Services on Demand
Print version ISSN 1517-8692
On-line version ISSN 1806-9940
Rev Bras Med Esporte vol.13 no.2 Niterói Mar./Apr. 2007
Daily energy expenditure and plasmatic lipid-lipoprotein levels in adolescents*
Dartagnan Pinto Guedes; Joana Elisabete Ribeiro Pinto Guedes; Décio Sabbatini Barbosa; Jair Aparecido de Oliveira
The aim of the present study was to analyze the impact of regular practice of physical activity facing estimates of daily energy expenditure (EEdaily) in the plasmatic lipid-lipoprotein profile in a representative sample of adolescents. The sample consisted of 452 subjects (246 females and 206 males), age between 15 and 18 years. The plasmatic lipid-lipoprotein concentrations were established through laboratory procedures. The data concerning the regular practice of physical activity were obtained though a retrospective instrument of self-recording. Estimates concerning the EEdaily were established based on the caloric cost associated with the type and the duration of the activities registered by the adolescents. The sample was divided in three groups of regular practice of physical activity: the least active, < 25º percentile of the EEdaily; the moderately active, 25-75º percentile of the EEdaily; and the most active, > 75º percentile of the EEdaily. Cutting points for an atherogenic lipid-lipoprotein risk were also established. The results of the analysis of covariance, having the participation of the body mass index controlled, showed that the HDL-C concentrations were significantly different according to the growing groups of EEdaily in females (p = 0.009) and in males (p = 0.010). However, the variation behavior of the values observed was different in the two sexes. The analysis of logistic regression showed that the relative risk for lower values of HDL-C was two times higher among the least active adolescents comparing with the most active ones. In both sexes the concentrations of total cholesterol, LDL-C and triglycerides did not present significant differences among the groups of EEdaily. In conclusion, more intense regular practice of physical activity as well as higher EEdaily are associated with higher concentrations of HDL-C in adolescents of both sexes, regardless of the variations of body weight. The associations between EEdaily and the other plasmatic components of lipid-lipoproteins treated in the present study were weak and inconsistent.
Keywords: Physical activity. Sedentarism. Cardiovascular risk factors. Cholesterol. Triglycerides.
Despite the trend of decline in death cases, in the industrialized societies the coronary arterial disease (CAD) is one of the main causes of morbid mortality(1). Although reasons which effectively may lead to this decrease of the mortality rates are not conclusive, such fact has been attributed to advances concerning diagnosis, treatment and health insurance coverage concerning this pathology(2).
Nowadays, developing countries have been presenting a profile of morbid mortality which suggests an epidemiological transition. In this case, from a situation in which there was higher predominance of infectious diseases to another model in which chronic degenerative diseases linked to risk behaviors, such as CAD, start to be the dominant causes of mortality(3). In Brazil, from 20 years of age on, it is estimated that CAD corresponds to approximately 20% of the deaths for known reasons(4). Moreover, CAD is the main cause of expenses in medical assistance in the country(5).
CAD presents a multifactor etiology and its clinical manifestations occur almost exclusively in adulthood(6). Nonetheless, it is well reported in the literature that the atherosclerosis process may trigger its development in childhood and adolescence as well as advance it in several stages, developing to a posterior premature coronariopathy in adulthood(7-9). Therefore, it has been recommended that CAD primary prevention strategies, including the promotion of suitable and regular physical exercise practice, begin as early as possible(10-12).
Epidemiological evidence reveals a strong identification between a compromised plasma lipid-lipoprotein profile and morbidity cases by CVD(13-15). Particularly in this case, in adult subjects, the available studies have tried to demonstrate that daily practice of physical activity may prevent or at least minimize the development of CAD as well as its risk factors, specifically, altered values of plasma lipids-lipoproteins. Nonetheless, in young populations the results of studies which try to show occasional association between physical activity practice and a favorable profile of plasma lipid-lipoprotein are clashing(16-25). These results may probably present divergences due to the different research framework proposed, the statistical procedures used in the data analysis as well as the nature and specifications of the methods applied in the data collection equivalent to the daily physical activity.
