Skip to main content
SpringerLink
Log in

Comparison of definitions for the metabolic syndrome in adolescents. The HELENA study

  • Original Article
  • Published:
European Journal of Pediatrics Aims and scope Submit manuscript

Abstract

Various definitions are used to define metabolic syndrome in adolescents. This study aimed to compare, in terms of prevalence and differences, five frequently used definitions for this population: International Diabetes Federation, National Cholesterol Education Program Adult Treatment Panel III (NCEP-ATP) modified by Cook, pediatric American Heart Association (AHA), World Health Organization, and Jolliffe and Janssen. A sample of 1004 adolescents (12.5–17.0 years) from the Healthy Lifestyle in Europe by Nutrition in Adolescence (HELENA) study was considered. The components of the definitions (waist circumference/BMI, plasma lipids, glycemia, and blood pressure) were applied, and definitions were compared by using crosstabs, sensitivity, specificity, and kappa coefficient. The prevalence of metabolic syndrome varied from 1.6 to 3.8% depending on the used definitions. Crosstabs comparing the definitions showed the fewest cases being misclassified (having metabolic syndrome or not) between NCEP-ATP and AHA. Analyses for kappa coefficient, sensitivity, and specificity confirmed this finding.

Conclusion: The different definitions do not classify the same adolescents as having MS and prevalence varied between diagnostic methods. The modified NCEP-ATP and the AHA definitions were most analogous in defining subjects as having metabolic syndrome or not.

What is known?

• Metabolic syndrome is not only a problem of adulthood but is already present in children and adolescents.

• Several diagnostic methods are used to define metabolic syndrome in adolescents.

What is new?

• Comparing the most frequently used definitions of metabolic syndrome in adolescents showed that they do not indicate the same adolescents as having metabolic syndrome.

• The modified National Cholesterol Education Program Adult Treatment Panel III and the pediatric American Heart Association definitions were most analogous in defining subjects as having metabolic syndrome or not.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AHA:

Pediatric American Heart Association

cMetS:

Continuous metabolic syndrome score

CVD:

Cardiovascular disease

HDL:

High-density lipoprotein

HELENA-CSS:

the Healthy Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study

HOMA:

Homeostasis Model Assessment

IDF:

International Diabetes Federation

MS:

Metabolic syndrome

NCEP-ATP:

National Cholesterol Education Program Adult Treatment Panel III modified by Cook

NHANES:

National Health and Nutrition Examination Survey

TC:

Total cholesterol

TG:

Triglycerides

WHO:

World Health Organization

References

  1. Andersen LB, Wedderkopp N, Hansen HS, Cooper AR, Froberg K (2003) Biological cardiovascular risk factors cluster in Danish children and adolescents: the European Youth Heart Study. Prev Med 37:363–367

    Article  CAS  PubMed  Google Scholar 

  2. Beghin L, Castera M, Manios Y, Gilbert CC, Kersting M, De Henauw S, Kafatos A, Gottrand F, Molnar D, Sjostrom M, Leclercq C, Widhalm K, Mesana MI, Moreno LA, Libersa C (2008) Quality assurance of ethical issues and regulatory aspects relating to good clinical practices in the HELENA Cross-Sectional Study. International Journal of Obesity (2005) 32(Suppl 5):S12–S18

    Article  Google Scholar 

  3. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310

    Article  CAS  PubMed  Google Scholar 

  4. Brambilla P, Lissau I, Flodmark CE, Moreno LA, Widhalm K, Wabitsch M, Pietrobelli A (2007) Metabolic risk-factor clustering estimation in children: to draw a line across pediatric metabolic syndrome. International Journal of Obesity (2005) 31:591–600

    Article  CAS  Google Scholar 

  5. Chen W, Srinivasan SR, Li S, Xu J, Berenson GS (2005) Metabolic syndrome variables at low levels in childhood are beneficially associated with adulthood cardiovascular risk: the Bogalusa Heart Study. Diabetes Care 28:126–131

    Article  PubMed  Google Scholar 

  6. Chu NF, Rimm EB, Wang DJ, Liou HS, Shieh SM (1998) Clustering of cardiovascular disease risk factors among obese schoolchildren: the Taipei Children Heart Study. Am J Clin Nutr 67:1141–1146

    CAS  PubMed  Google Scholar 

  7. Cole TJ, Freeman JV, Preece MA (1995) Body mass index reference curves for the UK, 1990. Arch Dis Child 73:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Cole TJ, Green PJ (1992) Smoothing reference centile curves: the LMS method and penalized likelihood. Stat Med 11:1305–1319

