Metabolic syndrome in young adults from two socioeconomic Latin American settings

Nutrition, Metabolism & Cardiovascular Diseases (2007) 17, 581e589

www.elsevier.com/locate/nmcd

Metabolic syndrome in young adults from two socioeconomic Latin American settings Patricia Bustos a,*, Antonio Augusto M. da Silva b, Hugo Amigo a, Heloisa Bettiol c, Marco A. Barbieri c a

Department of Nutrition, Faculty of Medicine, University of Chile, Independencia 1027, Santiago, Chile b Department of Public Health, Federal University of Maranha~o, Sa~o Luis, Brazil c Department of Puericulture and Pediatrics, Faculty of Medicine, University of Sa~o Paulo, Ribeira~o Preto, Brazil Received 26 October 2005; received in revised form 2 June 2006; accepted 5 June 2006

KEYWORDS Metabolic syndrome; Young adults; Risk factors

Abstract Background and aim: Since little information on the metabolic syndrome (MS) is available in Latin America, the aim of this study was to explore whether and to what extent differing socioeconomic conditions influence the prevalence of MS and its associated factors among young adults from two towns ~o Preto (RP), in Latin America: semi-rural Limache (L), Chile, and urban Ribeira Brazil. Methods and results: A cross-sectional study based on two independent investigations of 22- to 28 year-old subjects using a common methodology. The prevalence of MS (according to the US National Cholesterol Education Program) and its risk factors (smoking habit, alcohol and caloric intake, obesity, physical activity and socioeconomic conditions) were assessed. The prevalence of MS was 10% in L and in RP men, but was lower (4.8%) in RP women. Hyperglycemia was very low (0.8% in L and 1.1% in RP), while the prevalence of low HDL cholesterol levels was high (66.7% and 42.2%, respectively). Intermediate prevalences of hypertriglyceridemia (17.9% and 12.9%), elevated blood pressure (15.5% and 23.1%) and abdominal obesity (19.3% versus 12.7%) were detected. RP subjects had a higher educational level and more qualified jobs, came from smaller families, and a higher proportion were car owners. In L, the smoking habit was more frequent, subjects had higher excess weight and caloric intake, and lower levels of physical activity. Conclusions: Metabolic changes possibly leading to cardiovascular diseases in later life were present in both populations at an early age, but were higher in

* Corresponding author. Tel.: þ56 2 978 6213; fax: þ56 2 735 5581. E-mail address: [email protected] (P. Bustos). 0939-4753/$ - see front matter ª 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.numecd.2006.06.001

582

P. Bustos et al. the rural and less developed county. Our findings point to the existence of a cultural, educational and socioeconomic phenomenon that possibly influences the prevalence of the diagnostic components of MS through differences in lifestyles. ª 2006 Elsevier B.V. All rights reserved.

Introduction In recent years, most Latin American countries have experienced a rapid change in their epidemiological profiles. Morbidity and mortality from infectious and contagious diseases and malnutrition have decreased significantly, while noncommunicable chronic diseases (NCCD) and their associated risk factors have increased concomitantly [1e3]. Among these, the metabolic syndrome (MS) represents an adverse chronic condition comprising a set of cardiovascular risk factors related to central obesity, insulin resistance and hyperinsulinism [4e7]. In the United States, the reported prevalence of MS is 6.7% for persons aged 20 through 29 years and 43.5% for persons about 60 years old [8]. Increasing prevalences of MS have also been reported for this country, rising from 24.1% during the 1988e1994 period (National Health and Nutritional Examination Survey; NHANES III) to 27.0% in 1999e2000 (NHANES) [9]. In Korea, a 36% prevalence of MS has been recorded for the 30e79 age group [10], and in Oman a 21% prevalence has been recorded for subjects aged 20 years or more [11]. Studies on the prevalence of this syndrome are scarce and have been restricted to populations of middle and old age. However, it is important to conduct studies on younger populations to identify the age at which MS becomes relevant at the population level in both developed and developing countries. No studies have been conducted in Latin America to explore the prevalence of this syndrome. Thus, the aim of this study was to assess the prevalence of MS and some of its associated risk factors among young adults in two Latin American ~o Preto in Brazil and Limache in towns, Ribeira Chile, that have experienced a fast epidemiological and nutritional transition in recent years. This allowed exploring whether and to what extent differing socioeconomic conditions influence the prevalence of MS and its associated factors.

