Skip to main content

Prevalence and features of metabolic syndrome in childhood-onset systemic lupus erythematosus

Abstract

To estimate the prevalence and features of metabolic syndrome (MetS) in childhood-onset systemic lupus erythematosus (cSLE), we performed a cross-sectional study of 76 consecutive cSLE patients and 54 healthy controls, age and sex matched. All individuals were assessed for anthropometric and MetS features according to World Health Organization (WHO), NCEP Adult Treatment Panel III (NCEP-ATP III), and International Diabetes Federation (IDF) criteria. The cSLE patients were further assessed for clinical and laboratory manifestations, disease activity (Systemic Lupus Erythematosus Disease Activity Index), cumulative damage (Systemic Lupus International Collaborating Clinics (SLICC)), and current and cumulative drug exposures. Sixty-nine (90.8%) patients were female with mean age of 16.8 years [standard deviation (SD) ±4.0 years]. Mean disease duration was 4.8 years (SD ± 4.1). Based on the WHO MetS criteria, MetS was observed in two (2.6%) cSLE patients. We observed high prevalence of the MetS in cSLE patients according to NCEP-ATP III MetS criteria (18.4%) (p = 0.002) and according to IDF MetS criteria (17.1%) (p = 0.003). We did not observe MetS in the control group. No difference in cSLE patients <18 and ≥18 years was observed. We observed an association between the presence of MetS and SLICC scores in cSLE <18 years and cumulative corticosteroid dose adjusted by weight in cSLE ≥18 years. This study showed that MetS is frequently observed in cSLE using NCEP-ATP III MetS criteria and IDF MetS criteria. The identification of MetS is important to indicate cardiovascular morbidity and mortality in cSLE.

This is a preview of subscription content, access via your institution.

References

  1. Mohan C, Datta SK (1995) Lupus: key pathogenic mechanisms and contributing factors. Clin Imunnol Immunophatol 77:209–220

    CAS  Article  Google Scholar 

  2. Bader-Meunier B (2005) Initial presentation of childhood-onset systemic lupus erythematosus: a French multicenter study. J Pediatr 146:648–653

    CAS  Article  PubMed  Google Scholar 

  3. Taddio A, Rosseto E, Rosé CD, Brescia AM, Bracaglia C, Cortis E, Rigante D, Stabile A, Montico M, Ronfani L, Ventura A, Lepore L (2010) Prognostic impact of atypical presentation in pediatric systemic lupus erythematosus: results from a multicenter study. J Pediatr 156:972–977

    Article  PubMed  Google Scholar 

  4. von Scheven E, Bakkaloglu A (2009) What’s new in paediatric SLE? Best Pract Res Clin Rheumatol 23:699–708

    Article  Google Scholar 

  5. Tucker LB, Menon S, Schaller JG, Isenberg DA (1995) Adult and childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology and outcome. Br J Rheum 34:866–872

    CAS  Article  Google Scholar 

  6. Ravelli A, Ruperto N, Martini A (2005) Outcome in juvenile onset systemic lupus erythematosus. Curr Opin Rheumatol 17:568–573

    Article  PubMed  Google Scholar 

  7. Mina R, Brunner HI (2010) Pediatric lupus—are their differences in presentation, genetics, response to therapy, and damage accrual compared with adult lupus? Rheum Dis Clin N Am 36:53–80

    Article  Google Scholar 

  8. Parker B, Bruce IN (2010) The metabolic syndrome in systemic lupus erythematosus. Rheum Dis Clin N Am 36:81–97

    Article  Google Scholar 

  9. Telles R, Lanna C, Ferreira G, Ribeiro A (2010) Metabolic syndrome in patients with systemic lupus erythematosus: association with traditional risk factors for coronary heart disease and lupus characteristics. Lupus 19:803–809

    Article  PubMed  Google Scholar 

  10. Zonana-Nacach A, Santana-Sahagún E, Jiménez-Balderas FJ, Camargo-Coronel A (2008) Prevalence and factors associated with metabolic syndrome in patients with rheumatoid arthritis and systemic lupus erythematosus. J Clin Rheumatol 14:74–77

    Article  PubMed  Google Scholar 

  11. Bultink IEM, Turkstra F, Diamant M, Dijmans BAC, Voskuyl E (2008) Prevalence of and risk factors for the metabolic syndrome in women with systemic lupus erythematosus. Clin Exp Rheumatol 26:32–38

    CAS  PubMed  Google Scholar 

  12. Mok CC, Poon WL, Lai JPS, Wong CK, Chiu SM, Wong CK, Lun SWM, Ko GTC, Lam CWK, Lam CS (2010) Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus. Scand J Rheumatol 39:42–49