    Article  CAS  Google Scholar 

  9. Cook S, Auinger P, Huang TT (2009) Growth curves for cardio-metabolic risk factors in children and adolescents. J Pediatr 155(S6):e15–e26

    Google Scholar 

  10. Cook S, Weitzman M, Auinger P, Nguyen M, Dietz WH (2003) Prevalence of a metabolic syndrome phenotype in adolescents: findings from the third National Health and Nutrition Examination Survey, 1988-1994. Archives of Pediatrics & Adolescent Medicine 157:821–827

    Article  Google Scholar 

  11. Costa RF, Santos NS, Goldraich NP, Barski TF, Andrade KS, Kruel LF (2012) Metabolic syndrome in obese adolescents: a comparison of three different diagnostic criteria. J Pediatr 88:303–309

    Google Scholar 

  12. D'Adamo E, Santoro N, Caprio S (2011) Metabolic syndrome in pediatrics: old concepts revised, new concepts discussed. Pediatr Clin N Am 58:1241–1255 xi

    Article  Google Scholar 

  13. Eisenmann JC, Laurson KR, DuBose KD, Smith BK, Donnelly JE (2010) Construct validity of a continuous metabolic syndrome score in children. Diabetology & Metabolic Syndrome 2:8

    Article  Google Scholar 

  14. Ford ES, Li C (2008) Defining the metabolic syndrome in children and adolescents: will the real definition please stand up? J Pediatr 152:160–164

    Article  PubMed  Google Scholar 

  15. Gonzalez-Gross M, Breidenassel C, Gomez-Martinez S, Ferrari M, Beghin L, Spinneker A, Diaz LE, Maiani G, Demailly A, Al-Tahan J, Albers U, Warnberg J, Stoffel-Wagner B, Jimenez-Pavon D, Libersa C, Pietrzik K, Marcos A, Stehle P (2008) Sampling and processing of fresh blood samples within a European multicenter nutritional study: evaluation of biomarker stability during transport and storage. International Journal of Obesity (2005) 32(Suppl 5):S66–S75

    Article  CAS  Google Scholar 

  16. Johnson WD, Kroon JJ, Greenway FL, Bouchard C, Ryan D, Katzmarzyk PT (2009) Prevalence of risk factors for metabolic syndrome in adolescents: National Health and Nutrition Examination Survey (NHANES), 2001-2006. Archives of Pediatrics & Adolescent Medicine 163:371–377

    Article  Google Scholar 

  17. Jolliffe CJ, Janssen I (2007) Development of age-specific adolescent metabolic syndrome criteria that are linked to the Adult Treatment Panel III and International Diabetes Federation criteria. J Am Coll Cardiol 49:891–898

    Article  PubMed  Google Scholar 

  18. Kassi E, Pervanidou P, Kaltsas G, Chrousos G (2011) Metabolic syndrome: definitions and controversies. BMC Medicine 9:48

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kelly AS, Steinberger J, Jacobs DR, Hong CP, Moran A, Sinaiko AR (2011) Predicting cardiovascular risk in young adulthood from the metabolic syndrome, its component risk factors, and a cluster score in childhood. International Journal of Pediatric Obesity : IJPO : an Official Journal of the International Association for the Study of Obesity 6:e283–e289

    Article  Google Scholar 

  20. Keskin M, Kurtoglu S, Kendirci M, Atabek ME, Yazici C (2005) 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 115:e500–e503

    Article  PubMed  Google Scholar 

  21. Mancini MC (2009) Metabolic syndrome in children and adolescents - criteria for diagnosis. Diabetology & Metabolic Syndrome 1:20

    Article  Google Scholar 

  22. Martino F, Puddu PE, Pannarale G, Colantoni C, Zanoni C, Martino E, Barilla F (2014) Metabolic syndrome among children and adolescents from Southern Italy: contribution from the Calabrian Sierras Community Study (CSCS). Int J Cardiol 177:455–460

    Article  PubMed  Google Scholar 

  23. Moreno LA, De Henauw S, Gonzalez-Gross M, Kersting M, Molnar D, Gottrand F, Barrios L, Sjostrom M, Manios Y, Gilbert CC, Leclercq C, Widhalm K, Kafatos A, Marcos A (2008) Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study. International journal of obesity (2005) 32(Suppl 5):S4–11

    Article  Google Scholar 

  24. Morrison JA, Friedman LA, Gray-McGuire C (2007) Metabolic syndrome in childhood predicts adult cardiovascular disease 25 years later: the Princeton Lipid Research Clinics Follow-up Study. Pediatrics 120:340–345