Within this context, the aim of the present study was to analyze the impact of the daily physical activity practice, with data associated to the estimation of the daily energy expenditure in the plasma lipid lipoprotein of adolescents.
Data present in the database built from the research project 'Physical Activity, Diet Composition and Risk Factors Prone to Cardiovascular Diseases in Adolescents' were used for the study's elaboration. This research includes adolescents with age between 15 and 18 years of age of both sexes(26-28).
The research project had as target students regularly enrolled in the high school of the Application School linked to the State University of Londrina, Paraná State. Subjects who only went to this school were chosen due to the study's longitudinal characteristics (experimentation of health educational programs through diet interventions as well as physical exercises practice), and for its representation in the universe of high school students from the Londrina county, Paraná.
The intervention protocols in the study were approved by the Ethics Committee in Research of Londrina and followed norms of the 196/96 Resolution of the National Health Council on research involving humans. The subjects' inclusion in the study was voluntary and with authorization from the parents or responsible ones. All students enrolled in the school year of 2003, along with their parents or responsible ones, were contacted and informed about the study's nature and aims. 452 (246 girls and 206 boys) students out of the 518 enrolled ones, agreed to participate in the study.
As additional data of the sample analyzed in the study, we can highlight that, based on the socio-economical classification criteria of the students' families, with data concerning educational background of the family's leader, housing conditions, household appliances and cars possession, as well as the number of domestic servants(29), it was observed that 22% of the students were categorized in low socio-economical status; 27% in high status and 51% in intermediate status. Concerning the classification criteria of sexual maturation suggested by Tanner(30), 10% of the analyzed girls presented breasts development equivalent to stage III, 61% to stage IV and 29% to stage V. Among the boys, 49% were in stage IV of development of pubic hair, and the remaining 51% in stage V.
In the anthropometric field, height and body weight measurements were performed from the standards suggested by Gordon et al.(31). Body mass index (BMI) calculation was also established considering the ratio between the body weight and the square of the height measurements (kg/m2).
The doses of plasma lipid lipoproteins were performed with collection of samples of 10 ml of venous blood from the elbow fold, after a period of 10-12h fasting, between 07:00 and 08:00h in the morning. The serum was immediately separated by centrifugation, being the amounts of triglycerides (TG), total cholesterol (TC) and fractions, low density lipoproteins (LDL-C) and high density (HDL-C) determined. The TC was determined by the enzymatic method cholesterol oxidase/peroxidase in a spectrophotometer instrument. The HDL-C was measured through precipitant reactive method, and the LDL-C was calculated by the Friedewald formula(32). The TG was determined by the glycerol enzymatic method. Besides the absolute values of each plasma component, the TC/HDL-C and LDL-C/HDL-C ratios were considered. The reference values applied in order to define an atherogenic risk lipid lipoprotein profile followed the proposal presented for adolescents with the III Brazilian Guidelines on Dyslipidemias(33): TG > 130 mg/dl, TC > 200 mg/dl, LDL-C > 130 mg/dl and HDL-C < 35 mg/dl.
In order to have the physical activity practice levels estimated, the self-record retrospective instrument of the daily activities, devised by Bouchard et al. was used(34). In this case, the daily activities are classified in a continuum involving nine categories, according to estimates concerning mean caloric cost of the activities performed by humans: (1) rest in bed; (2) activities performed at sitting position; (3) mild activities performed at standing position; (4) activities which involve mild walks (< 4 km/hour); (5) mild hand labor; (6) active leisure activities and practice of recreational sports; (7) moderate hand labor; (8) active leisure activities and moderate sports practice; and (9) intense hand labor and practice of competitive sports. Since it is practical, innocuous and easy to be interpreted, the present instrument has been widely accepted and used in other studies involving young populations(25,35-38).
