Acessibilidade / Reportar erro

Increased ApoB/ApoA1 ratio is associated with excess weight, body adiposity, and altered lipid profile in children Please cite this article as: Castro AP, Hermsdorff HH, Milagres LC, Albuquerque FM, Filgueiras MS, Rocha NP, et al. Increased ApoB/ApoA1 ratio is associated with excess weight, body adiposity, and altered lipid profile in children. J Pediatr. 2019;95:238-46.

Abstract

Objective:

To investigate ApoB/ApoA1 ratio and its association with cardiovascular risk factors in children.

Methods:

Cross-sectional study with 258 children aged 8 and 9 years old, enrolled in all urban schools in the city of Viçosa-MG. Anthropometric and body composition assessment, as well as biochemical profile of the children was performed. Socioeconomic variables and sedentary lifestyle were evaluated through a semi-structured questionnaire.

Results:

Many children had excess weight (35.2%), abdominal adiposity (10.5%), and body fat (15.6%), as well as increased ApoB/ApoA1 ratio (14.7%), total cholesterol (51.8%), and triglycerides (19.8%). Children with excess weight and total and central fat had a higher prevalence of having a higher ApoB/ApoA1 ratio, as well as those with atherogenic lipid profile (increased LDL-c and triglycerides and low HDL-c). A direct association was found between the number of cardiovascular risk factors and the ApoB/ApoA1 ratio (p = 0.001), regardless of age and income.

Conclusion:

The increased ApoB/ApoA1 ratio was associated with excess weight, body adiposity (total and central), and altered lipid profile in children. Children with a higher number of cardiovascular risk factors had higher ApoB/ApoA1 ratio, in both genders.

KEYWORDS
Children; Dyslipidemias; Adiposity; Apolipoproteins

Resumo

Objetivo:

Investigar a razão ApoB/ApoA1 e sua relação com fatores de risco cardiovascular em crianças.

Métodos:

Estudo transversal com 258 crianças de 8 e 9 anos, matriculadas em todas as escolas urbanas de Viçosa-MG. Foi feita avaliação antropométrica, da composição corporal e bioquímica das crianças. As variáveis socioeconômicas e o sedentarismo foram avaliados por questionário semiestruturado.

Resultados:

Muitas crianças apresentaram excesso de peso (35,2%), de adiposidade abdominal (10,5%) e de gordura corporal (15,6%), bem como a razão ApoB/ApoA1 (14,7%), colesterol-total (51,8%) e triglicerídeos (19,8%) aumentados. Crianças com excesso de peso e de gordura total e central apresentaram maiores prevalências de maior razão ApoB/ApoA1, bem como as com perfil lipídico aterogênico (LDL-c e triglicerídeos aumentados e baixo HDL-c). Foi encontrada associação direta entre o número de fatores de risco cardiovascular e a razão ApoB/ApoA1 (p = 0,001), independente da idade e renda.

Conclusão:

A razão ApoB/ApoA1 aumentada esteve associada ao excesso de peso, de adiposidade corporal (total e central) e ao perfil lipídico alterado nas crianças. As crianças com maior número de fatores de risco cardiovascular apresentaram maior razão ApoB/ApoA1, em ambos os sexos.

PALAVRAS-CHAVE
Crianças; Dislipidemias; Adiposidade; Apolipoproteínas

Introduction

Exposure to the atherogenic lipid profile may induce changes in the arteries and contribute to atherosclerosis development, which may start in childhood.11 Hong MH. Atherosclerotic cardiovascular disease beginning in childhood. Korean Circ J. 2010;40:1-9. Studies have shown that elevated LDL cholesterol levels in children predict an increase in the intima-media layer thickness of the arteries in adults.22 Raitakari OT, Juonala K, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascuar Risk in Young Finns Study. JAMA. 2003;290:2277-83. Considering this fact, it is important to measure serum lipid levels in childhood as a strategy aimed to prevent cardiovascular diseases and atherosclerosis.