    Article  PubMed  Google Scholar 

  25. Nagy E, Vicente-Rodriguez G, Manios Y, Beghin L, Iliescu C, Censi L, Dietrich S, Ortega FB, De Vriendt T, Plada M, Moreno LA, Molnar D (2008) Harmonization process and reliability assessment of anthropometric measurements in a multicenter study in adolescents. International Journal of Obesity (2005) 32(Suppl 5):S58–S65

    Article  Google Scholar 

  26. Okosun IS, Lyn R, Davis-Smith M, Eriksen M, Seale P (2010) Validity of a continuous metabolic risk score as an index for modeling metabolic syndrome in adolescents. Ann Epidemiol 20:843–851

    Article  PubMed  Google Scholar 

  27. Pacifico L, Anania C, Martino F, Poggiogalle E, Chiarelli F, Arca M, Chiesa C (2011) Management of metabolic syndrome in children and adolescents. Nutrition, Metabolism, and Cardiovascular Diseases : NMCD 21:455–466

    Article  CAS  PubMed  Google Scholar 

  28. Pietrobelli A, Malavolti M, Battistini NC, Fuiano N (2008) Metabolic syndrome: a child is not a small adult. International Journal of Pediatric Obesity : IJPO : an Official Journal of the International Association for the Study of Obesity 3(Suppl 1):67–71

    Article  Google Scholar 

  29. Reinehr T, Wunsch R, Putter C, Scherag A (2013) Relationship between carotid intima-media thickness and metabolic syndrome in adolescents. J Pediatr 163:327–332

    Article  PubMed  Google Scholar 

  30. Sabin MA, Magnussen CG, Juonala M, Cowley MA, Shield JP (2012) The role of pharmacotherapy in the prevention and treatment of paediatric metabolic syndrome—implications for long-term health: part of a series on Pediatric Pharmacology, guest edited by Gianvincenzo Zuccotti, Emilio Clementi, and Massimo Molteni. Pharmacol Res 65:397–401

    Article  CAS  PubMed  Google Scholar 

  31. Sangun O, Dundar B, Kosker M, Pirgon O, Dundar N (2011) Prevalence of metabolic syndrome in obese children and adolescents using three different criteria and evaluation of risk factors. Journal of Clinical Research in Pediatric Endocrinology 3:70–76

    Article  PubMed  PubMed Central  Google Scholar 

  32. Schwandt P, Kelishadi R, Haas GM (2010) Ethnic disparities of the metabolic syndrome in population-based samples of german and Iranian adolescents. Metab Syndr Relat Disord 8:189–192

    Article  PubMed  Google Scholar 

  33. Steene-Johannessen J, Kolle E, Anderssen SA, Andersen LB (2009) Cardiovascular disease risk factors in a population-based sample of Norwegian children and adolescents. Scand J Clin Lab Invest 69:380–386

    Article  PubMed  Google Scholar 

  34. Tailor AM, Peeters PH, Norat T, Vineis P, Romaguera D (2010) An update on the prevalence of the metabolic syndrome in children and adolescents. International Journal of Pediatric Obesity : IJPO : an Official Journal of the International Association for the Study of Obesity 5:202–213

    Article  Google Scholar 

  35. Wilson PW, D'Agostino RB, Parise H, Sullivan L, Meigs JB (2005) Metabolic syndrome as a precursor of cardiovascular disease and type 2 diabetes mellitus. Circulation 112:3066–3072

    Article  CAS  PubMed  Google Scholar 

  36. Zimmet P, Alberti KG, Kaufman F, Tajima N, Silink M, Arslanian S, Wong G, Bennett P, Shaw J, Caprio S (2007) The metabolic syndrome in children and adolescents - an IDF consensus report. Pediatr Diabetes 8:299–306

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to all of the adolescents that took part in the HELENA study and to all researchers who set up the data for further analysis. Many thanks to Petra Pickert and Anke Carstensen for their contribution to laboratory work.

