Abstract
Objective. We aimed to estimate the attributable fraction of systolic (SBP) and diastolic blood pressure (DBP) that can be explained by family socioeconomic factors (FSFs) in adolescents using two observational studies. Methods. Participants were recruited by multistage random cluster in two cross-sectional studies performed in Europe [Healthy Lifestyle in Europe by Nutrition in Adolescence (HELENA) study, n = 3308] and Brazil [Brazilian Cardiovascular Adolescent Health (BRACAH) study, n = 991]. SBP and DBP were measured, and FSFs (socioeconomic status and parental education) were self-reported in both studies. The correlations of SBP and DBP with FSFs were examined by multilevel linear regression through two different models (hierarchical and fully adjusted). The generalized attributable fractions of the FSFs were estimated by comparing the models. Results. Our results showed a significant inverse relationship between parental education (father and mother) and SBP in European boys. The higher generalized attributable fraction to SBP was observed in boys (13.2–22.4%). In girls, we found lower generalized attributable fractions to DBP (10.8–12.1% in Brazilian girls and 3.1–3.8% in European girls). Conclusions. Our findings revealed a significant inverse relationship between parental education and SBP in European boys. FSF also significantly influenced blood pressure in adolescents, mainly in Brazilian adolescents.
Introduction
Chronic non-communicable diseases (NCDs) are the main source of disease burden worldwide; therefore, they comprise a major public health problem (Citation1). NCDs are highly prevalent, even during adolescence (Citation2), and previous studies have shown that having high blood pressure (BP) in childhood and adolescence is a risk factor for developing hypertension in adulthood (Citation3).
Of all the factors that may influence NCDs (e.g. genetics, intrauterine development, physical activity, sedentary behavior, tobacco use, total and abdominal obesity), family socioeconomic factors (FSFs) are both directly and indirectly associated with the health of adolescents, mostly indirectly through health behaviors (Citation4). Studies have shown that adolescents of lower socioeconomic status (SES) have a higher prevalence of NCDs (Citation5,Citation6).
However, most studies that have analyzed the association between FSFs and NCDs in adolescents have focused on obesity (Citation5,Citation7) or a cluster of cardiovascular risk factors (Citation8). Few studies have analyzed the association between FSFs and BP levels in adolescents from different geographical regions.
Therefore, we hypothesized that FSFs contribute significantly to the variation seen in systolic (SBP) and diastolic blood pressure (DBP) in adolescents. We tested this hypothesis in two cross-sectional observational studies conducted in adolescents: the Healthy Lifestyle in Europe by Nutrition in Adolescence (HELENA) study and the Brazilian Cardiovascular Adolescent Health (BRACAH) study.
Methods
In both studies, the samples were randomly selected. The objective of the HELENA study was to obtain data from a sample of European adolescents on a broad battery of nutrition and health-related parameters. Data collection took place during 2006 and 2007 in 10 cities from nine European countries. A detailed description of the HELENA sampling and recruitment methodology, data collection and quality control activities has been published elsewhere (Citation9,Citation10). After receiving complete information about the aims and methods of the study, all the parents/guardians signed a consent form, and adolescents gave assent to participate in the study. The protocol was approved by the human research review committees of the centers involved (Citation11).
The BRACAH study was conducted in the city of Maringá, located in the north-west of Paraná state (PR), southern Brazil, which has a population of approximately 330,000 (51,428 adolescents, 50.1% female). The methodology (sample size calculations and selection) of this study has been described previously (Citation12,Citation13). In brief, the population included 14–18-year-old adolescents of both genders who were enrolled in public or private high schools in Maringá in 2007. A broad battery of cardiovascular risk factors and health behavior parameters was investigated. A formal request to conduct this survey was sent to and subsequently accepted by the school boards of several schools of the city. This study was also approved by the Ethics Committee for Research Involving Human Participants of the University Center of Maringá and authorized by the Ethics Committee for Research Projects of the University of São Paulo in accordance with Brazilian law.
In the current study, we included adolescents from the HELENA and BRACAH studies with valid data on gender, age, SBP, DBP (outcomes), socioeconomic status, parental education, regular tobacco consumption, physical activity, sedentary behavior, body mass index (BMI) and waist circumference. These variables are described in detail below.
A total of 3308 adolescents from the HELENA study (12.5–17.5 years old) and 991 adolescents from the BRACAH study (14.0–17.5 years old) met all the inclusion criteria and were included in the analyses.
