Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Nutrition during the early life cycle

Cardiometabolic risk in adolescents with normal weight obesity

Abstract

Background

Normal weight obesity (NWO), which is defined by the excess of body fat in normal weight individuals, has been neglected among adolescents, due to their normal weight and young age. Few studies were carried out on the topic with adolescents.

Objective

To analyze whether the NWO is associated with cardiometabolic risk factors in adolescents.

Subjects/Methods

Cross-sectional study, with 506 normal weight adolescents aged 10–19 years, selected in schools in Brazil. Weight, height, waist circumference (WC) and neck circumference were obtained and the body mass index (BMI) and waist/height ratio (WHR) were calculated. Body composition analysis was performed using dual-energy X-ray absorptiometry. The clinical evaluation included lipid and glycid profile, platelets, leukocytes, lymphocytes, monocytes, uric acid and blood pressure, as well as the presence of metabolic syndrome (MS) and its components. NWO was defined by the presence of normal weight, according to BMI for age, and excess body fat (≥25% and ≥30% in males and females, respectively). Logistic regression models were used to analyze associations between normal weight adolescents with and without the NWO phenotype.

Results

NWO associated positively with abdominal obesity, analyzed through WC (OR = 1.36;95%CI = 1.27–1.47), WHR (OR = 25.89;95%CI = 10.43–64.26) and android fat (OR = 1.49;95%CI = 1.36–1.63); insulin resistance (OR = 4.09;95%CI = 1.72–9.70), hyperinsulinemia (OR = 3.83;95%CI = 1.50–9.76) and the highest values of the triglycerides-glycemia index (OR = 4.28;95%CI = 1.21–15.08); uric acid (OR = 1.81;95%CI = 1.29–2.55), as well as the changes in LDL (OR = 3.39;95%CI = 1.47–7.81), total cholesterol (OR = 2.77;95%CI = 1.22–6.29), and in at least one (OR = 1.87;95%CI = 1.04–3.37) or two (OR = 6.61;95%CI = 1.45–30.19) components of MS.

Conclusion

NWO is associated with the presence of cardiometabolic risk factors in adolescents.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1

References

  1. Obesity and overweight. https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight (accessed 18 Nov 2020).

  2. Adolescent and young adult health. https://www.who.int/news-room/fact-sheets/detail/adolescents-health-risks-and-solutions (accessed 10 Mar 2021).

  3. Javed A, Jumean M, Murad MH, Okorodudu D, Kumar S, Somers VK, et al. Diagnostic performance of body mass index to identify obesity as defined by body adiposity in children and adolescents: a systematic review and meta-analysis. Pediatr Obes. 2015;10:234–44.

    CAS  Article  Google Scholar 

  4. De Lorenzo A, Martinoli R, Vaia F, Di Renzo L. Normal weight obese (NWO) women: an evaluation of a candidate new syndrome. Nutr, Metab Cardiovascular Dis. 2006;16:513–23.

    Article  Google Scholar 

  5. Coelho CCN da S, Bragança MLBM, de Oliveira BR, Bettiol H, Barbieri MA, Cardoso VC, et al. Incidence of metabolic syndrome in adults with healthy weight, normal weight obesity, and overweight/obesity. Nutrition. 2021;85:111134.

    Article  Google Scholar 

  6. Taheri E, Hosseini S, Qorbani M, Mirmiran P. Association of adipocytokines with lipid and glycemic profiles in women with normal weight obesity. BMC Endocr Disord. 2020;20:171.

    CAS  Article  Google Scholar 

  7. Wijayatunga NN, Dhurandhar EJ. Normal weight obesity and unaddressed cardiometabolic health risk-a narrative review. Int J Obes. 2021. https://doi.org/10.1038/s41366-021-00858-7.

    Article  Google Scholar 

  8. Kapoor N, Lotfaliany M, Sathish T, Thankappan KR, Thomas N, Furler J, et al. Prevalence of normal weight obesity and its associated cardio-metabolic risk factors - Results from the baseline data of the Kerala Diabetes Prevention Program (KDPP). PLoS One. 2020;15:e0237974.

    CAS  Article  Google Scholar 

  9. Cota BC, Suhett LG, Leite NN, Pereira PF, Ribeiro SAV, Franceschini SDCC. Cardiometabolic risk and health behaviours in adolescents with normal-weight obesity: a systematic review. Public Health Nutr. 2021;24:870–81. https://doi.org/10.1017/S1368980020004863. Epub 2020 Dec 1. PMID: 33256881.