The ratio between pro-atherogenic (containing ApoB) and anti-atherogenic particles (containing ApoA1) may be associated with cardiovascular diseases.33 Barter PJ, Ballantyne CM, Carmena R, Cabezas MC, Chapman MJ, Couture P, et al. Apo B versus cholesterol in estimating cardiovascular risk and in guiding therapy: report of the thirty-person/ten-country panel. J Intern Med. 2006;259:247-58. ApoA1 is the main protein of the HDL-c particle, responsible for stimulating reverse cholesterol transport, removing excess from the tissues and redirecting it to the liver. Moreover, it can inhibit LDL-c oxidation, helps in the removal of toxic products, and it has anti-inflammatory properties.44 Navab M, Reddy ST, Van Lenten BJ, Fogelman AM. HDL and cardiovascular disease: atherogenic and atheroprotective mechanisms. Nat Rev Cardiol. 2011;8:222-32. In turn, ApoB is part of the atherogenic lipid fractions, including LDL-c, an intermediate-density lipoprotein (IDL), very low-density lipoprotein (VLDL), and lipoprotein (a).55 Kappelle PJ, Gansevoort RT, Hillege JL, Wolffenbuttel BH, Dullaart RP. Apolipoprotein B/A-I and total cholesterol/high-density lipoprotein cholesterol ratios both predict cardiovascular events in the general population independently of nonlipid risk factors, albuminuria and C-reactive protein. J Intern Med. 2011;269:232-42.

Thus, the ApoB/ApoA1 ratio has been investigated as a possible cardiometabolic predictor for atherosclerosis in adults.66 Qin G, Tu J, Zhang C, Tang X, Luo L, Wu J, et al. The value of the apoB/apoAI ratio and the non-HDL-C/HDL-C ratio in predicting carotid atherosclerosis among Chinese individuals with metabolic syndrome: a cross-sectional study. Lipids Health Dis. 2015;14:24. In children, studies have shown that the ApoB/ApoA1 ratio is associated with metabolic syndrome components, such as increased waist circumference and blood pressure, low HDL-c, and high triglycerides.77 Retnakaran R, Zinman B, Connelly PW, Harris SB, Hanley AJ. Nontraditional cardiovascular risk factors in pediatric metabolic syndrome. J Pediatr. 2006;148:176-82.,88 Savas Erdeve S, Simsek E, Dallar Y, Biyikli Z. Utility of ApoB/ApoA1 ratio for the prediction of cardiovascular risk in children with metabolic syndrome. Indian J Pediatr. 2010;77:1261-5. Additionally, lifestyle changes in obese children, such as sedentary lifestyle, seem to influence the higher ApoB/ApoA1 ratio.99 Ben Ounis O, Elloumi M, Makni E, Zouhal H, Amri M, Tabka Z, et al. Exercise improves the ApoB/ApoA-I ratio, a marker of the metabolic syndrome in obese children. Acta Paediatr Int J Paediatr. 2010;99:1679-85.

However, there is a gap in the knowledge on the association between the ApoB/ApoA1 ratio and cardiovascular risk factors in children, with this subject being scarcely studied in Brazil1010 Albuquerque MN, Diniz AS, Arruda IK. Apolipoproteins and their association with cardiometabolic risk biomarkers in adolescents. Nutr Hosp. 2015;32:2674-83. and in other countries in this age group.77 Retnakaran R, Zinman B, Connelly PW, Harris SB, Hanley AJ. Nontraditional cardiovascular risk factors in pediatric metabolic syndrome. J Pediatr. 2006;148:176-82.,88 Savas Erdeve S, Simsek E, Dallar Y, Biyikli Z. Utility of ApoB/ApoA1 ratio for the prediction of cardiovascular risk in children with metabolic syndrome. Indian J Pediatr. 2010;77:1261-5.

As the increased ApoB/ApoA1 ratio may contribute to the occurrence of atherosclerotic events in adult life, the aim of this study was to investigate the ApoB/ApoA1 ratio and its association with cardiovascular risk factors in children enrolled in urban schools in the municipality of Viçosa, state of Minas Gerais, Brazil.