    CAS  Article  PubMed  Google Scholar 

  13. Vilar MJP, Bezerra ELM, Silva TMA, Gadelha RGN, Fernandes HS, Gama AP et al (2006) Prevalence of metabolic syndrome and its components in Brazilian women with systemic lupus erythematosus: implications for cardiovascular risk. Ann Rheum Dis 64(Suppl III):362–363

    Google Scholar 

  14. Medeiros MM, Xavier de Oliveira ÍM, Ribeiro ÁT (2016) Prevalence of metabolic syndrome in a cohort of systemic lupus erythematosus patients from northeastern Brazil: association with disease activity, nephritis, smoking, and age. Rheumatol Int 36:117–124

    CAS  Article  PubMed  Google Scholar 

  15. Lozovoy MA, Simão AN, Hohmann MS, Simão TN, Barbosa DS, Morimoto HK, Reiche EM, Cecchini R, Dichi I (2011) Inflammatory biomarkers and oxidative stress measurements in patients with systemic lupus erythematosus with or without metabolic syndrome. Lupus 20:1356–1364

    CAS  Article  PubMed  Google Scholar 

  16. Muniz LF, Pereira RM, Silva TF, Bonfá E, Borba EF (2015) Impact of therapy on metabolic syndrome in young adult premenopausal female lupus patients: beneficial effect of antimalarials. Arthritis Care Res (Hoboken) 67:1255–1262

    Article  Google Scholar 

  17. Azevedo GD, Gadelha RG, Vilar MJ (2007) Metabolic syndrome in systemic lupus erythematosus: lower prevalence in Brazil than in the USA. Ann Rheum Dis 66:1542

    Article  PubMed  PubMed Central  Google Scholar 

  18. Rodríguez-Morán M, Salazar-Vázquez B, Violante R, Guerrero-Romero F (2004) Metabolic syndrome among children and adolescents aged 10–18 years. Diabetes Care 27:2516–2517

    Article  PubMed  Google Scholar 

  19. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of the systemic lupus erythematosus (letter). Arthritis Rheum 40:1725

    CAS  Article  PubMed  Google Scholar 

  20. ACR Ad Hoc Committee on Neuropsychiatric Lupus Nomencalture (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42:599–608

    Article  Google Scholar 

  21. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The committee on prognosis studies in SLE. Arthritis Rheum 35:630–640

    CAS  Article  PubMed  Google Scholar 

  22. Yee CS, Farewell VT, Isenberg DA, Griffiths B, Teh LS, Bruce IN, Ahmad Y, Rahman A, Prabu A, Akil M, McHugh N, Edwards C, D'Cruz D, Khamashta MA, Gordon C (2011) The use of systemic lupus erythematosus disease activity index-2000 to define active disease and minimal clinically meaningful change based on data from a large cohort of systemic lupus erythematosus patients. Rheumatology (Oxford) 50:982–988

    Article  Google Scholar 

  23. Ibañez D, Urowitz MB, Gladman DD (2003) Summarizing disease features over time: I. Adjusted mean SLEDAI derivation and application to an index of disease activity in lupus. J Rheumatol 30:1977–1982

    PubMed  Google Scholar 

  24. Gladman D, Ginzler E, Goldsmith C et al (1999) The development and initial validation of the systemic lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39:363–369

    Article  Google Scholar 

  25. Physical status (1995) The use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 854:1–452

    Google Scholar 

  26. Ford ES, Giles WH (2003) A comparison of the prevalence of the metabolic syndrome using two proposed definitions. Diabetes Care 26:575–581

    Article  PubMed  Google Scholar 

  27. Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WPT, Loria CM, Smith SC Jr (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:1640–1645

    CAS  Article  PubMed  Google Scholar 

  28. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) Expert Panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 285:2486–2497

    Article  Google Scholar 

  29. Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus. Provisional report of a WHO consultation. Diabet Med 15:539–593

    CAS  Article  PubMed  Google Scholar 

  30. Mina R, Klein-Gitelman MS, Nelson S, Eberhard BA, Higgins G, Singer NG, Onel K, Tucker L, O'Neil KM, Punaro M, Levy DM, Haines K, Ying J, Brunner HI (2015) Effects of obesity on health-related quality of life in juvenile-onset systemic lupus erythematosus. Lupus 24:191–197