  10. Pereira PF. Relação de perimetrias centrais com adiposidade, marcadores cardiometabólicos, inflamatórios e hormonais nas três fases da adolescência. Dissertação [Doutorado em Ciência da Nutrição] – Universidade Federal de Viçosa, 2014. https://www.locus.ufv.br/handle/123456789/390 (accessed 18 Nov 2020).

  11. IBGE | Cidades@ | Minas Gerais | Viçosa | Panorama. https://cidades.ibge.gov.br/brasil/mg/vicosa/panorama (accessed 18 Nov 2020).

  12. Luiz RR, Magnanini MMF, O Tamanho da Amostra em Investigações Epidemiológicas. In: Medronho, RA; Carvalho, DM; Block, KV; Luiz, RR; Werneck, GL Epidemiologia. São Paulo: Atheneu, p. 295–307, 2003.

  13. Growth reference data for 5-19 years. https://www.who.int/toolkits/growth-reference-data-for-5to19-years (accessed 18 Nov 2020).

  14. McCarthy HD, Ashwell M. A study of central fatness using waist-to-height ratios in UK children and adolescents over two decades supports the simple message – ‘keep your waist circumference to less than half your height’. Int J Obesity. https://www.nature.com/articles/0803226 (accessed 18 Nov 2020).

  15. Williams DP, Going SB, Lohman TG, Harsha DW, Srinivasan SR, Webber LS, et al. Body fatness and risk for elevated blood pressure, total cholesterol, and serum lipoprotein ratios in children and adolescents. Am J Public Health. 1992;82:358–63.

    CAS  Article  Google Scholar 

  16. Friedewald WT, Levy RI.Fredrickson DS, Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502. https://pubmed.ncbi.nlm.nih.gov/4337382/.

  17. NATIONAL HEART, LUNG, AND BLOOD INSTITUTE. Expert Panel on Integrated Guidelines for Cardiovascular Health and Risk Reduction in Children and Adolescents Full Report. National Institutes of Health, NIH Publication, n. 12-7486ª, out., 2012.

  18. Keskin M, Kurtoglu S, Kendirci M, Atabek ME, Yazici C. Homeostasis model assessment is more reliable than the fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents. Pediatrics. 2005;115:e500–e503.

    Article  Google Scholar 

  19. Sociedade Brasileira de Cardiologia - Publicações. I Diretriz de Prevenção de Aterosclerose na Infância e na Adolescência. Arquivos Brasileiros de Cardiologia, v. 85, n. 6, p. 1–36, 2005. http://publicacoes.cardiol.br/consenso/2005/prevatero.asp (accessed 18 Nov 2020).

  20. Guerrero-Romero F, Villalobos-Molina R, Jiménez-Flores JR, Simental-Mendia LE, Méndez-Cruz R, Murguía-Romero M, et al. Fasting triglycerides and glucose index as a diagnostic test for insulin resistance in young adults. Arch Med Res. 2016;47:382–7.

    CAS  Article  Google Scholar 

  21. Mohd Nor NS, Lee S, Bacha F, Tfayli H, Arslanian S. Triglyceride glucose index as a surrogate measure of insulin sensitivity in obese adolescents with normoglycemia, prediabetes, and type 2 diabetes mellitus: comparison with the hyperinsulinemic-euglycemic clamp. Pediatr Diabetes. 2016;17:458–65.

    CAS  Article  Google Scholar 

  22. de Andrade JP, Nobre F. VI Diretrizes Brasileiras de Hipertensão. SOCIEDADE BRASILEIRA DE HIPERTENSÃO. Arquivos Brasileiros de Cardiologia. 2010;v. 95:1–51. n. 1

    Google Scholar 

  23. Flynn JT, Kaelber DC, Baker-Smith CM, Blowey D, Carroll AE, Daniels SR, et al. Clinical Practice Guideline for Screening and Management of High Blood Pressure in Children and Adolescents. Pediatrics 2017;140. https://doi.org/10.1542/peds.2017-1904.

  24. INTERNATIONAL DIABETES FEDERATION (IDF). The IDF consensus definition of the metabolic syndrome in children and adolescentes. Diabetes Voice, v. 52, n.4, p. 29–32, 2007. Consensus statements: https://www.idf.org/e-library/consensus-statements/61-idf-consensus-definition-of-metabolic-syndrome-in-children-and-adolescents.html (accessed November 18, 2020).