Methods

Study population and sampling process

This is a cross-sectional study conducted between May and December of 2015, with a sample of 258 children aged 8 and 9 years, enrolled in all public (n = 17) and private (n = 7) schools in the urban area of the municipality of Viçosa, Minas Gerais, Brazil. This study is part of a larger project entitled "Vitamin D in childhood: intake, serum levels, and association with cardiovascular risk factors," from the Schoolchildren's Health Assessment Survey (Pesquisa de Avaliação da Saúde do Escolar - PASE).

The sample was calculated using the OpenEpi statistical program (Open Source Epidemiologic Statistics for Public Health, version 3.01), considering the prevalence of 50% for multiple outcomes, tolerable error of 5%, plus 10% losses and 10% confounding factors, totaling a sample size of 366 children.

For the evaluation of the ApoB/ApoA1 ratio, a subsample of 258 children was used, since the blood volume collected was not enough for the ApoB and ApoA1 measurement in all the children from the original project. It is worth mentioning that the final sample did not differ from the original sample in relation to gender, age, and cardiovascular risk factors.

A stratified random sampling process was performed on the schoolchildren, in which the number of children to be sampled in each school was related to the weighting by school, according to its size. Subsequently, the children were selected by drawing lots from a random number table, until the number of students needed per school was completed.

After contacting the parents, the children were invited to participate in the study. Those who used medications that interfered with glucose and/or lipid metabolism were not included in the study.

Data collection

Weight and height were measured using an electronic digital scale (Tanita®, model BC 553, IL, USA), with a capacity of 150 kilograms and a sensitivity of 100 grams. Weight was measured with the individuals in the orthostatic position, barefoot, and wearing light clothing. Height was measured using a portable vertical stadiometer (Alturexata®, MG, Brazil), measuring 2 meters, graduated in centimeters and subdivided into millimeters. Body mass index (BMI) was calculated based on the obtained values. Nutritional status was evaluated based on BMI/age, and children with z-score ≥−2 and <1 were considered as having normal weight, whereas those with z-score ≥1 were considered as having excess weight (overweight or obesity).1111 World Health Organization. Growth reference data for 5-19 years. Geneva: WHO; 2007.

Waist circumference (WC) was measured at the midpoint between the iliac crest and the last rib using a flexible, inelastic measuring tape, graduated in centimeters and subdivided into millimeters. Excessive abdominal adiposity was considered in the presence of values above the 90th percentile according to age and gender.1212 Filho VC, Fagundes RR, de Campos W. Anthropometric indices among schoolchildren from a municipality in Southern Brazil: a descriptive analysis using the LMS method. Rev Paul Pediatr. 2014;32:333-41. The waist-to-height ratio (WHtR) was calculated by dividing the waist measurement (cm) by height (cm), and values ≥ 0.5 were used to classify excess abdominal adiposity.1313 Ashwell M, Hsieh SD. Six reasons why the waist-to-height ratio is a rapid and effective global indicator for health risks of obesity and how its use could simplify the international public health message on obesity. Int J Food Sci Nutr. 2005;56:303-7.

The total and central body fat (android fat [AF] and gynoid fat [GF]) was evaluated in the supine position, using the dual-energy X-ray absorptiometry (DXA) method in the Diagnostic Imaging Sector of the Health Division of Universidade Federal de Viçosa. The AF comprises the region between the ribs and the pelvis, with the upper marking being made at 20% of the distance from the iliac crest and neck, and the lower marking being made above the pelvis. The gynoid region measurements included the hip, thighs, and overlaps of the leg and trunk regions, with the upper marking being made below the iliac crest at a distance of 1.5 times the android height.1414 Mazes RB, Barden HS, Hanson J. Dual-energy X-ray absorptiometry for total body and regional bone mineral and soft-tissue composition. Am J Clin Nutr. 1990;51:1106-12. Excess body fat was classified with values ≥85th percentile for age and gender, according to McCarthy et al.1515 McCarthy HD, Cole TJ, Fry T, Jebb SA, Prentice AM. Body fat reference curves for children. Int J Obes (Lond). 2006;30:598-602.

