Skip to main content
SpringerLink
Log in

Effects of obstructive sleep apnea severity on serum lipid levels in Greek children with snoring

  • Original Article
  • Published:
Sleep and Breathing Aims and scope Submit manuscript

Abstract

Background

Although obstructive sleep apnea (OSA) is related to dyslipidemia in adults, limited data are available regarding its effects on serum lipids during childhood. Aim of this study was to assess the potential relationships between severity of OSA and cholesterol or triglyceride levels in a cohort of Greek children.

Methods

Data from children with snoring who underwent polysomnography and complete serum lipids measurements during a specified study period were analyzed retrospectively.

Results

Overall, obese children (n = 261) had lower HDL cholesterol levels than non-obese subjects (n = 113) (49.6 ± 10.5 vs. 53.9 ± 11.4 mg/dL; p = 0.001) and higher triglyceride concentrations (69.8 ± 32.2 vs. 63.2 ± 27 mg/dL; p = 0.041). Non-obese subjects with moderate-to-severe OSA did not differ in triglycerides, total, and LDL cholesterol concentrations but had lower HDL cholesterol, when compared to non-obese children with primary snoring/mild OSA (50.4 ± 13.1 vs. 54.9 ± 10.7 mg/dL; p = 0.008). The risk for having low HDL cholesterol (≤40 mg/dL) was threefold higher in non-obese subjects with moderate-to-severe OSA than in those with primary snoring/mild OSA, even after adjustment for age and gender [OR = 3.44 (95% CI 1.44 to 8.24; p = 0.006)]. Concentrations of serum lipids in obese children were not associated with severity of OSA. HDL cholesterol was 48.5 ± 8.7 mg/dL in subjects with moderate-to-severe OSA and 50.0 ± 11.1 mg/dL in children with primary snoring/mild OSA (p = 0.519).

Conclusions

HDL cholesterol levels are inversely related to severity of OSA in non-obese children with snoring.

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

Similar content being viewed by others

References

  1. Shahar E, Whitney CW, Redline S, Lee ET, Newman AB, Javier Nieto F, O'Connor GT, Boland LL, Schwartz JE, Samet JM (2001) Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 163:19–25

    PubMed  CAS  Google Scholar 

  2. Marin JM, Carrizo SJ, Vicente E, Agusti AG (2005) Long-term cardiovascular outcomes in men with obstructive sleep apnoea–hypopnoea with or without treatment with continuous positive airway pressure: an observational study. Lancet 365:1046–1053

    PubMed  Google Scholar 

  3. Somers VK, White DP, Amin R, Abraham WT, Costa F, Culebras A, Daniels S, Floras JS, Hunt CE, Olson LJ, Pickering TG, Russell R, Woo M, Young T (2008) Sleep apnea and cardiovascular disease: an American Heart Association/American College of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing. J Am Coll Cardiol 52:686–717

    Article  PubMed  Google Scholar 

  4. Kaditis AG, Alexopoulos EI, Damani E, Hatzi F, Chaidas K, Kostopoulou T, Tzigeroglou A, Gourgoulianis K (2009) Urine levels of catecholamines in Greek children with obstructive sleep-disordered breathing. Pediatr Pulmonol 44:38–45

    Article  PubMed  Google Scholar 

  5. Snow AB, Khalyfa A, Serpero LD, Capdevila OS, Kim J, Buazza MO, Gozal D (2009) Catecholamine alterations in pediatric obstructive sleep apnea: effect of obesity. Pediatr Pulmonol 44:559–567

    Article  PubMed  Google Scholar 

  6. Kaditis AG, Alexopoulos EI, Kalampouka E, Kostadima E, Angelopoulos N, Germenis A, Zintzaras E, Gourgoulianis K (2004) Morning levels of fibrinogen in children with sleep-disordered breathing. Eur Respir J 24:790–797