  25. Fernández JR, Redden DT, Pietrobelli A, Allison DB. Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr. 2004;145:439–44.

    Article  Google Scholar 

  26. IBGE | Biblioteca | Detalhes | Pesquisa sobre padrões de vida - PPV. https://biblioteca.ibge.gov.br/biblioteca-catalogo.html?id=5469&view=detalhes (accessed 18 Nov 2020).

  27. Guedes DP, Lopes CC, Guedes JERP. Reprodutibilidade e validade do Questionário Internacional de Atividade Física em adolescentes. Rev Brasileira de Med do Esport. 2005;11:151–8.

    Article  Google Scholar 

  28. Centro de Estudos do Laboratório de Aptidão Física de São Caetano do Sul. CELAFISCS. https://celafiscs.org.br/ (accessed 18 Nov 2020).

  29. Serra-Majem L, Aracenta-Bartrina J. Introducción a la epidemiologia nutricional. In: Serra-Majem, L; Aracenta-Bartrina, J; Mataix-Verdú, J Nutrición y Salud Pública. Barcelona: Masson, p. 59–65, 1995. https://www.elsevier.com/books/nutricion-y-salud-publica/serra-majem/978-84-458-2191-6 (accessed 18 Nov 2020).

  30. Olafsdottir AS, Torfadottir JE, Arngrimsson SA. Health behavior and metabolic risk factors associated with normal weight obesity in adolescents. PLoS One. 2016;11. https://doi.org/10.1371/journal.pone.0161451.

  31. Correa-Rodríguez M, González-Ruíz K, Rincón-Pabón D, Izquierdo M, García-Hermoso A, Agostinis-Sobrinho C, et al. Normal-weight obesity is associated with increased cardiometabolic risk in young adults. Nutrients 2020;12. https://doi.org/10.3390/nu12041106.

  32. Kim JY, Han S-H, Yang B-M. Implication of high-body-fat percentage on cardiometabolic risk in middle-aged, healthy, normal-weight adults. Obesity. 2013;21:1571–7.

    Article  Google Scholar 

  33. Marques-Vidal P, Pécoud A, Hayoz D, Paccaud F, Mooser V, Waeber G, et al. Normal weight obesity: Relationship with lipids, glycaemic status, liver enzymes and inflammation. Nutr Metab Cardiovascular Dis. 2010;20:669–75.

    CAS  Article  Google Scholar 

  34. Raitakari OT, Juonala M, Kähönen M, Taittonen L, Laitinen T, Mäki-Torkko N, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the cardiovascular risk in young finns study. JAMA. 2003;290:2277–83.

    CAS  Article  Google Scholar 

  35. Flouris AD, Canham CH, Faught BE, Klentrou P. Prevalence of cardiovascular disease risk in Ontario adolescents. Arch Dis Child. 2007;92:521–3.

    Article  Google Scholar 

  36. Romanzini M, Reichert FF, Lopes A, da S, Petroski ÉL, Farias Júnior JCde. Prevalence of cardiovascular risk factors in adolescents. Cad de Saúde Pública. 2008;24:2573–81.

    Article  Google Scholar 

  37. Kapoor N, Furler J, Paul TV, Thomas N, Oldenburg B. Normal weight obesity: an underrecognized problem in individuals of South Asian descent. Clin Therapeutics. 2019;41:1638–42.

    Article  Google Scholar 

  38. Barroso TA, Marins LB, Alves R, Gonçalves ACS, Barroso SG, Rocha G de S. Associação Entre a Obesidade Central e a Incidência de Doenças e Fatores de Risco Cardiovascular. Int J Cardiovasc Sci. 2017;f:416–l:424.

  39. Camhi SM, Kuo J, Young DR. Identifying adolescent metabolic syndrome using body mass index and waist circumference. Prev Chronic Dis. 2008;5. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2578768/ (accessed 18 Nov 2020).

  40. Li C, Ford ES, Mokdad AH, Cook S. Recent trends in waist circumference and waist-height ratio among US children and adolescents. Pediatrics. 2006;118:e1390–1398.

    Article  Google Scholar 

  41. Vasques ACJ, Priore SE, Rosado LEFP de L, Franceschini S do CC. Utilização de medidas antropométricas para a avaliação do acúmulo de gordura visceral. Rev de Nutrção. 2010;23:107–18.

