C-reactive protein (CRP) is a marker of inflammation that has been shown to be predictive of cardiovascular diseases in adults. To evaluate the distribution of CRP as well as its association with metabolic syndrome and its components.
This is a cross-sectional study on adolescents aged 12–17, participants in the Study of Cardiovascular Risk in Adolescents (ERICA). Anthropometric, biochemical and blood pressure data were collected from 6316 adolescents, selected from a random sample of students in the cities of Brasilia, Fortaleza, João Pessoa, Manaus, Porto Alegre and Rio de Janeiro. Metabolic syndrome was defined by the criteria proposed by International Diabetes Federation for adolescent. Poisson regression model with robust variance, taking into consideration the study’s complex sampling design, was used to determine multivariate-adjusted prevalence rate ratios expressing the relationship of metabolic syndrome with CRP.
In adolescents with metabolic syndrome, CRP concentrations were five times higher (1.01 mg/l; interquartile range (IQR): 0.54–3.47) compared with those without metabolic syndrome (0.19 mg/l; IQR: 0.10–0.78). In multivariate Poisson regression analysis adjusted by sex, age and skin color, the prevalence of elevated CRP (>3.0 mg/l) was almost three times higher in adolescents with metabolic syndrome than in those without this condition (prevalence ratio (PR): 2.9; 95%CI: 2.0–4.3; P<0.001). Of the metabolic syndrome components, elevated waist circumference, low high-density lipoprotein-cholesterol and high triglycerides were significantly related to CRP in a graded (dose–response) manner.
The association of CRP with metabolic syndrome and its components suggests that inflammation may be useful in assessing cardiovascular risk in adolescents.
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Wang G, Christoffel KK, Brickman WJ, Hong X, Arguelles L, Zhang S et al. C-reactive protein in adolescent twins: patterns and relationship to adiposity. J Clin Endocrinol Metab 2011; 96: 3226–3233.
Chu NF, Rimm EB, Wang DJ, Liou HS, Shieh SM . Clustering of cardiovascular disease risk factors among obese schoolchildren: the Taipei Children Heart Study. Am J Clin Nutr 1998; 67: 1141–1146.
Ridker PM, Rifai N, Rose L, Buring JE, Cook NR . Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events. N Engl J Med 2002; 347: 1557–1565.
Ferranti S, Mozaffarian D . The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem 2008; 54: 945–955.
Dekker JM, Girman C, Rhodes T, Nijpels G, Stehouwer CD, Bouter LM et al. Metabolic syndrome and 10-year cardiovascular disease risk in the Hoorn Study. Circulation 2005; 112: 666–673.
Morrison JA, Friedman LA, Wang P, Glueck CJ . Metabolic syndrome in childhood predicts adult metabolic syndrome and type 2 diabetes mellitus 25 to 30 years later. J Pediatr 2008; 152: 201–206.
Guran O, Akalin F, Ayabakan C, Dereli FY, Haklar G . High‐sensitivity C‐reactive protein in children at risk for coronary artery disease. Acta Paediatr 2007; 96: 1214–1219.
Giannini DT, Kushnir MCC, Szklo M . Metabolic syndrome in overweight and obese adolescents: a comparison of two different diagnostic criteria. Ann Nutr Metab 2014; 64: 71–79.
Kuschnir MC, Bloch KV, Szklo M, Klein CH, Burafaldi LA, Abeu GA et al. ERICA: prevalence of metabolic syndrome in Brazilian adolescents. Rev Saude Publica 2016; 50: 11s.
Lourenco BH, Cardoso MA . ACTION Study Team.Cardoso,C-reactive protein concentration predicts change in body mass index during childhood. PLoS One 2014; 9: e90357.
Bloch KV, Szklo M, Kuschnir MC, Abreu GA, Barufaldi LA, Klein CH et al. The Study of Cardiovascular Risk in Adolescents—ERICA: rationale, design and sample characteristics of a national survey examining cardiovascular risk factor profile in Brazilian adolescents. BMC Public Health 2015; 15: 94.