The response rate of questionnaires was high, at more than 85% in the HELENA study and 83% in the BRACAH study.
Outcome
Blood pressure
In both studies, BP measurements were performed following the recommendations for adolescent populations (Citation14). BP levels in both studies were measured twice after weight and height measurements were taken. The subjects were seated in a separate, quiet room for 10 min with their backs supported and their feet on the floor. Two BP readings were taken, with a 10 min interval of quiet rest. The lower of the two measurements was used.
SBP and DBP were measured using the OMRON® M6 (HEM 70001) oscillometric monitor device in the HELENA study and the OMRON M3 (HEM 742) device in the BRACAH study. The OMRON M3 (HEM 742) has been clinically and epidemiologically validated for adolescents by the Brazilian Research Group (Citation15). The OMRON M6 (HEM 70001) has been approved by the British Hypertension Society (Citation16). These data collection procedures have been described previously (Citation17).
Independent variables
The following family socioeconomic factors (FSFs) were analyzed: socioeconomic status and parental education.
Socioeconomic status was based on the family's financial situation, but the questionnaires applied in the two studies were different because of the differences between the countries. In both studies, the SES was classified into three levels: low, medium and high.
In the HELENA study, we used the same definition as in previous studies in HELENA (Citation18,Citation19). The SES scale is composed of four questions, and for each response, a score was given to the following: “Do you have your own bedroom?” (No = 0, Yes = 1); “How many cars are there in your family?” (None = 0, 1 = 1, 2 = 2, > 2 = 3); “How many computers are there in your home?” (None = 0, 1 = 1, 2 = 2, ≥ 3 = 3); and “Do you have Internet access at home?” (No = 0, Yes = 1). We computed the total score by summing the answers from all the questions (range 0–8), and we grouped these scores into three levels: low (0–2), medium (Citation3–5) and high (Citation6–8). In the BRACAH study, the Brazilian Criteria of Economic Classification were employed. These criteria consider parents’ education level, presence/absence and number of domestic appliances, vehicles and rooms in the adolescent's home. Using a specific questionnaire score (range 0–46), the family was classified into one of seven categories [A1 (the wealthiest), A2, B1, B2, C, D and E (the poorest)] (Citation20). In BRACAH, we grouped these categories into three levels: low (D and E), medium (B2 and C) and high (A1, A2 and B1).
Parental education was calculated using a self-reported questionnaire in both studies, and classified into four levels: lower education, lower secondary education, higher secondary education and university degree.
Potential confounders
Potential confounders considered in this study were the following:
Country (only in the HELENA study).
Age (years): calculated from date of birth and date of medical examination.
Physical activity: measured by questionnaire in both studies. It was adapted for the assessment of physical activity levels (moderate and vigorous levels) among adolescents (Citation21). Active subjects were classified after they reached at least 60 min/day of moderate and vigorous physical activity according to recommendations (Citation22).
Sedentary behavior: measured by a structured questionnaire, including questions on the average amount of time spent in front of the television (TV), computer and/or video games. This questionnaire is a reliable tool for use in adolescents (Citation23,Citation24). For example, the question “On weekdays, how many hours do you usually watch TV?” assessed the time spent in front of the TV from Monday to Friday. In both studies, the time spent in front of the TV, computer and video games was classified into the following groups: 0–2 h/day, > 2–4 h/day and ≥ 4 h/day.
Regular tobacco smoking: defined as the regular consumption of at least one cigarette per day in the past month (Citation25);
BMI: calculated as weight (kg)/height2 (m2). The continuous variable of BMI was used in the analysis. Height was measured to the nearest 0.1 cm and body mass to the nearest 0.1 kg, with a wooden stadiometer and a calibrated portable digital scale, respectively (wearing light clothes and no shoes).
Waist circumference: measured in both studies at the midpoint between the lowest rib and the top of the iliac crest with a non-elastic tape to the nearest 0.1 cm (Citation26).
Statistical analysis
Descriptive analyses were presented as the means (quantitative variables) and percentages (qualitative variables) and 95% confidence intervals (CIs). The attributable fractions were estimated by multilevel linear regression models using fixed effects for intercepts which were fitted to analyze the relationship between each BP level (continuous values) and the independent variables (Citation27). The context variable was the school. Moreover, homoscedasticity was graphically assessed (not shown) in all regression models to meet the criteria of this analysis.