The retrospective instrument was filled out by the adolescents themselves in four days of the same week, two in the middle (between Monday and Friday) and two on the weekend (Saturday and Sunday). The pondered mean involving the two days of the middle and of the weekend was used for the calculation. For its administration, the day was divided in 96 periods of 15 minutes each. The study's participants received instructions and recommendations to identify the kind of activity classified between categories 1 and 9, performed in each 15-minute period, during the 24 hours of the day. A list with typical daily activities, exemplifying activities completed in the different categories, was presented to the adolescents in the trial to facilitate the completion of the instrument. Moreover, the participants were told to take additional notes if any performed activity had not been mentioned on the list specifically devised for this purpose.
Based on this data, the time expenditure of each study's participant in the different categories of physical activity was established. The expenditure time in categories 6 to 9 (mean energetic cost > 4.8 Mets) was considered as an indicator of moderate to vigorous intensity physical activity (MVPA). The expenditure time in categories 3 to 5 (mean energetic cost between 2.3 and 3.3 Mets) was used as an indicator of low intensity physical activity (LIPA); and in categories 1 and 2 (mean energetic cost < 1.5 Mets) as an indicator of physical inactivity (PHIN). Additionally, based on the caloric references suggested by the devisors of the used measurement instrument(34), the estimates of energetic expenditure by kilogram of body weight of the activities performed during the day (kcal/kg/day) were used as indicators of the daily physical activity practice (EEDaily). This procedure was validated to be used in adolescents with the double marked water criterion technique. The mean difference of the EEDaily between the two methods was of 1.2% with a variation coefficient of 15%(39).
The statistical treatment of the data was performed with the computer package Statistical Package for the Social Science (SPSS), version 13.0. Firstly, the sample was stratified in three groups of daily physical activity practice according to cut-points specific by sex and EEDaily. The least physically active group had those adolescents who presented EEDaily below percentile 25 (< 35.1 and < 35.2 kcal/kg/day between girls and boys, respectively). Adolescents between 25 and 75 percentiles of the EEDaily (35.2-37.7 and 35.3-39.5 kcal/kg/day between girls and boys, respectively) were considered moderately physically active, and those above the percentile 75 of the EEDaily (> 37.8 and > 39.6 kcal/kg/day between girls and boys, respectively) were considered the most physically active. Later, in order to have the anthropometric and daily physical activity practice variables selected in the study analyzed, variance analysis procedures were conducted. The comparisons between the values equivalent to the plasma lipid lipoproteins of the categorized adolescents in each of the three groups of daily physical activity practice (least active, moderately active and most active) were performed through co-variance analysis. In the trial to control the additional effects concerning surplus weight in the impact of physical activity over the lipid lipoprotein profile, the BMI values were considered as co-variables in the statistical analysis. Odds Ratio (OR) values, established through binary logistic regression analysis, also controlling the BMI values, were used in order to establish estimates concerning the related risk with adolescents who present atherogenic risk lipid lipoprotein profile due to the categorization in decreasing groups of daily physical activity practice. Reliability interval of 95% was adopted.
Statistical data concerning the anthropometric variables as well as daily physical activity practice are found in table 1. The cut-points equivalent to the 25 and percentiles are lower among girls, suggesting hence that boys are daily more active. In both sexes, occasional differences observed concerning age, height, body weight and BMI of the adolescents joined in the three groups of daily physical activity practice are not mentioned in statistical language. However, as expected, the mean expenditure time in the LIPA, MVPA and categories of physical activity practice and the EEDaily present statistically significant differences (p < 0.000) favorable to the girls and the most physically active boys. The mean time of PHIN is significantly higher among least physically active adolescents (p < 0.000).