Vasconcellos MTL, Silva PLN, Szklo M, Kuschnir MCC, Klein CH, Abreu GA et al. Sampling design for the Study of Cardiovascular Risks in Adolescents (ERICA). Cad Saude Publica 2015; 31: 921–930.
DeBoer MD . Obesity, systemic inflammation, and increased risk for cardiovascular disease and diabetes among adolescents: a need for screening tools to target interventions. Nutrition 2013; 29: 379–386.
Tanner JM . Growth at Adolescence. 2nd ed. Blackwell Scientific Publications: Oxford, 1962.
Instituto Brasileiro de Geografia e Estatística (IBGE) Um Estado das Categorias de Classificação de Cor ou Raça. IBGE: Rio de Janeiro, 2008.
Department of Health and Human Services USA. Preventing tobacco use among young people. A report of the Surgeon General: US Department of Health and Human Services. Atlanta, Georgia, 1994.
Global Youth Tobacco Survey Collaborating Group. Differences in worldwide tobacco use by gender: findings from the Global Youth Tobacco Survey. J Sch Health 2003; 73: 207–215.
Farias Júnior JC, Lopes AS, Mota J, Santos MP, Ribeiro JC, Hallal PC . Validade e reprodutibilidade de um questionário para medida de atividade física em adolescentes: uma adaptação do Self-Administered Physical Activity Checklist. Rev Bras Epidemiol 2012; 15: 198–210.
Biddle S, Cavill N, Sallis JF . Young and Active? Young People and Health-enhancing Physical Activity: Evidence and Implications. Health Education Authority: London, 1998, pp 17–48.
Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J . Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 2007; 85: 660–667.
National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004; 114: 555–576.
Stergiou GS, Yiannes NG, Rarra VC . Validation of the Omron 705 IT oscillometric device for home blood pressure measurement in children and adolescents: the Arsakion School Study. Blood Press Monit 2006; 11: 229–234.
Zimmet P, Alberti KGM, Kaufman F, Tajima N, Silink M, Arslanian S et al. The metabolic syndrome in children and adolescents–an IDF consensus report. Pediatr Diabetes 2007; 8: 299–306.
U.S. Food And Drug Administration (FDA) Guidance for Industry - Review Criteria for Assessment of C Reactive Protein (CRP), High Sensitivity C-Reactive Protein (hsCRP) and Cardiac C-Reactive Protein (cCRP) Assays. FDA: Silver Spring, MD, 2005.
DeBoer MD, Gurka MJ, Sumner AE . Diagnosis of the metabolic syndrome is associated with disproportionately high levels of high-sensitivity C-reactive protein in non–Hispanic Black adolescents an analysis of NHANES 1999–2008. Diabetes Care 2011; 34: 734–740.
Ford ES, Giles WH, Myers GL, Rifai N, Ridker PM, Mannino DM . C-reactive protein concentration distribution among US children and young adults: findings from the National Health and Nutrition Examination Survey, 1999–2000. Clin Chem 2003; 49: 1353–1357.
Lambert M, Delvin EE, Paradis G, O’Loughlin J, Hanley JA, Levy E . C-reactive protein and features of the metabolic syndrome in a population-based sample of children and adolescents. Clin Chem 2004; 50: 1762–1768.
Ford ES . Prevalence of the metabolic syndrome defined by the International Diabetes Federation among adults in the U.S. Diabetes Care 2005; 28: 2745–2749.
Bloch KV, Klein CH, Szklo M, Kuschnir MCC, Abreu GA, Barufaldi LA et al. ERICA: prevalências de hipertensão arterial e obesidade em adolescentes Brasileiros. Rev Saude Publica 2016; 50 (Suppl 1), 9s.
Roh EJ, Lim JW, Ko KO, Cheon EJ . A useful predictor of early atherosclerosis in obese children: serum high-sensitivity C-reactive protein. J Korean Med Sci 2007; 22: 192–197.