Methods The current analysis was cross-sectional, based on information obtained in two independent

investigations carried out using a common methodology and whose principal aim was to determine whether NCCD could have an early origin. The survey in Chile was carried out between 2001 and 2003 and involved 998 adults aged 22e28 years randomly selected from 3096 children born between 1974 and 1978 in the Chilean town of Limache in the Valparaiso Region. Subjects in the sample who emigrated from the city, refused to participate, were serving a custodial sentence or had a learning disability, corresponding to a total of 24.6%, were randomly replaced using the same sampling frame. Limache is a semi-rural town located 120 km from the capital city of Santiago. Its inhabitants are mainly dedicated to agriculture. The town was chosen for this survey based on the availability of information regarding birth registration, as well as the low migration rates of its population. ~o Preto is an urban city located in the Ribeira ~o Paulo. The city southeastern Brazilian state of Sa has one of the highest per capita incomes in Brazil. The economic base of the city is centered on the cultivation of sugar cane as well as on tertiary, industrial and commercial sectors. People belonging to a birth cohort studied in 1978/79 were located between 2002 and 2004. From the initial cohort of 9067 individuals, after the exclusion of babies whose mothers did not reside in the city (2094), twins (146) and those who died up to 20 years of age (343), 6484 individuals were eligible for the study. A total of 5665 individuals were located. Among these, one of each three individuals belonging to the same geographic area was contacted, invited to participate and asked to attend the base hospital. Among the individuals located, 12.4% had to be replaced using the original sampling frame because of refusal, imprisonment, death after 20 years of age and failure to appear for the interview. Thus, 2063 young adults effectively participated in the study, corresponding to 31.8% of the eligible sample. The same questionnaire used to collect information regarding the socioeconomic and demographic situation of the family and lifestyle (physical activity and food, tobacco and alcohol consumption) was applied in both towns. Anthropometric and blood pressure measurements were taken in the hospitals and a blood sample was

Socioeconomic status and Metabolic Syndrome obtained following a 12-h fast. All subjects gave informed consent to undergo these determinations. The procedures, questionnaires and definitions of every risk factor as well as the analysis of blood samples were based on the same protocols and therefore are outlined together. Blood pressure, weight, waist circumference and height of the subjects were measured by university nurses who were periodically supervised in order to minimize any variation between observations and to ensure the precision and accuracy of these measurements according to international recommendations. The anthropometric measurements were carried out with the participants wearing no shoes and minimum clothing. Height was measured to the last complete millimeter in barefoot participants and weight was assessed using beam weighing scales. The definitive weight recorded was obtained after a uniform subtraction of the average weight of clothing. Waist circumference was also assessed using a flexible tape at the level of the navel with the patient standing. Blood pressure was measured three times according to the procedure adopted in other epidemiological studies [12,13], using a 740 Omron sphygmomanometer. The average of the measurements of the last two readings, made at an interval of 10 min between each other, was calculated. In Chile, HDL cholesterol was measured by precipitation according to the technique of Seigler and Wu and triglycerides were measured using enzymatic methods (HUMAN factor, Gesellschaft fu ¨r Biochemica und Diagnostica, Germany). In Brazil automatic enzymatic colorimetry methods were applied using the Dade Behring XPand device and reagents of Dade Behring Dimension for clinical chemistry for HDL, total cholesterol, and triglycerides. In both Chile and Brazil an enzymatic colorimetric method (GOD/PAP, Human Diagnostic, Germany) was used to record blood glucose levels. Additionally, insulin was determined by radioimmunoassay to calculate insulin resistance using the homeostatic model assessment (HOMA-IR) [14]. A diagnosis of MS was made when three or more of the following factors were present: abdominal obesity (waist circumference >102 cm in males or >88 cm in females), triglycerides 150 mg/dL, HDL cholesterol <40 mg/dL in males or <50 mg/dL in females, fasting glucose 110 mg/dL and blood pressure 130/85 mmHg, according to the Third Report of the National Cholesterol Education Program Expert Panel on Detection, Evaluation and Treatment of high blood cholesterol in adults [4]. Additionally, HOMA values 2.53 were considered to indicate insulin resistance according to the distribution of a healthy Chilean population [15].