For multivariate analysis, we used two different models: hierarchical and fully adjusted models. The hierarchical models included only the FSF variables, and these analyses (Citation28) were adjusted for age. The hierarchical models including the FSF variables (each variable in a separate model, e.g. one model for SES, another two models for each parent's education) were not adjusted for the potential confounders (individual behaviors, BMI or waist circumference). The objective was to obtain crude associations between FSFs and BP levels.
The subsequent fully adjusted multivariate models assessed associations adjusted for the following variables: age, FSFs (each variable in a separate model) and potential confounders (individual behaviors, BMI or waist circumference). The p values ≤ 0.20 were adopted in the univariate analysis (Citation28). Significance was considered if p values were < 0.05 or if there was more than 10% modification in β due to any variable already in the model.
Comparison of the hierarchical and the fully adjusted models was performed to estimate the generalized attributable fraction of FSFs associated with BP levels. To calculate the attributable fractions, we adapted the formula proposed by Menvielle et al. (Citation29) (logic equation is maintained) to continuous data (βh - βf)/(βh - 1), where βf refers to the β for SES and parental education in the fully adjusted model, and βh refers to the β in the hierarchical model. We performed comparisons between the models, with the aim of estimating the proportion of the effect of the FSFs on BP levels, and this proportion was already “adjusted” for the confounders’ variables because the R2 values from the full models were adjusted for all variables.
The statistical software package Stata version 12.0 (Stata Corp., College Station, TX, USA) was used for all statistical calculations. All analyses were adjusted for the clustered nature of the sample using the “svy” set of commands and stratified by gender because interactions between gender and the studied variables were observed (p < 0.001).
Results
Subjects’ characteristics, BP levels, independent variables and potential confounders are shown in . We did not find any significant associations between FSFs and BP levels in girls in either study. In both models, parental education (father and mother) was inversely associated with SBP in boys from the HELENA study. The Supplementary Table I (A and B) to be found online at http://informahealthcare.com/doi/abs/10.3109/08037051.2015.1033171 presents the β coefficients from both regression models for BP levels in the girls Supplementary Table I. (A) to be found online at http://informahealthcare.com/doi/abs/10.3109/08037051.2015.1033171 and boys Supplementary Table I. (B) to be found online at http://informahealthcare.com/doi/abs/10.3109/08037051.2015.1033171 of both studies.
Table I. Characteristics of the samples from the HELENA and BRACAH studies.
Subject characteristics, FSF variables, BP levels and potential confounders are shown in . shows the proportion of BP explained by FSFs for boys () and girls (). In boys, the association between BP and FSF levels was higher in the BRACAH study than in the HELENA study, with higher percentages in the SBP. The proportions explained by the association between SBP and FSF in both studies regarding girls were similar, whereas for DBP the proportion was higher in the Brazilian study.
Figure 1. Proportion of blood pressure levels explained by familial social factors for (A) boys and (B) girls. HELENA, Healthy Lifestyle in Europe by Nutrition in Adolescence; BRACAH, Brazilian Cardiovascular Adolescent Health Study.
Discussion
To our knowledge, this article is the first to analyze FSFs and BP levels in adolescents from two different observational studies (HELENA study, European sample; and BRACAH study, Brazilian sample). Only parental education was found to be associated with SBP in boys in the HELENA study; however, we did not find any significant associations in girls in either study. The principal message from our study is that parental education level is an important determinant of cardiovascular health and may play an important role in adolescent health, but it is not a good predictor of BP during adolescence. This finding was determined by the results of the generalized attributable fractions. The results from two different studies conducted in adolescents strengthen the conclusions.
Parental education has been previously observed to be directly associated with various aspects of adolescent health in developed and developing countries (Citation30); however, in our study, we found only an inverse association in boys from the HELENA study. These results may be due to parents with less education receiving less health care for their sons (Citation31). Another plausible explanation for this association is that adolescents of lower socioeconomic levels have lower levels of physical fitness (Citation19) and also lower levels of physical activity (Citation32), and these variables are directly associated with high levels of BP (Citation33). In our analysis, we adjusted for physical activity and sedentary behavior because adolescents from lower socioeconomic levels have a higher prevalence of high BP risk factors.