The neck circumference (NC) was assessed in the Frankfurt horizontal plane, with the child standing erect, using an inextensible measuring tape (TBW®, SP, Brazil), just below the laryngeal prominence in the neck, perpendicular to the largest axis of the neck. Minimal pressure was exerted to allow full contact of the tape with the skin. The increased values were classified according to the cutoff points proposed by Nafieu et al.1616 Nafiu OO, Burke C, Lee J, Voepel-Lewis T, Malviya S, Tremper KK. Neck circumference as a screening measure for identifying children with high body mass index. Pediatrics. 2010;126:e306-10.

Waist circumference (WC), waist-to-height ratio (WHtR), neck circumference, and android/gynoid fat ratio were considered indicators of central adiposity, whereas BMI was the indicator of total adiposity.

Blood pressure (BP) was measured three times, with the child in the sitting position with five-minute intervals, considering the mean value for BP classification according to the 7th Brazilian Guideline of Arterial Hypertension. High blood pressure was classified as systolic (SBP) and/or diastolic (DBP) blood pressure above the 95th percentile, according to age, gender, height percentile, on at least three different occasions.1717 Malachias MV, Souza WK, Plavinik FL, Rodrigues CI, Brandão AA, Neves MF, et al. VII Diretriz brasileira de hipertensão arterial. Arq Bras Cardiol. 2016;107:S1-83. BP was measured using the automatic device (Omron®, HEM 907, IL, USA).

Venous blood samples were collected between eight and ten a.m., after overnight fasting, and centrifuged at 1000 × g for 10 min at 4 °C. Levels of total cholesterol (TC), HDL-c, LDL-c, triglycerides (TG), and C-reactive protein (CRP) were measured using the colorimetric enzymatic method using a commercial kit (Bioclin®, MG, Brazil) in an automated analyzer (BS-200 Mindray®, China) at the Laboratory of Clinical Analyses (LAC) of the Nutrition and Health Department of Universidade Federal de Viçosa (UFV). Non-HDL-cholesterol was estimated by the formula: Non-HDL-c = TC-HDL-c. The lipid profile classification was performed according to the Brazilian Society of Cardiology.1818 Xavier HT, Izar MC, Faria Neto JR, Assad MH, Rocha VZ, Sposito AC, et al. V Diretriz brasileira de dislipidemias e prevenção da aterosclerose. Arq Bras Cardiol. 2013;101:S1-22. The serum levels of leptin, ApoA1, ApoB and homocysteine were analyzed through commercial ELISA kits, nephelometry (Beckman Coulter, CA, USA), and chemiluminescence (standardized protocols from Diagnóstico Brasil), respectively. Intra-assay variations were 4% for both ApoA1 and ApoB. Because there were no cutoff points for the classification of the ultra-sensitive C-reactive protein, leptin, homocysteine, ApoA1 and ApoB in the studied age group, values ≥85th percentile were considered at risk.

A semi-structured questionnaire was applied personally by trained interviewers to parents or guardians to assess sociodemographic variables, such as gender and family income per capita, and total time of physical activity (TPA). The children were classified as active when they performed 300 minutes or more of moderate or vigorous physical activity weekly and were considered inactive when they performed less than 300 minutes, as classified by the National School Health Survey.1919 Brasil. Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional de Saúde do Escolar (PeNSE) - 2012. Rio de Janeiro: IBGE; 2013. Available from: http://biblioteca.ibge.gov.br/visualizacao/livros/liv64436.pdf [cited 30.10.15].
http://biblioteca.ibge.gov.br/visualizac...
It is important to mention that none of the girls had experienced menarche at the time of this study.

Statistical analysis

The normality of the data was verified by the Kolmogorov-Smirnov test. Pearson's chi-squared test and Fisher's exact test were used to compare the prevalence of cardiovascular risk factors between genders and ApoB/ApoA1 values.

Poisson regression was performed with crude and adjusted robust variance to analyze the associations between ApoB/ApoA1 ratio and age, time of physical activity, anthropometric variables, body composition, and clinical and biochemical variables. Variables with a significance level ≤0.20 were included in the regression model. According with the linear regression analysis, the ApoB/ApoA1 ratio was also evaluated according to the number of cardiovascular risk factors (TPA, WHtR, CT, HDL-c, LDL-c, TG, non-HDL cholesterol, AF/GF, excess weight). Statistical analyses were performed using the software SPSS® (SPSS for Windows, Version 16.0., Chicago, USA) and Stata (Stata Statistical Software: Release 10, College Station, TX, USA). Values of p < 0.05 were considered statistically significant.

