausal women. Postmenopausal stage was significantly associated with higher odds for MetS, even in the multivariate model (OR = 1·46; P < 0·05). The OR for high BP decreased linearly as the education level increased (P < 0·001 for low, intermediate and higher v. illiterate). In contrast to what was found in men, in women the odds for MetS decreased significantly as the education level increased (P < 0·05 for intermediate and higher v. illiterate), but this significance disappeared in the multivariate model. Women with family history of CVD showed higher odds for high WC (P < 0·05), high BP (P < 0·05), high FBG (P < 0·001) and high TC (P < 0·05). The OR for MetS was higher in those with a family history of CVD (P < 0·05), which was no longer significant after adjustment for covariates. Univariate and multiple logistic regression analyses showed no significant effect of smoking, marital status and occupation on the risk of MetS (Table 4).
Discussion
MetS is considered a problem of global proportions, affecting both developed and underdeveloped countries in a rapidly progressive way(Reference Gu, Reynolds and Wu3, Reference Ford14–Reference Oh, Hong and Sung17). The prevalence in different countries, nevertheless, varies considerably. Such contrast is due to many factors. The most obvious is that different diagnostic criteria lead to different results, especially in specific subgroups(Reference Alberti, Zimmet and Shaw18–Reference Cheung, Ong and Man20). Our data were based on the NCEP-ATPIII criteria, one of the most widely used in medical practice. In the present study, conducted in a large nationally representative sample of adults, 30·0 % of the studied individuals had MetS. The prevalence of MetS was significantly higher in women (36·1 %) than in men (20·6 %). The MetS prevalence estimated in the current study is similar to that reported in a previous study carried out in a population of Greater Tunis, located in the north of Tunisia(Reference Allal-Elasmi, Haj Taieb and Hsairi10). Several studies have reported an increased rate of MetS in women compared with men(Reference Harzallah, Alberti and Ben Khalifa8, Reference Allal-Elasmi, Haj Taieb and Hsairi10, Reference Velásquez-Meléndez, Gazzinelli and Côrrea-Oliveira21, Reference Jaber, Brown and Hammad22). In the present study the higher MetS prevalence in women could be explained by the fact that central obesity was three times more frequent in women than in men (65·5 % v. 20·6 %, respectively). Central obesity has been shown to be an important predictor of CVD and diabetes(Reference Yusuf, Hawken and Ounpuu23, Reference Wang, Rimm and Stampfer24). The large WC in women may be explained by hormonal factors, postmenopausal weight gain and the general lack of participation in physical and sports activities among adult Tunisian women(Reference Ghannem25). It has been suggested that multiple pregnancies may increase the risk of developing central obesity, insulin resistance and hypertension(Reference Lasky, Becerra and Boto26, Reference Catalano27), all components of MetS. We also found that age was an important factor in determining higher prevalence of MetS for both men and women, but the effect of age on MetS risk was more important in women. Similar results have been reported in many studies in other populations(Reference Miccoli, Bianchi and Odoguardi16, Reference Park, Oh and Cho28).
With regard to the area of residence, urban area was independently associated with increased risk of MetS in both men and women. For both genders, urban residents showed higher OR for central obesity, diabetes and dyslipidaemia. Previous studies have documented higher MetS prevalence in the urban v. rural population(Reference Weng, Liu and Ma29–Reference Ntandou, Delisle and Agueh31). Furthermore, these studies showed that rural dwellers had higher diet quality and physical activity than their urban counterparts. Urbanization often is associated with increased income and adoption of an unhealthy lifestyle, such as unhealthy food habits, with the transition from traditional rural diets (with a low glycaemic index and a higher fibre content) to a diet rich in salt, saturated fats and poor-quality carbohydrates (such as provided by fast foods)(Reference Mittal and Singh32). Furthermore, increased psychological stress, which is inevitable with urbanization, may be related to the development of MetS(Reference Tamashiro33).
In the present study we failed to detect an association between smoking and MetS, a result similar to that found in a Brazilian cohort(Reference da Silveira, Horta and Gigante34) but contrary to what has been reported in other studies(Reference Lee, Jung and Park35, Reference Steemburgo, Dall'Alba and Grosss36). We also studied the effect of family history of CVD on MetS. Results revealed that the risk of acquiring MetS was two- or threefold higher in men and women with a family history of CVD. After controlling for confounding factors, the result remained significant only for men. A positive family history of CVD has been reported to affect BP and serum glucose level(Reference Válek and Vlasáková37, Reference Hunt, Heiss and Sholinsky38). Furthermore, individuals with a family history of CVD had an elevated risk for MetS(Reference Lee, Jung and Park35).