Results equivalent to the co-variance analysis, statistically controlling the data associated with the BMI are shown in table 2. The plasma concentrations of HDL-C (p = 0.009 and p = 0.010 for girls and boys, respectively) of the adolescents analyzed in the study present differences according to the increasing groups of daily physical activity practice; however, the variation behavior of the values observed is different in the two sexes. While in the boys the most remarkable differences are observed in the most active group in comparison with its moderately active and least active pairs, in the girls this phenomenon is observed in the moderately active group in relation to the least active one. The values observed concerning TC, LDL-C, TG and the TC/HDL-C and LDL-C/HDL-C ratios did not present statistical differences among the three daily physical activity practice groups.
Table 3 shows the OR dimensions followed by the reliability intervals of 95% equivalent to the relative risk of the adolescents analyzed in the study present atherogenic risk lipid lipoprotein profile due to the classification in daily physical activity practice groups. The results of the logistic regression analysis show that the OR dimensions for dislypoproteinemia are higher in girls and among adolescents of lower daily physical activity practice when compared with the remaining groups. Nevertheless, in the present investigation, only in the HDL-C case the adolescents with lower EEDaily demonstrate higher relative risk statistically significant of presenting compromising amounts in comparison with their pairs of higher EEDaily (girls OR = 2.18; 95% IC 1.31-3.11; boys OR = 1.96; 95% IC 1.26-2.75). In the other three plasma components (TC, LDL-C and TG) it was verified that the found OR values are not relevant in statistical language.
The main finding of the present study revealed that, in adolescents, high EEDaily, induced by daily physical activity practice, is associated with higher serum concentrations of HDL-C. Moreover, the EEDaily and the highest amounts of HDL-C present specific behavior in each sex. The OR also showed significant higher risk of finding atherogenic risk HDL-C values in the least active adolescents group compared with its pairs joined in the most physically active group. The associations observed between the EEDaily and the remaining plasma components of lipid lipoproteins treated in the present study were weak and inconsistent. Corroborating with the expectations found in the literature, the results found here agree with the data provided by studies previously conducted, involving other measurement indicators aimed at monitoring physical activity(16-25).
Sometimes the modifications in the plasma lipid lipoprotein profile of adolescents are tried to be justified by the concomitant alterations in their body weight(17,25). In the present study, the values of BMI were statistically controlled with the co-variance analysis. In that case, even in the lack of participation of the BMI values, the results found showed that the adolescents who belonged to the group with higher EEDaily presented significantly higher values of HDL-C compared with its pairs which belong to the groups of lower EEDaily.
It has been proved in studies involving adults that a less physically active lifestyle is a risk behavior clearly identified with altered values of plasma lipid lipoproteins (40-43); however, this association has not been confirmed with the same potential in young populations, which has been intriguing the researchers of the field.
The justifications which possibly explain the observed differences in the magnitude of the associations between physical activity and lipid lipoproteins plasma concentrations of adults and adolescents are still obscure. Nonetheless, the less discriminatory ability concerning the daily physical activity practice and lipid lipoprotein profile of adolescents compared with adults, besides implications concerning the biological maturation process, deserved attention.
The fact that adolescents are naturally more active in their routine compared with adults has been a widely used argument by some researchers(16-17,19) once the occasional variations in the plasma lipid lipoproteins amount in a higher level of daily physical activity practice do not present the same sensibility than in adults. However, based on the found results in the present study, such hypothesis should be discarded, taking into consideration that the expenditure time of the most active adolescents in MVPA was significantly higher than its moderately active and least physically active pairs. As an illustration, we can say that the mean expenditure time in MVPA (> 4.8 Mets) in boys considered the most physically active was 98.17 minutes/day; that is, higher than the 30-60 daily minutes recommended for adolescents by the public health organs(44-45), which was not the case of boys considered moderately active (25.29 minutes/day) and least active (5.27 minutes/day). Among the girls, those considered most active spent a mean time in MVPA of 48.29 minutes/day, while the least active ones, in average, remained only 0.47 minute/day in this category of physical activity. Therefore, both most active and least active adolescents in the groups of daily physical activity as well as the EEDaily were represented in the sample selected for the study.