    Article  PubMed  CAS  Google Scholar 

  7. Tauman R, Ivanenko A, O'Brien LM, Gozal D (2004) Plasma C-reactive protein levels among children with sleep-disordered breathing. Pediatrics 113:e564–e569

    Article  PubMed  Google Scholar 

  8. Redline S, Storfer-Isser A, Rosen CL, Johnson NL, Kirchner HL, Emancipator J, Kibler AM (2007) Association between metabolic syndrome and sleep-disordered breathing in adolescents. Am J Respir Crit Care Med 176:401–408

    Article  PubMed  Google Scholar 

  9. Verhulst SL, Schrauwen N, Haentjens D, Rooman RP, Van Gaal L, De Backer WA, Desager KN (2007) Sleep-disordered breathing and the metabolic syndrome in overweight and obese children and adolescents. J Pediatr 150:608–612

    Article  PubMed  CAS  Google Scholar 

  10. Gozal D, Kheirandish-Gozal L, Serpero LD, Sans Capdevila O, Dayyat E (2007) Obstructive sleep apnea and endothelial function in school-aged nonobese children: effect of adenotonsillectomy. Circulation 116:2307–2314

    Article  PubMed  Google Scholar 

  11. Li J, Bosch-Marce M, Nanayakkara A, Savransky V, Fried SK, Semenza GL, Polotsky VY (2006) Altered metabolic responses to intermittent hypoxia in mice with partial deficiency of hypoxia-inducible factor-1alpha. Physiol Genomics 25:450–457

    Article  PubMed  CAS  Google Scholar 

  12. Iiyori N, Alonso LC, Li J, Sanders MH, Garcia-Ocana A, O'Doherty RM, Polotsky VY, O'Donnell CP (2007) Intermittent hypoxia causes insulin resistance in lean mice independent of autonomic activity. Am J Respir Crit Care Med 175:851–857

    Article  PubMed  CAS  Google Scholar 

  13. Newman AB, Nieto FJ, Guidry U, Lind BK, Redline S, Pickering TG, Quan SF (2001) Relation of sleep-disordered breathing to cardiovascular disease risk factors: the sleep heart health study. Am J Epidemiol 154:50–59

    Article  PubMed  CAS  Google Scholar 

  14. Gozal D, Capdevila OS, Kheirandish-Gozal L (2008) Metabolic alterations and systemic inflammation in obstructive sleep apnea among nonobese and obese prepubertal children. Am J Respir Crit Care Med 177:1142–1149

    Article  PubMed  CAS  Google Scholar 

  15. Kaditis AG, Alexopoulos EI, Damani E, Karadonta I, Kostadima E, Tsolakidou A, Gourgoulianis K, Syrogiannopoulos GA (2005) Obstructive sleep-disordered breathing and fasting insulin levels in nonobese children. Pediatr Pulmonol 40:515–523

    Article  PubMed  Google Scholar 

  16. Li AM, Chan MH, Chan DF, Lam HS, Wong EM, So HK, Chan IH, Lam CW, Nelson EA (2006) Insulin and obstructive sleep apnea in obese Chinese children. Pediatr Pulmonol 41:1175–1181

    Article  PubMed  Google Scholar 

  17. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL (2002) 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 11:1–190

    Google Scholar 

  18. Ogden CL, Flegal KM, Carroll MD, Johnson CL (2002) Prevalence and trends in overweight among US children and adolescents, 1999–2000. Jama 288:1728–1732

    Article  PubMed  Google Scholar 

  19. Kaditis AG, Alexopoulos E, Chaidas K, Ntamagka G, Karathanasi A, Tsilioni I, Kiropoulos TS, Zintzaras E, Gourgoulianis K (2009) Urine concentrations of cysteinyl leukotrienes in children with obstructive sleep-disordered breathing. Chest 135:1496–1501

    Article  PubMed  CAS  Google Scholar 

  20. American Thoracic Society (1996) Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med 153:866–878

    Google Scholar 

  21. 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. Arch Pediatr Adolesc Med 157:821–827