    Article  Google Scholar 

  42. Yang HR, Chang EJ. Insulin resistance, body composition, and fat distribution in obese children with nonalcoholic fatty liver disease. Asia Pac J Clin Nutr. 2016;25:126–33.

    PubMed  Google Scholar 

  43. Zhang M, Wang B, Liu Y, Sun X, Luo X, Wang C, et al. Cumulative increased risk of incident type 2 diabetes mellitus with increasing triglyceride glucose index in normal-weight people: The Rural Chinese Cohort Study. Cardiovasc Diabetol. 2017;16:30.

    Article  Google Scholar 

  44. Sánchez-Íñigo L, Navarro-González D, Pastrana-Delgado J, Fernández-Montero A, Martínez JA. Association of triglycerides and new lipid markers with the incidence of hypertension in a Spanish cohort. J Hypertens. 2016;34:1257–65.

    Article  Google Scholar 

  45. Zhang S, Du T, Zhang J, Lu H, Lin X, Xie J, et al. The triglyceride and glucose index (TyG) is an effective biomarker to identify nonalcoholic fatty liver disease. Lipids Health Dis. 2017;16:15.

    Article  Google Scholar 

  46. Sánchez-Íñigo L, Navarro-González D, Fernández-Montero A, Pastrana-Delgado J, Martínez JA. The TyG index may predict the development of cardiovascular events. Eur J Clin Invest. 2016;46:189–97.

    Article  Google Scholar 

  47. Bragança MLBM, de Oliveira BR, Fonseca JM, Batalha MA, Bogea EG, Coelho CCN da S, et al. Assessment of blood biomarkers in adolescents classified by body mass index and body fat percentage. Cadernos de Saúde Pública 2020;36. https://doi.org/10.1590/0102-311x00084719.

  48. García-Hermoso A, Agostinis-Sobrinho C, Camargo-Villalba GE, González-Jiménez NM, Izquierdo M, Correa-Bautista JE, et al. Normal-weight obesity is associated with poorer cardiometabolic profile and lower physical fitness levels in children and adolescents. Nutrients. 2020;12. https://doi.org/10.3390/nu12041171.

  49. Wiklund P, Törmäkangas T, Shi Y, Wu N, Vainionpää A, Alen M, et al. Normal-weight obesity and cardiometabolic risk: a 7-year longitudinal study in girls from prepuberty to early adulthood. Obes (Silver Spring). 2017;25:1077–82.

    CAS  Article  Google Scholar 

  50. Moulin-Mares SRA, Oliosa PR, Faria ER, Zago-Gomes MP, Mill JG. Association of uric acid with cardiovascular risk in Brazilian children and adolescents. Nutr, Metab Cardiovascular Dis. 2021;31:314–21.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank all adolescents who participated in this study and their parents/guardians and the Coordination of Improvement of Higher Level Personnel (CAPES, Brazil, funding code 001) for the master’s scholarship granted to BCC. This study received support from the National Council for Scientific and Technological Development (CNPq) (scholarship no. 485986 / 2011-6) and the Research Support Foundation of the State of Minas Gerais (FAPEMIG) (scholarship no. APQ-01618-10). CNPq and FAPEMIG did not participate in the design, analysis, or writing of the article.

Author information

Authors and Affiliations

Authors

Contributions

BCC was responsible for the analysis and interpretation of the data, conducted the literature search, as well as wrote the manuscript. SEP acted in the conception and design of the study, as well as the critical review of the paper. SAVR and LLJ participated in the analysis and interpretation of data, as well as the critical review of the paper. ERF and FRF participated in the conception of the study design, data collection, as well as the critical review of the paper. PFF participated in the conception of the study design, data collection, and writing of the article. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Bruna Clemente Cota.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval

This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all the procedures involving human subjects were approved by the Ethics Committee on Human Research of the Federal University of Viçosa (case number 0140/2010). Moreover, this project was presented to the Municipal Department of Education, the Regional Superintendent of Education, and principals of schools. All participants, as well as their responsible parents/guardians, were informed about the objectives of the research, and written informed consent was obtained from the parents of all adolescents.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cota, B.C., Priore, S.E., Ribeiro, S.A.V. et al. Cardiometabolic risk in adolescents with normal weight obesity. Eur J Clin Nutr 76, 863–870 (2022). https://doi.org/10.1038/s41430-021-01037-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-021-01037-7

Search

Quick links