Ethical aspects

This study was carried out in accordance with the guidelines defined in the Declaration of Helsinki and all procedures involving human subjects were approved by the Human Research Ethics Committee of Universidade Federal de Viçosa (UFV; Opinion No. 663.171/2014). Informed consent was obtained from all parents or legal guardians, after they were informed about the study objectives.

Results

A total of 258 children were evaluated, 56% females. Many children had excess weight (35.2%), abdominal adiposity (10.5%), and body fat (15.6%), as well as increased ApoB/ApoA1 ratio (14.7%), serum levels of total cholesterol (51.8%), and triglycerides (19.8%). Additionally, 8.9%, 17.9%, and 24% of the children had increased serum levels of ultrasensitive CRP, leptin, and homocysteine, respectively. The prevalence of reduced serum ApoA1 and HDL-c levels was higher in boys than in girls. In turn, girls had a higher prevalence of increased serum levels of triglycerides and leptin (Table 1).

Table 1
Distribution of the children's age, physical activity time, anthropometric, body composition, and biochemical variables, according to gender; Viçosa, MG, Brazil, 2015.

Children with a higher ApoB/ApoA1 ratio were more inactive, had increased WHtR, excess weight, and altered lipid profile (Table 2).

Table 2
Distribution of children's physical activity time, anthropometric, body composition, and biochemistry variables, according to ApoB/ApoA1 ratio; Viçosa, MG, Brazil, 2015.

In regression models, children with excess of weight and indicators of total and central adiposity (WHtR, waist circumference, body fat, and AF/GF) had a higher prevalence of higher ApoB/ApoA1 ratio (≥85th percentile), regardless of gender, age, and income. Interestingly, children with an atherogenic lipid profile increased (total cholesterol, LDL-c, non-HDL-c, and triglycerides and low HDL-c) also had higher prevalence of a higher ApoB/ApoA 1 ratio, regardless of gender, age, income, and body fat (Table 3).

Table 3
Association between the increased ApoB/ApoA1 ratio (dependent variable) and anthropometric, body composition, and biochemical variables in children; Viçosa, MG, Brazil, 2015.

Children with a higher number of cardiovascular risk factors had a higher ApoB/ApoA1 ratio, regardless of age and income, in both girls and boys (Fig. 1).

Figure 1
Association between the ApoB/ApoA1 ratio and the number of cardiovascular risk factors in children, according to gender. Mean (95% CI), Linear regression adjusted for age and income; Viçosa, MG, Brazil, 2015.

Discussion

In the present study, a higher ApoB/ApoA1 ratio was associated with excess body weight and adiposity (total and central), as well as an altered lipid profile in children. There was a direct association between the number of cardiovascular risk factors and the ApoB/ApoA1 ratio, regardless of age and income.

In children and adolescents from Canada, an association was also found between the increased ApoB/ApoA1 ratio and excess weight.77 Retnakaran R, Zinman B, Connelly PW, Harris SB, Hanley AJ. Nontraditional cardiovascular risk factors in pediatric metabolic syndrome. J Pediatr. 2006;148:176-82. In a study carried out in the United States, children and adolescents with normal weight and abdominal obesity (WHtR ≥ 0.5) had a higher number of cardiovascular risk factors, such as hypertension, increased levels of triglycerides, and LDL-c, as well as insulin resistance when compared to those without abdominal obesity.2020 Mokha JS, Srinivasan SR, Dasmahapatra P, Fernandez C, Chen W, Xu J, et al. Utility of waist-to-height ratio in assessing the status of central obesity and related cardiometabolic risk profile among normal weight and overweight/obese children: the Bogalusa Heart Study. BMC Pediatr. 2010;10:73. In Brazilian children and adolescents, the ApoB/ApoA1 ratio was associated with more than one cardiovascular risk factor (BMI, WC, WHtR, HDL-c, and triglycerides), corroborating the present findings.1010 Albuquerque MN, Diniz AS, Arruda IK. Apolipoproteins and their association with cardiometabolic risk biomarkers in adolescents. Nutr Hosp. 2015;32:2674-83.