Another trial of justification which could partly explain the differences observed between the magnitude of the physical activity-plasma concentrations associations of adults and adolescents is related to lower variations found in the lipid lipoproteins concentrations of younger subjects. The expectation is that the proportion of adolescents who will present altered values of plasma lipid lipoproteins is significantly lower than of adults; thus, the impact of the daily physical activity practice in the plasma lipid lipoproteins amounts should be, to begin with, due to their dimensions being already close to healthy values.
Conversely, the justification which most fulfills the differences observed between the magnitude of physical activity-plasma lipid lipoproteins concentrations associations of adults and adolescents may be related to the fact that metabolic adaptations linked with the control of the plasma lipid lipoproteins concentrations in the performance of physical exertion result from complex interactions involving hormones, enzymes and receptors and therefore, particularly occur in the young body, differently from the adult's(46). In this context, theoretically, it is assumed that the significant associations observed in adults may not be the cause, with the participation therefore of additional effects from other non-identified metabolic variables, affecting hence, the impact of the daily physical activity practice in the plasma concentrations of lipid lipoproteins, which is not apparent in adolescents due to their lack of total biological maturation. Such fact may probably suggest that the conception that the consequences concerning least daily physical activity practice in the plasma concentrations of lipid lipoproteins may take some time to be identified.
New data presented in the present study are related with the impact of the EEDaily, an indicator strongly accepted concerning the daily physical activity practice(16,25,34,39), in the atherogenic risk lipid lipoprotein profile, established through the cut-points clinically relevant for adolescents(33). When using a conventional statistical framework aimed to identify associations between physical activity and plasma lipid lipoproteins concentrations, which is the case of the correlation coefficients, it is possible to identify that some more physically active subjects may present dyslipoproteinaemias, and, on the other hand, some less physically active subjects may present a desirable lipid lipoprotein profile. Therefore, in order to estimate the relative risk of adolescents classified in decreasing groups of EEDaily who present compromising plasma lipid lipoproteins concentrations, binary logistic regression analysis was applied. In summary, with the dimensions of the OR values, higher relative risk was observed for adolescents who present atherogenic risk lipid lipoprotein profile with decrease in EEDaily. Nevertheless, due to the reliability intervals breadth equivalent to the calculated values of OR, only girls and boys with low EEDaily (< 35.1 and < 35.2 kcal/kg/day respectively) demonstrated significant relative risk in statistical language and approximately of two-fold more (girls OR = 2.18; 95% IC 1.31-3.11; boys OR = 1.96; 95% IC 1.6-2.75) of presenting HDL-C values < 35 mg/dl compared with girls and boys with high EEDaily (> 37.8 among boys and > 39.6 kcal/kg/day among girls).
The results of the present study must be interpreted with some limitations. First, the data concerning the daily physical activity practice as well as the EEDaily were obtained through a retrospective instrument of self-record of the daily activities, which was filled by the adolescents themselves. Although the validity and reproducibility indications of the instrument are available and fulfill the proposed acceptance criteria(39), other measurements concerning physical activity as well as the EEDaily, which is the case of the accelerometers, may offer more robust and conclusive results. Second, eating habits of the adolescents analyzed in the study have not been considered; besides that, higher ingestion of food rich in total and saturated fat may interfere in the plasma lipid lipoproteins concentrations(28,47-48), the same situation happening with smoking(28,49-50). Moreover, the sample framework applied, involving non-randomly selection of the subjects and with specific social, economical and cultural features, may weaken the external validity of the study as well as make its results' generalization difficult.
In conclusion, the found results suggest that high EEDaily is associated with HDL-C concentrations also high in adolescents of both sexes. Concerning the difficulties to obtain reliable indicators for daily physical activity practice in young populations, especially concerning the energy expenditure of the daily activities, a better understanding on the complex dose-response relationship between physical activity and plasma lipid lipoproteins concentrations is important for the proposition of physical activity practice recommendations aimed to prevention of dyslipoproteinemias in young subjects and in adult ages in the future.
