Abstract
Purpose
Evidence suggests that plasma retinol-binding protein 4 (RBP4) and insulin resistance are related to body fat (BF). We aimed to assess the relationship between RBP4 and insulin resistance with obesity in a mixed (skin color) cohort of the Brazilian population.
Methods
A nested case–control study was conducted in 227 schoolchildren aged 7–14 years. Schoolchildren with a high BF percentage (% BF, ≥ 30 for girls and ≥ 25 for boys) were identified as the obese group (n = 137), and those with lower values were identified as the non-obese group (n = 90). Percentage of body fat (% BF) was determined by tetrapolar bioimpedance (Quantum II, RJL System), RBP4 by enzyme-linked immunosorbent assay (Immunology Consultants Laboratory), plasma fasting insulin by chemiluminescent immunoassay (Access® Immunoassay System) and insulin resistance by the homeostasis model insulin resistance (IRHOMA) index. Serum lipid profile and arterial blood pressure were evaluated.
Results
The significant independent risk factors associated with obesity were as follows: male sex, increased serum LDL-C, RBP4 and IRHOMA. Among children with higher RBP4, the association with obesity increased significantly (from 3.1 to 8.5) in the presence of insulin resistance, when compared to higher RBP4 and non-insulin resistance.
Conclusion
IRHOMA and RBP4 showed significant associations with obesity and traditional CVD risk factors. They might therefore be used as a marker for CVD risk and have clinical implications in the development of comorbidities associated with obesity.
Similar content being viewed by others
References
Daniels SR, Jacobson MS, McCrindle BW et al (2000) American heart association childhood obesity research summit: executive summary. Circulation 119:2114–2123
World Health Organization (2000) Obesity: preventing and managing the global epidemic, report of a WHO consultation on obesity, Geneva, 1997 June 3–5
Instituto Brasileiro de Geografia e Estatística. Indicadores sociodemográficos e de saúde no Brasil. Rio de Janeiro: Instituto Brasileiro de Geografia e Estatística (2009). (Estudos e Pesquisas: Informação Demográfica e Socioeconômica, 25)
Weiss R, Kaufman FR (2008) Metabolic complications of childhood obesity: identifying and mitigating the risk. Diabetes Care 31(2):310–316
Kolotkin RL, Crosby RD, Williams GR et al (2001) The relationship between health-related quality of life and weight loss. Obes Res 9:564–571
Cândido APC, Benedetto R, Castro APP et al (2009) Cardiovascular risk factors in children and adolescents living in an urban area of Southwest of Brazil: Ouro Preto study. Eur J Pediatr 168:1373–1382
Freitas SN, Caiaffa WT, César CC et al (2007) A comparative study of methods for diagnosis of obesity in urban mixed-race population in Minas Gerais. Public Health Nutr 10:883–890
Cândido APC, Ferreira S, Lima AA et al (2007) Lipoprotein (a) as a risk factor associated with ischemic heart disease: Ouro Preto study. Atherosclerosis 191:454–459
Lee D-C, Lee J-W, Im J-A (2007) Association of serum retinol binding protein 4 and insulin resistance in apparently healthy adolescents. Metab, Clin Exp 3:327–331
Pala L, Monami M, Ciani S et al (2012) Adipokines as possible new predictors of cardiovascular diseases: a case control study. J Nutr Metab. doi:10.1155/2012/253428
Conroy R, Espinal Y, Fennoy L et al (2011) Retinol binding protein 4 is associated with adiposity-related co-morbidity risk factors in children. J Pediatr Endocrinol Metab 24:913–919
Santoro N, Perrone L, Cirillo G et al (2009) Variations of retinol binding protein 4 levels are not associated with changes in insulin resistance during puberty. J Endocrinol Invest 32:411–414
Kanaka-Gantenbein C, Margeli A, Pervanidou P et al (2008) Retinol- binding protein 4 and lipocalin-2 in childhood and adolescent obesity: when children are not just “Small Adults”. Clin Chem 7:1176–1182
Deurenberg P, Kusters CS, Smit HE (1990) Assessment of body composition by bioelectrical impedance in children and young adults is strongly age-dependent. Eur J Clin Nutr 44:261–268
Willams DP, Going SB, Lohman TG et al (1992) Body fatness and risk for elevated blood pressure, total cholesterol, and serum lipoprotein ratios in children and adolescents. Am J Public Health 82:358–363
Giuliano ICB, Caramelli B, Pellanda L et al. (2005) Diretriz de prevenção da aterosclerose na infância e adolescência. Arq Bras Cardiol 85:1–36
Madeira IR, Carvalho CN, Gazolla FM et al (2008) Ponto de corte do índice Homeostatic Model Assessment for Insulin Resistance (HOMA-IR) avaliado pela curva receiver operating characteristc (ROC) na detecção da síndrome metabólica em crianças pré-púberes com excesso de peso. Arq Bras Endocrinol Metabol 52(9):1466–1473
Keskin M, Kurtoglu S, Kendirci M et al (2005) Homeostasis model assessment is more reliable than fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents. Pediatrics 115(4):500–503
Burrows AR, Leiva BL, Burqueño AM et al (2006) Sensibilidad insulínica en niños de 6 a 15 años: associación con estado nutricional y pubertad. Revista Médica de Chile 134:1417–1426
Copeland K, Pankratz K, Cathey V et al (2006) Acanthosis nigricans, insulin resistance (HOMA) and dyslipidemia among native American children. J Okla State Med Assoc 99:19–24