Silva IT, Sanches LB, Mello AP, Damasceno NR . Impact of C-reactive protein on cardiovascular risk in adolescents. Arq Bras Cardiol 2010; 94: 585–591.
Packard RR, Libby P . Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin Chem 2008; 54: 24–38.
Cushman M, McClure LA, Howard VJ, Jenny NS, Lakoski SG, Howard G . Implications of increased C-reactive protein for cardiovascular risk stratification in black and white men and women in the US. Clin Chem 2009; 55: 1627–1636.
Blaha MJ, Rivera JJ, Budoff MJ, Blankstein R, Agatston A, O'Leary DH et al. Association between obesity, high-sensitivity C-reactive protein ⩾2mg/l, and subclinical atherosclerosis: implications of JUPITER from the Multi-Ethnic Study of Atherosclerosis. Arterioscler Thromb Vasc Biol 2011; 31: 1430–1438.
Cardoso-Saldaña G, Juárez-Rojas J, Zamora-González J, Raygoza-Pérez M, Martinez-Alvarado R, Posadas-Sánchez R et al. C-reactive protein levels and their relationship with metabolic syndrome and insulin resistance in Mexican adolescents. J Pediatr Endocrinol Metab 2007; 20: 797–806.
Soriano-Guillén L, Hernández-García B, Pita J, Domínguez-Garrido N, Del Río-Camacho G, Rovira A . High-sensitivity C-reactive protein is a good marker of cardiovascular risk in obese children and adolescents. Eur J Endocrinol 2008; 159: R1–R4.
Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB . Low-grade systemic inflammation in overweight children. Pediatrics 2001; 107: E13.
Barja S, Acevedo M, Arnaiz P, Berríos X, Bambs C, Guzmán B et al. Marcadores de aterosclerosis temprana y síndrome metabólico en niños. Rev Med Chil 2009; 137: 522–530.
Wu DM, Chu NF, Shen M-H, Wang SC . Obesity, plasma high sensitivity c-reactive protein levels and insulin resistance status among school children in Taiwan. Clin Biochem 2006; 39: 810–815.
Brasil AR, Norton RC, Rossetti MB, Leão E, Mendes RP . Proteína C reativa como indicador de inflamação de baixa intensidade em crianças e adolescentes com e sem obesidade. J Pediatr (Rio J) 2007; 83: 477–480.
Oliveira AC, Oliveira AM, Adan LF, Oliveira NF, Silva AM, Ladeia AM . Retraction: update to ‘C-reactive protein and metabolic syndrome in youth: a strong relationship?’. Obesity (Silver Spring) 2009; 17: 1113.
Yoshida T, Kaneshi T, Shimabukuro T, Sunagawa M, Ohta T . Serum C-reactive protein and its relation to cardiovascular risk factors and adipocytokines in Japanese children. J Clin Endocrinol Metab 2006; 91: 2133–2137.
El-shorbagy HH, Ghoname IA . High-sensitivity C-reactive protein as a marker of cardiovascular risk in obese children and adolescent. Health 2010; 2: 1078–1084.
The study ERICA was supported by the Brazilian Ministry of Health (Science and Technology Department) and the Brazilian Ministry of Science and Technology (Financiadora de Estudos e Projetos/FINEP and Conselho Nacional de Pesquisa/CNPq) (grants FINEP: 01090421, CNPq: 565037/2010-2, 405009/2012-7 and 457050/2013-6).
The authors declare no conflict of interest.
About this article
Cite this article
Giannini, D., Kuschnir, M., de Oliveira, C. et al. C-reactive protein in Brazilian adolescents: distribution and association with metabolic syndrome in ERICA survey. Eur J Clin Nutr 71, 1206–1211 (2017). https://doi.org/10.1038/ejcn.2017.74
The role of lifestyle and non-modifiable risk factors in the development of metabolic disturbances from childhood to adolescence
International Journal of Obesity (2020)
Diabetology & Metabolic Syndrome (2019)