Author contributions

TV and ES performed the statistical analyses and drafted the manuscript. KV and IH launched the idea and supervised the full process of the manuscript development. CCS and FO performed extra statistical analyses and reviewed the manuscript. LAM coordinated the HELENA study. CB, MGG, FG, LB, DM, YM, MJG, KW, CL, JD, MA, AK, MJC, and SDH critically reviewed the manuscript. All authors approved the final version of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Medicine and Health Sciences, Ghent University, Ghent, Belgium

    Tine Vanlancker & Emmily Schaubroeck

  2. Department of Public Health, Ghent University, Ghent, Belgium

    Krishna Vyncke, Stefaan De Henauw & Inge Huybrechts

  3. PROFITH “PROmoting FITness and Health through physical activity” Research Group, Department of Physical Education and Sports, Faculty of Sport Sciences, University of Granada, Granada, Spain

    Cristina Cadenas-Sanchez & Francisco B. Ortega

  4. Institut für Ernährungs und Lebensmittelwissenschaften Ernährungphysiologie, Rheinische Friedrich Wilhelms, Universität Bonn, Bonn, Germany

    Christina Breidenassel

  5. ImFINE Research Group, Faculty of Physical Activity and Sport-INEF, Department of Health and Human Performance, Technical University of Madrid, Madrid, Spain

    Christina Breidenassel & Marcela González-Gross

  6. CIBER: CB12/03/30038 Fisiopatología de la Obesidad y la Nutrición, CIBERobn, Instituto de Salud Carlos III (ISCIII), Madrid, Spain

    Marcela González-Gross

  7. Inserm, CHU Lille, U995—LIRIC—Lille Inflammation Research International Center, Université Lille, 59000, Lille, France

    Frederic Gottrand & Laurent Beghin

  8. Inserm, CHU Lille, CIC 1403—Centre d’investigation clinique, Université Lille, 59000, Lille, France

    Frederic Gottrand & Laurent Beghin

  9. GENUD—Growth, Exercise, Nutrition and Development, University of Zaragoza, Zaragoza, Spain

    Luis A. Moreno

  10. School of Health Sciences, University of Zaragoza, Zaragoza, Spain

    Luis A. Moreno

  11. Medical Faculty, Department of Paediatrics, University of Pécs, Pécs, Hungary

    Denes Molnár

  12. Department of Nutrition and Dietetics, School of Health Science and Education, Harokopio University, Athens, Greece

    Yannis Manios

  13. Department of Paediatrics, Private Medical University Salzburg, Salzburg, Austria

    Kurt Widhalm

  14. INRAN (National Research Institute on Food and Nutrition), Rome, Italy

    Catherine Leclercq

  15. Department of Epidemiology and Public Health, U-744 INSERM, Institut Pasteur de Lille, Universite Lille Nord de France, Lille, France

    Jean Dallongeville

  16. Food Science and Technology and Nutrition Institute, Spanish National Research Council, Metabolism and Nutrition, Immunonutrition Research Group, Madrid, Spain

    Marcos Ascensión

  17. School of Medicine, Preventive Medicine and Nutrition Unit, Heraklion, University of Crete, Crete, Greece

    Anthony Kafatos

  18. Department of Medical Physiology, School of Medicine, Granada University, Granada, Spain

    Manuel J. Castillo

  19. Department of Biosciences and Nutrition, Karolinska Institutet, Huddinge, Sweden

    Francisco B. Ortega

  20. International Agency for Research on Cancer, 150 Cours Albert Thomas, 69372, Lyon CEDEX 08, France

    Marc J. Gunter & Inge Huybrechts

Authors
  1. Tine Vanlancker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmily Schaubroeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Krishna Vyncke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristina Cadenas-Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christina Breidenassel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marcela González-Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Frederic Gottrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Luis A. Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Laurent Beghin
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Denes Molnár
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yannis Manios
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Marc J. Gunter
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Kurt Widhalm
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Catherine Leclercq
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jean Dallongeville
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Marcos Ascensión
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Anthony Kafatos
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Manuel J. Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Stefaan De Henauw
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Francisco B. Ortega
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Inge Huybrechts
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

on behalf of the HELENA project group*

Corresponding author

Correspondence to Inge Huybrechts.

Ethics declarations

Funding

The HELENA study took place with the financial support of the European Community Sixth RTD Framework Programme (Contract FOOD-CT-2005-007034). KV is financially supported by the Research Foundation Flanders (FWO). CCS is supported by a grant from the Spanish Ministry of Economy and Competitiveness (BES-2014-068829). FBO is supported by a grant from the Spanish Ministry of Science and Innovation (RYC-2011-09011).

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Additional information

Communicated by Mario Bianchetti

*The authors of this paper take sole responsibility for its content. See Supplemental Material for a complete list of the HELENA project members.

Revisions received: 7 December 2016; 9 December 2016

Electronic supplementary material

ESM 1

(DOCX 23.7 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vanlancker, T., Schaubroeck, E., Vyncke, K. et al. Comparison of definitions for the metabolic syndrome in adolescents. The HELENA study. Eur J Pediatr 176, 241–252 (2017). https://doi.org/10.1007/s00431-016-2831-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-016-2831-6

Keywords

Search

Navigation