We found an association between the independent variables and the outcome only in boys in the HELENA study. A possible explanation may be that parents encourage girls to take care of their own health and use health services more than boys (Citation34,Citation35), whereas boys are more dependent on their parents. The health of adults is also directly associated with educational and socioeconomic levels (Citation36,Citation37).
We conducted further analysis, in which we quantified the generalized attributable fraction of FSFs in BP levels. In the BRACAH study, the percentages were higher than in the HELENA study for both genders; therefore, the family socioeconomic factors influence the levels of BP in Brazilian adolescents more than in Europeans. In countries with low to middle incomes, FSFs are associated with obesity (Citation5), which is directly associated with high BP (Citation38,Citation39). In adolescents from Brazil, these associations may be due to the young people living in these countries being more vulnerable to the rapid economic and urban development (Citation30) that mainly affects healthy behaviors such as physical activity (Citation40).
An important aspect to consider is that the criteria used to define FSFs are different in these two studies. The differences in results can be partly explained by these methodological aspects. Another factor that may influence the recorded prevalence of FSFs is the question of measurement accuracy. Differential or non-differential misclassification effects (error due to disease status or exposure) of FSF prevalence are unpredictable and may have caused the underestimation or overestimation of the true prevalence. In this study, it is likely that the validity of the criteria and tools varied for each characteristic of the adolescents (Citation41). In addition, there are differences between low socioeconomic class in Brazil and low socioeconomic class in Europe, but it was not possible to measure this difference in this sample. However, we believe that this factor is a small limitation because the questionnaires measured the family's financial situation and were divided into three levels in both studies.
Even with negative results, this study adds more evidence to the existing literature about FSFs and cardiovascular risk in adolescents. As noted previously, “we are biased by findings that are published and are thus blind to any studies that produce negative findings” (42, p. 785), and the publication of negative results may help to avoid potential publication bias in this area.
Because of methodological differences between the HELENA and the BRACAH studies (e.g. age range and geographical region), data from both studies were analyzed separately, but we used the multilevel analysis to control the influence of contextual (country-specific) variables because several studies have shown that they can influence the outcome (Citation43,Citation44).
A limitation of this study is its cross-sectional design; consequently, causality cannot be established. In addition, BP was measured only on a single occasion. Moreover, it was not possible to adjust the analysis for other factors potentially associated with BP and/or FSF, such as alcohol consumption, genetics or intrauterine development, in either of the samples. However, the large sample size, the diverse geographical origins of the samples and multilevel analyses help to strengthen this study.
Implications and contribution
Our findings reveal a significant inverse association between parental education (father and mother) and SBP in European boys. In addition, FSFs greatly influence BP in adolescents, mainly in Brazilian adolescents. These results suggest that future interventions aiming to improve adolescent health should consider parents’ educational levels to prevent elevated BP in adolescent populations and its implications for adult health.
Authors’ contributions
ACFM and HBC were the principal design researchers responsible for the data collection in the BRACAH study; LAM, MY, MS, AK, KW, LB and FG were the principal design researchers responsible for the data collection in the HELENA study; ACFM, HCB and LAM analyzed and performed data interpretation, as well as helping to draft the manuscript. All authors were involved in revising the manuscript critically for important intellectual content. ACFM was primarily responsible for the final content. All authors read and approved the final manuscript.
Supplementary material available online
Supplementary Tables IA, B showing β coefficients from regression models for blood pressure levels in girls and boys.
iblo_a_1033171_sm4433.doc
Download MS Word (173.5 KB)Declaration of interest: The authors state no conflicts of interest.
Funding
The HELENA Study received financial support by the European Community Sixth RTD Framework Program [contract FOOD-CT-2005-007034]. The authors take sole responsibility for the content of this article. This study was also supported by a grant from the Spanish Ministry of Health: Maternal, Child Health and Development Network [no. RD08/0072], a grant from the Spanish Ministry of Education [EX-2008-0641] and the Swedish Heart-Lung Foundation [20090635]. Augusto César de Moraes was given a scholarship from São Paulo Research Foundation - FAPESP [proc. 2011/11137-1 and 2011/20662-2]. Luis A. Moreno was given a scholarship as a visiting professor from the Brazilian government by the Science without Borders Program by CNPq (National Council of Technological and Scientific Development) and CAPES (Coordination of Improvement of Higher Education Personnel) [proc. 007/2012]. The GENUD Research Group was co-financed by the European Regional Development Fund [MICINN-FEDER].
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