583 The risk factors for MS studied were: smoking, caloric and alcohol intake as well as insufficient physical activity. The following criteria were adopted to define these risk factors: smoking habit was considered to be present if the subject had smoked within a month before the interview, excessive alcohol consumption was defined as the ingestion of more than 31.1 g of alcohol a day according to the cut-off points proposed by Dawson and revised by Dufour [16], and insufficient physical activity was defined if the participants had less than 600 MET-minutes/week according to the International Physical Activity Questionnaire (IPAQ) in its short version [17]. Body mass index (BMI) was calculated to classify nutritional status using the following categories: underweight (BMI < 18.5), normal (between 18.5 and 24.9), overweight (between 25.0 and 29.9) and obese (BMI  30) according to the international recommendations of the World Health Organization [18]. Caloric intake was calculated using a food frequency questionnaire. Variables addressed to measure socioeconomic factors were occupation (non-manual, manual and unemployed) according to the International Classification of Occupations [19], educational level of the participant (8, 9e11 and 12 years of study), number of siblings, number of persons in the house, and percentage of car owners. The information was typed on a double form in an Access program in both Chile and Brazil and the analysis was carried out using the SPSS (version 13.1) and Stata (version 8.0) software. Total prevalence rates were determined in each city and also according to sex, and statistical significance was determined by the chi-square test for the comparison of proportions and by the Student t-test for comparison of the means. Both studies were completed under the internationally accepted ethical guidelines for human surveys and were approved by the Ethics Committees of the respective institutions, i.e., the Faculty of Medicine, University of Chile, and the ~o Preto, University Faculty of Medicine of Ribeira ~o Paulo. of Sa

Results The characteristics of the subjects studied in the two cities were different: the population of ~o Preto, Brazil, was younger, with a Ribeira female/male ratio close to one. Over 30% had an educational level of more than 12 years and the proportion of people with non-manual and qualified manual occupations was also higher than

584 that found in Chile. In Limache, the sample consisted predominantly of women, the educational level was lower (only 20% had more than 12 years of schooling) and the proportion of subjects in the ‘‘out of work’’ category reached 50% (Table 1). The socioeconomic characteristics of the families also differed between the two towns: in ~o Preto, the number of family members Ribeira and siblings was lower than in Limache while the number of car owners per family was higher (Table 1). A high prevalence of excess weight was recorded in both countries, with values reaching 50% in Chile. Differences according to sex were also observed, with males in Brazil showing higher overweight and obesity levels, whereas in Chile the prevalence of these conditions was higher among females. Underweight subjects were practically non-existent in Chile, while in Brazil the prevalence of this nutritional problem reached almost 9% among females (Table 2). Both countries had high prevalences of some risk factors for chronic adult disease, i.e. high levels of tobacco and alcohol intake, especially among males. Nearly 60% of men in both countries were considered to be ‘‘physically active’’ (>1500 MET-minutes/week). In contrast, females showed higher levels of insufficient physical activity, ~o Preto reaching 50% in Limache and 40% in Ribeira (Table 3). The prevalence of the metabolic syndrome was low in both populations of young adults, reaching ~o Preto and in both sexes 10% in men from Ribeira ~o Preto in Limache, while in women of Ribeira the prevalence of the disease was lower: 4.8% (Table 4). Regarding the components of the metabolic syndrome, a very low prevalence of high fasting glucose levels and a high prevalence of low HDL values were found. Hypertriglyceridemia, abdominal obesity and elevated blood pressure showed intermediate prevalences. Subjects in Chile had significantly higher proportions of abdominal obesity and hypertriglyceridemia and low HDL values, while the Brazilian subjects had a higher prevalence of elevated blood pressure (Table 4). There were also differences according to sex in almost all variables, the most remarkable being the high proportion of increased blood pressure levels among men, especially in Brazil. Hypertriglyceridemia was also high among men while low HDL values were more common among women. In Limache, a higher prevalence of abdominal obesity in women was also detected (Table 4).

P. Bustos et al. Mean HOMA-IR values were also very different in the two countries: 2.52 in Limache and 1.53 ~o Preto. In addition, the proportion of in Ribeira subjects with high HOMA-IR values was also quite different: 34.5% in Chile and 13.9% in Brazil (Table 4).