    Article  PubMed  Google Scholar 

  22. McArdle N, Hillman D, Beilin L, Watts G (2007) Metabolic risk factors for vascular disease in obstructive sleep apnea: a matched controlled study. Am J Respir Crit Care Med 175:190–195

    Article  PubMed  CAS  Google Scholar 

  23. Tauman R, O'Brien LM, Ivanenko A, Gozal D (2005) Obesity rather than severity of sleep-disordered breathing as the major determinant of insulin resistance and altered lipidemia in snoring children. Pediatrics 116:e66–e73

    Article  PubMed  Google Scholar 

  24. Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA (1998) Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med 338:1650–1656

    Article  PubMed  CAS  Google Scholar 

  25. de Ferranti SD, Gauvreau K, Ludwig DS, Neufeld EJ, Newburger JW, Rifai N (2004) Prevalence of the metabolic syndrome in American adolescents: findings from the Third National Health and Nutrition Examination Survey. Circulation 110:2494–2497

    Article  PubMed  Google Scholar 

  26. 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 

  27. Stokes KY, Cooper D, Tailor A, Granger DN (2002) Hypercholesterolemia promotes inflammation and microvascular dysfunction: role of nitric oxide and superoxide. Free Radic Biol Med 33:1026–1036

    Article  PubMed  CAS  Google Scholar 

  28. Stokes KY, Granger DN (2005) Hypercholesterolemia: its impact on ischemia–reperfusion injury. Expert Rev Cardiovasc Ther 3:1061–1070

    Article  PubMed  CAS  Google Scholar 

  29. Waters KA, Sitha S, O'Brien LM, Bibby S, de Torres C, Vella S, de la Eva R (2006) Follow-up on metabolic markers in children treated for obstructive sleep apnea. Am J Respir Crit Care Med 174:455–460

    Article  PubMed  CAS  Google Scholar 

  30. Robinson GV, Pepperell JC, Segal HC, Davies RJ, Stradling JR (2004) Circulating cardiovascular risk factors in obstructive sleep apnoea: data from randomised controlled trials. Thorax 59:777–782

    Article  PubMed  CAS  Google Scholar 

  31. Li J, Grigoryev DN, Ye SQ, Thorne L, Schwartz AR, Smith PL, O'Donnell CP, Polotsky VY (2005) Chronic intermittent hypoxia upregulates genes of lipid biosynthesis in obese mice. J Appl Physiol 99:1643–1648

    Article  PubMed  CAS  Google Scholar 

  32. Li J, Thorne LN, Punjabi NM, Sun CK, Schwartz AR, Smith PL, Marino RL, Rodriguez A, Hubbard WC, O'Donnell CP, Polotsky VY (2005) Intermittent hypoxia induces hyperlipidemia in lean mice. Circ Res 97:698–706

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

None of the authors have any conflicts of interest to disclose.

Author information

Authors and Affiliations

  1. Sleep Disorders Laboratory, University of Thessaly School of Medicine, Larissa, Greece

    Emmanouel I. Alexopoulos, Eleni Kostadima, Dimitrios Kaditis, Epameinondas Zakynthinos, Konstantinos Gourgoulianis & Athanasios Kaditis

  2. Department of Otorhinolaryngology, Larissa University Hospital, Larissa, Greece

    Eleftheria Gletsou

Authors
  1. Emmanouel I. Alexopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eleftheria Gletsou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eleni Kostadima
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dimitrios Kaditis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Epameinondas Zakynthinos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Konstantinos Gourgoulianis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Athanasios Kaditis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Athanasios Kaditis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alexopoulos, E.I., Gletsou, E., Kostadima, E. et al. Effects of obstructive sleep apnea severity on serum lipid levels in Greek children with snoring. Sleep Breath 15, 625–631 (2011). https://doi.org/10.1007/s11325-010-0410-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11325-010-0410-z

Keywords

Search

Navigation