1. Ventura SJ, Anderson RN, Smith BL. Births and deaths: preliminary data for 1997. National vital statistics reports. Volume 47, Number 4. Hyattsville: National Center for Health Statistics, 1998. [ Links ]
2. Sytkowsky PA, Kannel WB, D'Agostino RB. Changes in risk factors and the decline in mortality from cardiovascular disease. N Engl J Med. 1990;322:1635-41. [ Links ]
3. Ministério da Saúde. Estatística de Mortalidade 1989. Brasília, 1993. [ Links ]
4. Lessa I. Introdução à epidemiologia das doenças cardiovasculares no Brasil. In: Lessa I. O adulto brasileiro e as doenças da modernidade. Epidemiologia das doenças crônicas não-transmissíveis. São Paulo: Editora Hucitec, 1998;73-6. [ Links ]
5. Buss PM. Assistência hospitalar no Brasil (1984-1991): uma análise preliminar baseada no Sistema de Informação Hospitalar do SUS. Inf Epidemiol SUS. 1993; 2:5-44. [ Links ]
6. Stary HC. The sequence of cell and matrix changes in atherosclerotic lesions of coronary arteries in the first forty years of life. Eur Heart J. 1990;11(suppl E):3019. [ Links ]
7. Berenson GS, Wattigney WA, Tracy RE, Newman WP, Srinivasan SR, Webber LS, et al. Atherosclerosis of the aorta and coronary arteries and cardiovascular risk factors in persons aged 6 to 30 years studied at necropsy: The Bogalusa Heart Study. Am J Cardiol. 1992;70:851-8. [ Links ]
8. Strong PJ, Malcom TG, McMahan AC, Tracy RE, Newman WP, Herderick EE, et al. Prevalence and extent of atherosclerosis in adolescents and young adults. JAMA. 1999;281:727-35. [ Links ]
9. Berenson GS, Srinivasan SR, Bao W, Newman WP, Tracy RE, Wattigney WA. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. N Engl J Med. 1998;338:1650-6. [ Links ]
10. Walter HJ, Hoffman A, Vaughan RD, Wynder EL. Modification of risk factors for coronary heart disease. Five-year results of a school-based intervention trial. N Engl J Med. 1988;318:1093-100. [ Links ]
11. Kimm SY, Payne GH, Styanou MP, Waclawiw MA, Lichtenstein C. National trends in the management of cardiovascular disease risk factors in children: II NHLBI Survey of Primary Care Physicians. Pediatrics. 1998;102:E50. [ Links ]
12. Gidding SS. Preventive pediatric cardiology: tobacco, cholesterol, obesity and physical activity. Pediatr Clin North Am. 1999;46:253-62. [ Links ]
13. Jacobs DR, Mebane IL, Bongdiwala SL, Criqui MH, Tyroler HA. High density lipoprotein cholesterol as a predictor of cardiovascular disease mortality in men and women: the follow-up study of the lipid research clinics prevalence study. Am J Epidemiol. 1990;131:32-47. [ Links ]
14. Stampfer MJ, Sacks FM, Salvini S, Willett WC, Hennekens CH. A prospective study of cholesterol, apolipoproteins, and the risk of myocardial infarction. N Engl J Med. 1991;325:373-81. [ Links ]
15. Manninen V, Tenkanen L, Koskinen P, Huttunen JK, Mänttäri M, Heinonen OP. Joint effects of serum triglyceride and LDL cholesterol and HDL cholesterol concentration on coronary heart disease risk in the Hensinki Heart Study. Circulation. 1992;85:37-45. [ Links ]
16. Caspersen CJ, Nixon PA, DuRant RH. Physical activity epidemiology applied to children and adolescents. Exerc Sci Sports Rev. 1998;26:341-403. [ Links ]
17. Armstrong N, Simons-Morton B. Physical activity and blood lipids in adolescents. Pediatr Exerc Sci. 1994;6:381-405. [ Links ]