Discussion The present study confirms the low prevalence of metabolic syndrome among young adults in both countries. However, the prevalence in Limache ~o Preto was slightly and among men of Ribeira higher than the figures observed in other countries for this age group [8,20,21]. The study also highlighted the high prevalence of some of the components of the MS (low values of HDL and high levels of blood pressure), some of the underlying causes of this pathology (i.e. obesity and insufficient physical activity) and other risk factors for NCCD (smoking and alcoholism). A low prevalence of hyperglycemia was also noticed. Our findings point to the existence of a cultural, educational and socioeconomic phenomenon that possibly influences the prevalence of the diagnostic components of MS based on differences in lifestyles, rather than belonging to a particular place. Among young people, the rural and less developed Limache showed a higher prevalence of high levels of HOMA and other risk factors for cardiovascular diseases. People from Limache also had a lower socioeconomic level than their Brazilian counterparts (as evaluated by schooling and intra-familiar socio-demographic variables). On the other hand, a high socioeconomic status in Brazil was associated with a lower number of persons in the family, lower number of siblings, non-manual or qualified manual occupations, higher number of car owners, higher level of physical activity, lower prevalence of smokers, higher intake of alcohol and lower caloric intake. In parallel, high socioeconomic status in Brazil was also associated with lower blood pressure levels, lower abdominal obesity, lower triglycerides, higher HDL levels, similar fasting glucose levels, but definitely lower HOMA levels and a lower prevalence of overweight and obesity. These findings suggest that the people from the two cities could be in different stages of the epidemiologic and nutritional transition and/or that the differences found in the socioeconomic conditions are responsible for these results. Possibly increasing awareness of cardiovascular ~o risk factors among well-off people in Ribeira Preto may have helped them to develop healthier

General and socioeconomic characteristics of the samples according to sex, in Chile and Brazil ~o Preto, Brazil Ribeira

Limache, Chile Total (n)

Men (n)

Women (n) P *

Total (n)

Men (n)

Total Chile Men Chile Women Chile vs. Brazil vs. Brazil vs. Brazil Women (n) P **

P ***

P ****

P *****

Age (years): mean  SD % by gender

24.8  1.6 25.0  1.6 24.7  1.6 100.0 43.7 56.3

0.009 e

23.9  0.7 23.9  0.7 23.9  0.7 100.0 48.2 51.8

0.999 <0.001 e 0.019

<0.001 e

<0.001 e

Schooling (years) (%) 8 9e11 12

n ¼ 998 21.4 56.8 21.7

n ¼ 436 24.5 55.3 20.2

n ¼ 561 19.1 57.9 23.0

0.100

n ¼ 2063 15.5 50.4 34.1

n ¼ 995 16.3 51.7 32.1

n ¼ 1068 14.8 49.2 36.1

0.151 <0.001

<0.001

<0.001

Occupation (%) Non-manual Qualified manual Semi-qualified manual Non-qualified manual Out of work

n ¼ 996 13.2 13.3 7.4 27.9 38.2

n ¼ 435 15.4 25.5 4.1 42.3 12.6

n ¼ 561 11.2 4.3 9.6 16.9 57.9

<0.001 n ¼ 2061 23.8 21.1 16.6 17.8 20.8

n ¼995 15.4 21.0 23.0 15.6 25.0

n ¼ 1066 31.6 21.1 10.6 19.8 16.9

<0.001 <0.001

<0.001

<0.001

No. of siblings: mean  SD 3.6  2.3

3.5  2.2

3.7  2.3

0.165

2.5  1.7

2.5  1.7

2.5  1.7

0.999 <0.001

<0.001

<0.001

No. of persons in the family: mean  SD

4.4  1.8

4.3  1.7

4.5  1.8

0.075

3.9  1.5

4.0  1.5

3.9  1.5

0.134 <0.001

0.001

<0.001

Car owners (%)

25.9

30.2

22.6

0.007

82.0

77.0

0.002 <0.001

<0.001

<0.001

79.0

Socioeconomic status and Metabolic Syndrome

Table 1

*P value for the difference between men and women in Chile. **P value for the difference between men and women in Brazil. ***P value for the difference between Chile and Brazil. ****P value for the difference between men in Chile and Brazil. *****P value for the difference between women in Chile and Brazil.