Mion Júnior D, Junior OK, Gomes MAM et al (2006) V Diretrizes Brasileiras de Hipertensão Arterial. São Paulo, Sociedade Brasileira de Hipertensão, Sociedade Brasileira de Cardiologia, Sociedade Brasileira de Nefrologia
Tanner JM (1962) Growth at adolescence, 2nd edn. Blackwell Scientific Publications, Oxford, p 326
Rhie JY, Choi BM, Eun SH et al (2011) Association of serum retinol binding protein 4 with adiposity and pubertal development in Korean children and adolescents. Korean Acad Med Sci 26:797–802
Matthews DR, Hosker JP, Rudenski AS et al (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419
Gungor N, Saad R, Janosky J et al (2004) Validation of surrogate estimates of insulin sensitivity and insulin secretion in children and adolescents. J Pediatr 144:47–55
Del Prato S, Riccio A, Kreutzenberg VS et al (1995) Basal plasma insulin levels exert a qualitative but not a quantitative effect on glucose-mediated glucose uptake. Am J Physiol 268:1089–1095
Araujo CL, Dumith SC, Menezes AMB et al (2010) Nutritional status of adolescents: the 11- year follow-up of the 1993 Pelotas (Brazil) birth cohort study. Cadernos de Saúde Pública 26(10):1895–1903
Wang Y (2002) Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics 110:903–910
Van Lenthe FJ, Kemper CG, van Mechelen W (1996) Rapid maturation in adolescence results in greater obesity in adulthood: the Amsterdam Growth and Health Study. Am J Clin Nutr 64:18–24
Novaes JF, Lamounier JA, Franceschini SC et al (2009) Fatores ambientais associados ao sobrepeso infantil. Revista de Nutrição (Campinas) 22:661–673
Barbosa Filho VC, Campos W, Bozza R et al (2012) The prevalence and correlates of behavioral risk factors for cardiovascular health among Southern Brazil adolescents: a cross section study. BMC Pediatr. doi:10.1186/1471-2431-12-130
Coelho LG, Cândido AP, Machado-Coelho GL et al (2012) Association between nutritional status, food habits and physical activity level in schoolchildren. J Pediatr 88(5):406–412
Rutters F, Nieuwenhuizen AG, Verhoef SP et al (2009) The relationship between leptin, gonadotropic hormones, and body composition during puberty in a Dutch children cohort. Eur J Endocrinol 160:973–978
Lin CJ, Chu NF, Hung YJ et al (2012) The association of retinol binding protein 4 with metabolic syndrome and obesity in adolescents: the effects of gender and sex hormones. Clin Pediatr 52(1):16–23
Horlick MB, Rosenbaum M, Nicolson M et al (2000) Effect of puberty on the relationship between circulating leptin and body composition. J Clin Endocrinol Metabol 85:2509–2518
Kos K, Wong S, Tan BK et al (2011) Human RBP4 adipose tissue expression in gender specific and influenced by leptin. Clin Endocinol 74:197–205
Dai S, Fulton JE, Harrist RB et al (2009) Blood lipids in children: age- related patterns and association with body-fat indices. Am J Prev Med 32(2):556–564
Monti LD, Brambilla P, Stefani I et al (1995) Insulin regulation of glucose turnover and lipid levels in obese children with fasting normo insulinemia. Diabetologia 38:739–747
Kannel WB, D’ Agostino RB, Belanger AJ (1995) Concept of bridging the gap from youth to adulthood. Am J Med Sci 310:2569–2575
Balagopal P, Graham TE, Kahn BB et al (2007) Reduction of elevated serum retinol binding protein (RBP4) in obese children by lifestyle intervention: association with subclinical inflammation. J Clin Endocrinol Metab 92:1971–1974
Kim LY, Kim TK, Cheong ES et al (2012) Relation of absolut or relative adiposity to insulin resistance, retinol binding protein-4, leptin, and adiponectin in type 2 diabetes. Diabetes Metab J 36:415–421
Friebe D, Neef M, Erbs S et al (2010) Retinol binding protein 4 (RBP4) is primarily associated with adipose tissue mass in children. Int J Pediatr Obes 6(2–2):345–352
Foy CG, Foley KL, D’Agostino RB et al (2006) Physical activity, insulin sensitivity, and hypertension among US adults: findings from Insulin Resistance Atherosclerosis Study. Am J Epidemiol 163:921–928
Atebek ME, Pirgon O, Kurtoglu S (2007) Assessment of abnormal glucose homeostasis and insulin resistance in Turkish obese children and adolescents. Diabetes Obes Metab 9:304–310
Hotamisligil GS, Arner P, Caro JF et al (1995) Increased adipose tissue expression of tumor necrosis factor- alpha in human obesity and insulin resistance. J Clin Investig 95:2409–2415
Blanner WS (1989) Retinol binding protein- the serum transport protein for vitamin A. Endocr Rev 10:308–316
Acknowledgments
The authors wish to thank Conselho Nacional de Desenvolvimento Cientifico e Tecnológico–CNPq (Grant no. 474965/04), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES, Fundação de Amparo a Pesquisa do Estado de Minas Gerais—FAPEMIG (Grant APQ-02028-09) and Prefeitura Municipal de Ouro Preto for financial support. GLLMC is recipient of a CNPq individual research grant of productivity (Grant no. 302315/2011-0). The authors thank Dr. Eduardo de Castro Ferreira, for revision of the manuscript.
Conflict of interest
The authors state no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Castro, A.P.P., Cândido, A.P.C., de Carvalho Nicolato, R.L. et al. Retinol-binding protein 4 and insulin resistance are related to body fat in primary and secondary schoolchildren: the Ouro Preto study. Eur J Nutr 53, 433–440 (2014). https://doi.org/10.1007/s00394-013-0543-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-013-0543-5