18. Despres JP, Bouchard C, Malina RM. Physical activity and coronary heart disease risk factors during childhood and adolescents. Exerc Sport Sci Rev. 1990; 18:243-61. [ Links ]
19. Tolfrey K, Jones AM, Campbell IG. The effects of aerobic exercise training on the lipid-lipoprotein profile of children and adolescents. Sports Med. 2000;29: 99-112. [ Links ]
20. Katzmarzyk PT, Malina RM, Bouchard C. Physical activity, physical fitness, and coronary heart disease risk factors in youth: The Quebec Family Study. Prev Med. 1999;29:555-62. [ Links ]
21. Guerra S, Duarte J, Mota J. Physical activity and cardiovascular disease risk factors in schoolchildren. Eur Phys Educ Rev. 2001;7:269-81. [ Links ]
22. Boreham CA, Twisk J, Savage MJ, Cran GW, Strain JJ. Physical activity, sports participation, and risk factors in adolescents. Med Sci Sport Exerc. 1997;29: 788-93. [ Links ]
23. Schmidt GJ, Walkuski JJ, Stensel DJ. The Singapore Youth Coronary Risk and Physical Activity Study. Med Sci Sports Exerc. 1998;30:105-13. [ Links ]
24. Raitakari OT, Taimela S, Porkka KVK, Telama R, Valimaki I, Akerblom HK, et al. Associations between physical activity and risk factors for coronary artery disease: The Cardiovascular Risk in Young Finns Study. Med Sci Sports Exerc. 1997; 29:1055-61. [ Links ]
25. Eisenmann JC, Katzmarzyk PT, Perusse L, Bouchard C, Malina RM. Estimated daily energy expenditure and blood lipids in adolescents: The Quebec Family Study. J Adolesc Health. 2003;33:147-53. [ Links ]
26. Guedes DP, Guedes JERP, Barbosa DS, Oliveira JA. Níveis de prática de atividade física habitual em adolescentes. Rev Bras Med Esporte. 2001;7:187-99. [ Links ]
27. Guedes DP, Guedes JERP, Barbosa DS, Oliveira JA. Aptidão física relacionada à saúde e fatores de risco predisponentes às doenças cardiovasculares em adolescentes. Rev Port Ciências Desporto. 2002;5:31-46. [ Links ]
28. Guedes DP, Guedes JERP, Barbosa DS, Oliveira JA, Stanganelli LCR. Fatores de risco cardiovasculares em adolescentes: indicadores biológicos e comportamentais. Arq Bras Cardiol. 2006;86:439-50. [ Links ]
29. ANEP. Critério de Classificação Econômica Brasil. São Paulo: Associação Nacional de Empresas de Pesquisa, 2000. [ Links ]
30. Tanner JM. Growth at adolescence. 2nd ed. Oxford: Blackwell Scientific Publications, 1962. [ Links ]
31. Gordon CC, Chumlea WC, Roche AP. Stature, recumbent length, and weight. In: Lohman TG, Roche AP, Martorell R, editors. Anthropometric standardization reference manual. Champaign, Illinois: Human Kinetics, 1988;3-8. [ Links ]
32. Friedewald WT, Levy RI, Frederickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of preparative ultracentrifuge. Clin Chem. 1972;18:499-502. [ Links ]
33. Sociedade Brasileira de Cardiologia. III Diretrizes Brasileiras sobre Dislipidemias e Diretrizes de Prevenção da Aterosclerose do Departamento de Aterosclerose da Sociedade Brasileira de Cardiologia. Arq Bras Cardiol. 2001;77:supl 3. [ Links ]
34. Bouchard C, Tremblay A, Leblanc C, Lortie G, Sauard R, Therialt G. A method to assess energy expenditure in children and adults. Am J Clin Nutr. 1983;37:461-7. [ Links ]
35. Shephard RJ, Bouchard C. Relationship between perceptions of physical activity and health-related fitness. J Sports Med Phys Fitness. 1995;35:149-58. [ Links ]