    CAS  Article  PubMed  Google Scholar 

  31. Kozu KT, Silva CA, Bonfá E, Sallum AM, Pereira RM, Viana VS, Borba E, Campos LM (2013) Dyslipidaemia in juvenile dermatomyositis: the role of disease activity. Clin Exp Rheumatol 31:638–644

    PubMed  Google Scholar 

  32. Parker B, Urowitz MB, Gladman DD et al (2015) Impact of early disease factors on metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort. Ann Rheum Dis 74:1530–1536

    Article  PubMed  Google Scholar 

  33. Posadas-Romero C, Torres-Tamayo M, Zamora-González J, Aguilar-Herrera BE, Posadas-Sánchez R, Cardoso-Saldaña G, Ladrón de Guevara G, Solis-Vallejo E, El Hafidi M (2004) High insulin levels and increased low-density lipoprotein oxidizability in pediatric patients with systemic lupus erythematosus. Arthritis Rheum 50:160–165

    CAS  Article  PubMed  Google Scholar 

  34. Parker B, Urowitz MB, Gladman D et al (2013) Clinical associations of the metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort. Ann Rheum Dis 72:1308–1314

    Article  PubMed  Google Scholar 

  35. Demir S, Artim-Esen B, Şahinkaya Y, Pehlivan Ö, Alpay-Kanıtez N, Omma A, Erer B, Kamalı S, Gül A, Aral O, Öcal L, İnanç M (2016) Metabolic syndrome is not only a risk factor for cardiovascular diseases in systemic lupus erythematosus but is also associated with cumulative organ damage: a cross-sectional analysis of 311 patients. Lupus 25:177–184

    CAS  Article  PubMed  Google Scholar 

  36. Cheung BM, Ong KL, Man YB, Wong LY, Lau CP, Lam KS (2006) Prevalence of the metabolic syndrome in the United States national health and nutrition examination survey 1999–2002 according to different defining criteria. J Clin Hypertens (Greenwich) 8:562–570

    Article  Google Scholar 

  37. Cook S, Weitzman M, Auinger P, Nguyen M, Dietz WH (2003) Prevalence of a metabolic syndrome phenotype in adolescents. Arch Pediatr Adolesc Med 157:821–827

    Article  PubMed  Google Scholar 

  38. Duncan GE, Li SM, Zhou XH (2004) Prevalence and trends of a metabolic syndrome phenotype among U.S. adolescents, 1999–2000. Diabetes Care 27:2438–2443

    Article  PubMed  Google Scholar 

  39. Kim HM, Park J, Kim HS, Kim DH (2007) Prevalence of the metabolic syndrome in Korean adolescents aged 12–19 years from the Korean National Health and Nutrition Examination Survey 1998 and 2001. Diabetes Care 30:701–706

    CAS  Article  PubMed  Google Scholar 

  40. Agirbasli M, Cakir S, Ozme S, Ciliv G (2006) Metabolic syndrome in Turkish children and adolescents. Metabolism 55:1002–1006

    CAS  Article  PubMed  Google Scholar 

  41. Esmaillzadeh A, Mirmiran P, Azadbakht L, Etemadi A, Azizi F (2006) High prevalence of the metabolic syndrome in Iranian adolescents. Obesity (Silver Spring) 14:377–382

    Article  Google Scholar 

  42. Seki M, Matsuo T, Carrilho AJ (2009) Prevalence of metabolic syndrome and associated risk factors in Brazilian schoolchildren. Public Health Nutr 12:947–952

    Article  PubMed  Google Scholar 

  43. Rinaldi AE, Pimentel GD, Pereira AF, Gabriel GF, Moreto F, Burini RC (2010) Metabolic syndrome in overweight children from the city of Botucatu—Sao Paulo State—Brazil: agreement among six diagnostic criteria. Diabetol Metab Syndr 2:39

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Simone Appenzeller.

Ethics declarations

Disclosures

None.

Grants

Grants were provided by Fundação Apoio À Pesquisa Estado São Paulo-Brasil (FAPESP 2008/02917-0 and 2009/06049-6 and 2009/15286-1) and Conselho Nacional Pesquisa Desenvolvimento-Brasil CNPq (300447/2009-4 and 471343/2011-0 and 302205/2012-8 and 473328/2013-5 and 157534/2015-4).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sinicato, N.A., Postal, M., de Oliveira Peliçari, K. et al. Prevalence and features of metabolic syndrome in childhood-onset systemic lupus erythematosus. Clin Rheumatol 36, 1527–1535 (2017). https://doi.org/10.1007/s10067-017-3602-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-017-3602-0

Keywords

  • Childhood-onset systemic lupus erythematosus
  • Metabolic syndrome