Excess central adiposity has been considered the main component of the metabolic syndrome and is strongly associated with dyslipidemia and an increase in the number of cardiovascular risk factors, both in adults2121 Cuschieri S, Vassallo J, Calleja N, Camilleri R, Borg A, Bonnici G, et al. Prevalence of obesity in Malta. Obes Sci Pract. 2016;2:466-70. and children.2222 Vásquez FD, Corvalám CL, Uauy RE, Kain JA. Anthropometric indicators as predictors of total body fat and cardiometabolic risk factors in Chilean children at 4, 7 and 10 years of age. Eur J Clin Nutr. 2017;71:536-43. Excess central adiposity may lead to an increased ApoB/ApoA1 ratio through different mechanisms: (1) decreased hepatic LDL receptor and/or decreased lipoprotein lipase (LPL) activity, both important for the removal of remaining chylomicrons from the circulation containing ApoB molecules2323 Cooper AD. Hepatic uptake of chylomicron remnants. J Lipid Res. 1997;38:2173-92.,2424 Morita SY. Metabolism and modification of apolipoprotein B-containing lipoproteins involved in dyslipidemia and atherosclerosis. Bio Pharm Bull. 2016;39:1-24.; (2) increased adipokine secretion by adipose tissue in obese individuals; (3) reduction in serum HDL-c levels, the main characteristic of dyslipidemia associated with central obesity.2525 Chan CD, Barret HP, Watts GF. Dyslipidemia in visceral obesity. Am J Cardiovasc Drugs. 2004;4:227-46. In obese individuals, the low HDL-c level is a consequence of the increase in HDL-c catabolism, thus favoring a decrease in ApoA1 levels.2626 Lin GM, Liu K, Colangelo LA, Lakoski GS, Tracy RP, Greenlan P. Low-density lipoprotein cholesterol concentrations and association of high-sensitivity C-reactive protein concentrations with incident coronary heart disease in the multi-ethnic study of atherosclerosis. Am J Epidemiol. 2016;183:46-52. Moreover, body fat accumulation is one of the main factors that can modify small-density LDL expression, because in both adults and children, abdominal obesity is associated with the lower density and the smaller particle size of LDL-c.2727 Miyashita M, Okada T, Kuromori Y, Harada K. LDL particle size, fat distribution and insulin resistance in obese children. Eur J Clin Nutr. 2006;60:416-20.

It is worth mentioning that, in this study, children with three or more cardiovascular risk factors had higher ApoB/ApoA1 ratio values in both genders. This direct association suggests the possible influence of pro-atherogenic particles (containing ApoB) and anti-atherogenic particles (containing ApoA1) on cardiovascular diseases, as there is an increase in the number of risk factors. To date, no similar studies have been found, and thus, the results indicate the precocity of this association occurring as early as in childhood.

The present study showed no association between serum levels of leptin, CRP, and homocysteine with ApoB/ApoA1 ratio. One possible hypothesis is that these markers participate in the cardiometabolic risk through a pathway other than the ApoB/ApoA1 ratio, with these being recognized as important indicators of subclinical inflammation, while apolipoproteins are involved in lipid metabolism.2828 Navarro P, de Dios O, Gavela-Pérez T, Jois A, Garcés C, Soriano-Guillém L. High-sensitivity C reactive protein and leptin levels related to body mass index changes throughout childhood. J Pediatr. 2016;178:178-82. However, to date, no other studies have been found that evaluated the association between a higher ApoB/ApoA1 ratio and these cardiometabolic markers, as well as the mechanisms involved.

One limitation of this study is the fact that it has a cross-sectional design, which does not allow for establishing cause-and-effect associations. It is important to emphasize that few Brazilian studies have evaluated non-classical cardiovascular markers, such as the ApoB/ApoA1 ratio, in healthy prepubertal children. As these alterations may contribute to the onset of atherosclerotic disease, early identification is crucial for the planning and implementation of public health policies, with actions directed at food and nutritional education and the stimulation of physical activity. These actions may contribute to reducing future mortality from cardiovascular diseases and other obesity-related diseases.