After menopause, oestrogen diminution is correlated with the appearance of symptoms and with changes in risks of disease that have an important impact on women's health(Reference Silva, Barrett-Connor and Ramires39, Reference Al-Azzawi and Palacios40). Postmenopausal status may explain in part the acceleration of CVD with ageing. Changes in the hormonal milieu at menopause contribute to the development of insulin resistance(Reference Kalish, Barrett-Connor and Laughlin41). The present study showed that postmenopausal status was associated with increased odds for MetS, even after adjustment for confounding variables. This finding is in accordance with those reported by previous studies(Reference Eshtiaghi, Esteghamati and Nakhjavani42, Reference Janssen, Powell and Crawford43).
Increasing interest is being taken in the relationship between SES and MetS. However, it has not been completely consistent between studies(Reference Park, Oh and Cho28, Reference da Silveira, Horta and Gigante34, Reference Lee, Jung and Park35, Reference Loucks, Rehkopf and Thurston44). In Tunisia there is only one previous study conducted in the population of Greater Tunis investigating the relationship between education, as a socio-economic indicator, and MetS. An inverse relationship was found between this factor and MetS only in women(Reference Allal-Elasmi, Haj Taieb and Hsairi10). However, in that study adjustment was done only for age. In the current study, we examined the association of education level and occupation with MetS adjusting for possible confounding factors. Our results revealed that men with elevated level of education had significantly greater odds of having central obesity and dyslipidaemia. In the same group, the odds of having MetS increased with increasing level of education, even in the multivariate model. In women, higher education levels were protective against hypertension. In contrast to what was observed in men, in women, education level was inversely related to MetS, but without significance after adjusting for potential confounding variables. Our findings are partially consistent with those reported in Korean adults(Reference Park, Yun and Lee45). With respect to occupation, no association was found between this variable and MetS in both genders. There is some explanation for the gender difference in the relationship between education and MetS. Lower educational level is related to high morbidity and mortality from CVD, a relationship that is clearer among women than men(Reference Heller, Williams and Sittampalam46). Women with low levels of education have additional psychosocial risks (including high depressive symptoms, income under the poverty threshold, unemployment and single parenting) compared with men with low education(Reference Thurston, Kubzansky and Kawachi47). However, highly educated women are provided with greater levels of social, psychological and economic support(Reference Winkleby, Jatulis and Frank48). Furthermore, women with higher SES generally are more aware of the importance of health and fitness, and therefore tend to consume a healthy diet and regularly practise sports and exercise. In contrast, men of higher SES lead a more sedentary lifestyle and have a greater opportunity for smoking and consuming alcohol and rich foods(Reference Allal-Elasmi, Haj Taieb and Hsairi10). Future research focused on identifying mechanisms responsible for gender differences in the relationship between SES and MetS will provide better knowledge of the potential pathways.
Our study has strengths and limitations. The strengths include: the large sample consisting of both urban and rural populations; a sound representation of the national population; and detailed information on potential confounding factors. As a cross-sectional study, the present analysis is, however, limited in its ability to elucidate a causal relationship. The response rate was also less than desired as only 79·5 % of contacted participants and 58·0 % of targeted participants were included in the study. This introduces the possibility of selection bias and therefore limits the generalizability of the findings. Participants with missing values of the risk factors necessary for a diagnosis of MetS were excluded from the analysis to ensure that all analyses were done on the same data. There were no differences in baseline characteristics between those excluded and those included in the analysis. It is therefore unlikely that any bias resulted from the exclusion of persons with missing data. Another limitation was the absence of the measurement of HDL-C as explained above. Information about diet and physical activity was not included in the study.
Conclusion
The prevalence of MetS is high in both men and women in Tunisia. MetS is not only a concern for the urban population, but is also a matter of debate in rural areas. To reduce the risk of MetS, a multidimensional effort by individuals, society and the national health programme is necessary. Future prospective studies are also needed to clarify other potential risks for MetS.
Acknowledgements
The study was financed by the European Commission (ICA3-CT-2002-1001) and supported by a grant from the Ministry of Public Health of Tunisia. The authors declare that they have no competing interests. H.B. conceived the protocol, managed data collection and drafted the manuscript. S.B.A. researched the literature, conducted statistical analyses, contributed to interpretation of the results and to writing the manuscript. H.A.-S. and S.B. contributed to data collection management. P.T., B.M., F.D., N.A. and H.B.R. contributed to the study design and revision of the manuscript. All authors reviewed and edited the manuscript and approved the final version of the manuscript. The authors extend appreciation to all of the dedicated field workers and those who helped facilitate the field work in each survey site.