585

586

Table 2

Nutritional status and caloric intake among men and women in Chile and Brazil ~o Preto, Brazil Ribeira

Limache, Chile

Total Chile vs. Brazil

Men Chile vs. Brazil

Women Chile vs. Brazil

Total %

Men %

Women %

P*

Total %

Men %

Women %

P **

P ***

P ****

P *****

Body mass index Underweight Normal Overweight Obese

n ¼ 998 0.8 49.4 34.3 15.5

n ¼ 436 0.5 51.6 37.6 10.3

n ¼ 562 1.1 47.7 31.7 19.6

<0.001

n ¼ 2056 5.7 58.4 23.9 12.0

n ¼ 992 2.6 53.9 30.3 12.8

n ¼ 1064 8.6 62.1 17.7 11.1

<0.001

<0.001

0.003

<0.001

Caloric intake (kcal) SD N

2963 1345 982

3637 1380 429

2439 1055 553

<0.001

2121 727 2063

2355 743 995

1903 639 1068

<0.001

<0.001

<0.001

<0.001

*P value for the difference between men and women in Chile. **P value for the difference between men and women in Brazil. ***P value for the difference between Chile and Brazil. ****P value for the difference between men in Chile and Brazil. *****P value for the difference between women in Chile and Brazil.

Table 3

Risk factors for the metabolic syndrome among men and women in Chile and Brazil ~o Preto, Brazil Ribeira

Limache, Chile Total % (n) Men % (n)

Women % (n) P *

Physical activity Active Sufficiently active Insufficiently active

(999) 39.0 22.6 38.3

(437) 59.3 18.1 22.7

(562) 23.3 26.2 50.5

Current smokers (%)

56.4 (999)

66.4 (437) 48.6 (562)

Excessive alcohol intake (%)

13.8 (999)

29.3 (437) 1.8 (562)

Men % (n)

Women % (n) P **

(995) 61.6 13.9 24.5

(1068) 41.8 17.9 41.3

P ***

P ****

P *****

<0.001 <0.001

0.119

<0.001

<0.001 17.2 (2063) 20.8 (995) 13.9 (1068)

<0.001 <0.001

<0.001

<0.001

<0.001 20.3 (2049) 32.8 (988) 8.7 (1061)

<0.001 <0.001

0.191

<0.001

P. Bustos et al.

*P value for the difference between men and women in Chile. **P value for the difference between men and women in Brazil. ***P value for the difference between Chile and Brazil. ****P value for the difference between men in Chile and Brazil. *****P value for the difference between women in Chile and Brazil.

Total % (n)

<0.001 (2063) 51.3 15.5 33.2

Total Chile Men Chile Women Chile vs. Brazil vs. Brazil vs. Brazil

<0.001 <0.001 0.005 <0.001 *P value for the difference between men and women in Chile. **P value for the difference between men and women in Brazil. ***P value for the difference between Chile and Brazil. ****P value for the difference between men in Chile and Brazil. *****P value for the difference between women in Chile and Brazil.

0.489 13.9 (2043) 16.1 (991) 11.8 (1052) 34.5 (999) 35.7 (437) 33.6 (562) Elevated HOMA (%)

0.813 <0.001 0.009 <0.001 0.195 <0.001 <0.001 0.002 <0.001 0.755

<0.001 0.734 0.020

(1065) <0.001 <0.001 (1067) 0.066 <0.001 (1050) <0.001 <0.001 (1050) 0.019 <0.001 (1052) 0.569 0.435 6.4 14.0 9.8 44.7 1.0 (994) (994) (987) (987) (991) 41.1 11.3 16.1 39.5 1.2 (2059) (2061) (2037) (2037) (2043) 23.7 12.7 12.9 42.2 1.1 <0.001 <0.001 <0.001 <0.001 0.085 (561) (561) (562) (561) (562) Components of the metabolic syndrome High blood pressure 15.5 (998) 27.7 (437) 6.1 Abdominal obesity 19.3 (998) 4.8 (437) 30.7 High triglycerides 17.9 (999) 22.9 (437) 14.1 Low HDL values 66.7 (997) 55.0 (436) 75.8 High fasting glucose 0.8 (999) 1.4 (437) 0.4