In summary, a higher ApoB/ApoA1 ratio was associated with excess weight, body adiposity (total and central), and altered lipid profile in children. Children with a higher number of cardiovascular risk factors had higher ApoB/ApoA1 ratio, regardless of age and income.

  • Please cite this article as: Castro AP, Hermsdorff HH, Milagres LC, Albuquerque FM, Filgueiras MS, Rocha NP, et al. Increased ApoB/ApoA1 ratio is associated with excess weight, body adiposity, and altered lipid profile in children. J Pediatr. 2019;95:238-46.
  • Funding
    Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - process n. 478910/2013-4).

Acknowledgements

The authors would like to thank the children and their parents for their participation in the study, to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - process No. 478910/2013-4) for the financial support, and for the HHM Hermsdorff's fellowship in Research Productivity, to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarships granted to graduate students, and to BioClin for the donation of kits for biochemical analyses.

References

  • 1
    Hong MH. Atherosclerotic cardiovascular disease beginning in childhood. Korean Circ J. 2010;40:1-9.
  • 2
    Raitakari OT, Juonala K, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascuar Risk in Young Finns Study. JAMA. 2003;290:2277-83.
  • 3
    Barter PJ, Ballantyne CM, Carmena R, Cabezas MC, Chapman MJ, Couture P, et al. Apo B versus cholesterol in estimating cardiovascular risk and in guiding therapy: report of the thirty-person/ten-country panel. J Intern Med. 2006;259:247-58.
  • 4
    Navab M, Reddy ST, Van Lenten BJ, Fogelman AM. HDL and cardiovascular disease: atherogenic and atheroprotective mechanisms. Nat Rev Cardiol. 2011;8:222-32.
  • 5
    Kappelle PJ, Gansevoort RT, Hillege JL, Wolffenbuttel BH, Dullaart RP. Apolipoprotein B/A-I and total cholesterol/high-density lipoprotein cholesterol ratios both predict cardiovascular events in the general population independently of nonlipid risk factors, albuminuria and C-reactive protein. J Intern Med. 2011;269:232-42.
  • 6
    Qin G, Tu J, Zhang C, Tang X, Luo L, Wu J, et al. The value of the apoB/apoAI ratio and the non-HDL-C/HDL-C ratio in predicting carotid atherosclerosis among Chinese individuals with metabolic syndrome: a cross-sectional study. Lipids Health Dis. 2015;14:24.
  • 7
    Retnakaran R, Zinman B, Connelly PW, Harris SB, Hanley AJ. Nontraditional cardiovascular risk factors in pediatric metabolic syndrome. J Pediatr. 2006;148:176-82.
  • 8
    Savas Erdeve S, Simsek E, Dallar Y, Biyikli Z. Utility of ApoB/ApoA1 ratio for the prediction of cardiovascular risk in children with metabolic syndrome. Indian J Pediatr. 2010;77:1261-5.
  • 9
    Ben Ounis O, Elloumi M, Makni E, Zouhal H, Amri M, Tabka Z, et al. Exercise improves the ApoB/ApoA-I ratio, a marker of the metabolic syndrome in obese children. Acta Paediatr Int J Paediatr. 2010;99:1679-85.
  • 10
    Albuquerque MN, Diniz AS, Arruda IK. Apolipoproteins and their association with cardiometabolic risk biomarkers in adolescents. Nutr Hosp. 2015;32:2674-83.
  • 11
    World Health Organization. Growth reference data for 5-19 years. Geneva: WHO; 2007.
  • 12
    Filho VC, Fagundes RR, de Campos W. Anthropometric indices among schoolchildren from a municipality in Southern Brazil: a descriptive analysis using the LMS method. Rev Paul Pediatr. 2014;32:333-41.
  • 13