36. Huang Y, Malina RM. Physical activity and correlates of estimated energy expenditure in Taiwanese adolescents 12-14 years of age. Am J Hum Biol. 1996; 8:225-36. [ Links ]
37. Katzmarzyk PT, Malina RM, Song TMK, Bouchard C. Physical activity and health-related fitness in youth: a multivariate analysis. Med Sci Sport Exerc. 1998;30: 709-14. [ Links ]
38. Bratteby LE, Sandhagen B, Lötborn M, Samuelson G. Daily energy expenditure and physical activity assessed by an activity diary in 374 randomly selected 15-year-old adolescents. Eur J Clin Nutr. 1997;51:592-600. [ Links ]
39. Bratteby LE, Sandhagen B, Fan H, Samuelson G. A 7-day activity diary for assessment of daily energy expenditure validated by the doubly labeled water method in adolescents. Eur J Clin Nutr. 1997;51:585-91. [ Links ]
40. Marrugat J, Elosua R, Covas MI, Molina L, Rubiés-Prat J. Amount and intensity of physical activity, physical fitness and serum lipids in men. Am J Epidemiol. 1996;143:562-9. [ Links ]
41. Forrest KY, Bunker CH, Kriska AM, Ukoli FA, Huston SL, Markovi CN. Physical activity and cardiovascular risk factors in a developing population. Med Sci Sports Exerc. 2001;33:1598-604. [ Links ]
42. Guedes DP, Guedes JERP. Atividade física, aptidão cardiorrespiratória, composição da dieta e fatores de risco predisponentes às doenças cardiovasculares. Arq Bras Cardiol. 2001;77:243-50. [ Links ]
43. Durstine JL, Grandjean PW, Davis PG, Ferguson MA, Alderson NL, DuBose KD. Blood lipid and lipoprotein adaptations to exercise: a quantitative analysis. Sports Med. 2001;31:1033-62. [ Links ]
44. Biddle S, Sallis JF, Cavill N. Policy framework for young people and health-enhancing physical activity. In: Biddle S, Sallis JF, Cavill N, editors. Young and active? Young people and health-enhancing physical activity: evidence and implications. London: Health Education Authority, 1998;3-16. [ Links ]
45. Twisk JWR. Physical activity guidelines for children and adolescents: a critical review. Sports Med. 2001;31:617-27. [ Links ]
46. Boreham C, Riddoch C. The physical activity, fitness and health of children. J Sports Sci. 2001;19:915-29. [ Links ]
47. Grundy SM, Denke MA. Dietary influences on serum lipids and lipoproteins. J Lipid Res. 1990;31:1149-72. [ Links ]
48. Pedridou E, Malamou H, Doxiadis S, Pantelakis S, Kanellopoulou G, Toupadaki N, et al. Blood lipids in Greek adolescents and their relation to diet, obesity and socioeconomic factors. Ann Epidemiol. 1995;5:286-91. [ Links ]
49. Graig WY, Palomaki GE, Johnson M, Haddow JE. Cigarette smoking-associated changes in blood lipid and lipoprotein levels in the 8-to-19-year-old age group: a meta-analysis. Pediatrics. 1990;85:155-8. [ Links ]
50. Paulus D, Saint-Remy A, JeanJean M. Smoking during adolescence: association with other cardiovascular risk factors in Belgian adolescents. Eur J Public Health. 2000;10:39-44. [ Links ]
Dartagnan Pinto Guedes
Rua Ildefonso Werner, 177, Condomínio Royal Golf
86055-545 Londrina, PR
E-mail: darta@ sercomtel.com.br
Received in 1/3/06.
Final version received in 3/8/06.
Approved in 25/10/06.
All the authors
declared there is not any potential conflict of interests regarding this article.
* Universidade Estadual de Londrina, Paraná. Apoio do MCT/CNPq.