P* Women % (n) Men % (n)

0.959 7.6 (2028) 10.7 (985) 4.8 (1043) <0.001

P ***** P **** P *** Women % (n) Total % (n) Total % (n)

Men % (n)

~o Preto, Brazil Ribeira Limache, Chile

10.1 (997) 10.1 (436) 10.2 (561) Metabolic syndrome

Table 4

Prevalence of the metabolic syndrome and its components among men and women in Chile and Brazil

P **

Total Chile Men Chile Women Chile vs. Brazil vs. Brazil vs. Brazil

Socioeconomic status and Metabolic Syndrome

587 lifestyle habits, which prevented some of them from showing high levels of early markers of future ~o Preto cardiovascular disease. Since in Ribeira access to health care is nearly universal, medical intervention may have also contributed to positive changes in lifestyle habits in this town. The prevalence of metabolic syndrome was the same among men and women in Chile while in Brazil the proportion of males was double that of females. One of the explanations for this finding may be that Brazilian women are more physically active and have lower levels of caloric intake than their Chilean counterparts, a fact suggesting greater concern among Brazilian women regarding the maintenance of their physical shape. This finding agrees with information pointing to a decreasing prevalence of obesity among Brazilian women within the high socioeconomic group between 1989 and 1997 [2]. This is also in line with some reports pointing out that anorexic/restrictive behavior appears to be on the increase among young women in Brazil [22]. The presence of elevated blood glucose levels was low in both cities. This may be due to the fact that more time is needed for this problem to manifest, since initially it is the pancreas that maintains homeostasis by secreting more insulin and generating insulin resistance before the installation of hyperglycemia. The data for Chile support this hypothesis, considering that 35% of the participants had elevated HOMA-IR levels (>2.53). The fact that the prevalence of metabolic syndrome increases in people with base diseases such as hypertension or insulin resistance is already well known [23]. The reason why Chilean women showed higher abdominal obesity and lower HDL levels may be due to the fact that they also had a higher caloric intake and lower physical activity, with a higher percentage of housewives or students grouped in the ‘‘out of work’’ category. A revision of the criteria defining the clinical identification of MS appears necessary given that the cut-off points in HDL levels adopted recently (<40 mg/dL for men and <50 for women) appear to be very high. It seems difficult to accept that 75% of Chilean females and over 40% of the young population in Brazil have lower values at this age. Moreover, the cut-off point (135/85) for elevated blood pressure appears to be very low for males, resulting in a high proportion of altered values among young men. Figures from Korea also suggest that this cut-off point is inadequate [24]. These observations agree with an early study which suggested that MS may not be as well defined and characterized as it is often assumed [25]. Moreover, the

588 discrepancy between the prevalence of MS diagnosis and the elevation of HOMA levels suggests lack of precision of both measures. A possible explanation for the different prevalences of some of the components of the MS could be that the samples were assessed by different laboratories, but it should be mentioned that because of the similar techniques used for the determination of glycemia, HDL or triglycerides it is possible to find similar values in different laboratories and that in this case, the determinations were carried out by trained professionals using validated and internationally standardized methodology. One of the principal strengths of the present studies is that they were representative of two young healthy populations. Another strength of these studies is that the information was obtained using the same methodology (including the same questionnaire and the same supervised techniques), thereby allowing comparisons between the two countries. Appropriate sample sizes were achieved in each country and the power to detect differences in proportions and means was higher than 90% in most cases. This study demonstrates that the first metabolic changes possibly leading to cardiovascular risk are present in both semi-rural and urban populations at an early age. This finding indicates a need to design and implement interventions to prevent these risk factors from increasing at a later age. Modifications such as control and treatment of excess weight, which has been pinpointed as one of the most important determining factors in the increase in MS at this age, are necessary [26].

Acknowledgments

P. Bustos et al.

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The study in Chile received financial support from the Chilean National Fund for Scientific and Technological Development (Fondecyt), under grant 1010572, and the study in Brazil was supported by Conselho Nacional de Desenvolvimento Cientı´~o de Amparo fico e Tecnolo ¸a ´gico (CNPq) and Fundac ~o Paulo (FAPESP), under a ` Pesquisa do Estado de Sa grant 2000/09508-7.

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