    Ashwell M, Hsieh SD. Six reasons why the waist-to-height ratio is a rapid and effective global indicator for health risks of obesity and how its use could simplify the international public health message on obesity. Int J Food Sci Nutr. 2005;56:303-7.
  • 14
    Mazes RB, Barden HS, Hanson J. Dual-energy X-ray absorptiometry for total body and regional bone mineral and soft-tissue composition. Am J Clin Nutr. 1990;51:1106-12.
  • 15
    McCarthy HD, Cole TJ, Fry T, Jebb SA, Prentice AM. Body fat reference curves for children. Int J Obes (Lond). 2006;30:598-602.
  • 16
    Nafiu OO, Burke C, Lee J, Voepel-Lewis T, Malviya S, Tremper KK. Neck circumference as a screening measure for identifying children with high body mass index. Pediatrics. 2010;126:e306-10.
  • 17
    Malachias MV, Souza WK, Plavinik FL, Rodrigues CI, Brandão AA, Neves MF, et al. VII Diretriz brasileira de hipertensão arterial. Arq Bras Cardiol. 2016;107:S1-83.
  • 18
    Xavier HT, Izar MC, Faria Neto JR, Assad MH, Rocha VZ, Sposito AC, et al. V Diretriz brasileira de dislipidemias e prevenção da aterosclerose. Arq Bras Cardiol. 2013;101:S1-22.
  • 19
    Brasil. Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional de Saúde do Escolar (PeNSE) - 2012. Rio de Janeiro: IBGE; 2013. Available from: http://biblioteca.ibge.gov.br/visualizacao/livros/liv64436.pdf [cited 30.10.15].
    » http://biblioteca.ibge.gov.br/visualizacao/livros/liv64436.pdf
  • 20
    Mokha JS, Srinivasan SR, Dasmahapatra P, Fernandez C, Chen W, Xu J, et al. Utility of waist-to-height ratio in assessing the status of central obesity and related cardiometabolic risk profile among normal weight and overweight/obese children: the Bogalusa Heart Study. BMC Pediatr. 2010;10:73.
  • 21
    Cuschieri S, Vassallo J, Calleja N, Camilleri R, Borg A, Bonnici G, et al. Prevalence of obesity in Malta. Obes Sci Pract. 2016;2:466-70.
  • 22
    Vásquez FD, Corvalám CL, Uauy RE, Kain JA. Anthropometric indicators as predictors of total body fat and cardiometabolic risk factors in Chilean children at 4, 7 and 10 years of age. Eur J Clin Nutr. 2017;71:536-43.
  • 23
    Cooper AD. Hepatic uptake of chylomicron remnants. J Lipid Res. 1997;38:2173-92.
  • 24
    Morita SY. Metabolism and modification of apolipoprotein B-containing lipoproteins involved in dyslipidemia and atherosclerosis. Bio Pharm Bull. 2016;39:1-24.
  • 25
    Chan CD, Barret HP, Watts GF. Dyslipidemia in visceral obesity. Am J Cardiovasc Drugs. 2004;4:227-46.
  • 26
    Lin GM, Liu K, Colangelo LA, Lakoski GS, Tracy RP, Greenlan P. Low-density lipoprotein cholesterol concentrations and association of high-sensitivity C-reactive protein concentrations with incident coronary heart disease in the multi-ethnic study of atherosclerosis. Am J Epidemiol. 2016;183:46-52.
  • 27
    Miyashita M, Okada T, Kuromori Y, Harada K. LDL particle size, fat distribution and insulin resistance in obese children. Eur J Clin Nutr. 2006;60:416-20.
  • 28
    Navarro P, de Dios O, Gavela-Pérez T, Jois A, Garcés C, Soriano-Guillém L. High-sensitivity C reactive protein and leptin levels related to body mass index changes throughout childhood. J Pediatr. 2016;178:178-82.

Publication Dates

  • Publication in this collection
    11 Apr 2019
  • Date of issue
    Mar-Apr 2019

History

  • Received
    15 July 2017
  • Accepted
    26 Dec 2017
  • Published
    10 Feb 2018
Sociedade Brasileira de Pediatria Av. Carlos Gomes, 328 cj. 304, 90480-000 Porto Alegre RS Brazil, Tel.: +55 51 3328-9520 - Porto Alegre - RS - Brazil
E-mail: jped@jped.com.br