Association of sleep characteristics with adiposity markers in children
-
Theresa Herttrich
Abstract
Background
Accumulating evidence suggests a relationship between sleep alterations and overweight/obesity in children. Our aim was to investigate the association of sleep measures other than obstructive sleep apnea or sleep duration with overweight/obesity and metabolic function in children.
Methods
We conducted a prospective cohort study in school- aged children (aged 5 to 8 years, prepubertal, and 12 to 15 years, pubertal) with overweight/obesity and normal-weight children. All children underwent a standardized in-laboratory polysomnography followed by a fasting blood assessment for glucose and metabolic testing. Subjective sleep measures were investigated by a 7-day sleep diary and questionnaire. We analyzed prepubertal and pubertal groups separately using logistic regression and partial correlation analyses.
Results
A total of 151 participants were analyzed. Overweight/obese children had significantly higher odds for arousal index (prepubertal children: 1.28, Confidence interval (CI): 1.06, 1.67; pubertal children: 1.65, CI: 1.19, 2.29) than normal-weight children, independent of age and gender. In prepubertal children, arousal-index was positively associated with C-peptide (r=0.30, p=0.01), whereas Minimum O2 saturation was negatively associated with triglycerides (r=−0.34, p=0.005), adjusting for age and sex. However, associations were attenuated by further adjustment for body mass index standard deviation scores (BMI-SDS). In pubertal children, higher level of apnea-hypopnea-index and pCO2 predicted increased lipoprotein (a) levels (r=0.35, p=0.03 and r=0.40, p=0.01, respectively), independent of age, sex, and BMI-SDS. A negative association was found between pCO2 and high-density lipoprotein (HDL)-cholesterol (r=−0.40, p=0.01).
Conclusions
Overall, we report that sleep quality as measured by arousal index may be compromised by overweight and obesity in children and warrants attention in future intervention programs.
Funding source: German Diabetes Association
Funding source: German Federal Ministry of Education and Research
Funding source: European Union
Funding source: European Regional Development Fund
Funding source: Tuebinger Program for the Advancement of Women in Science
Research funding: This work was supported by the German Diabetes Association and by the German Federal Ministry of Education and Research (IFB and Competence Network Adiposity). LIFE is funded by the European Union, by the European Regional Development Fund and by means of the Free State of Saxony within the framework of the excellence initiative. Dr. Quante was supported from the Tuebinger Program for the Advancement of Women in Science.
Author Contribution Statement: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission. Study design: AH, AK, WK and MQ. Data collection: TH, JD, JKl and KS. Analysis: TH, JD, JKr and MQ. Interpretation: TH, JD, AM, OJ and MQ. Manuscript preparation: TH, JD, MQ and WK.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
Informed consent: Informed consent was obtained from all individuals included in this study.
Ethical approval: This study was conducted according to the guidelines laid down in the Declaration of Helsinki, and the Ethics committee of the University of Leipzig approved all procedures (Reg. No. 144-2009-06072009).
References
1. Cappuccio, FP, Taggart, FM, Kandala, N-B, Currie, A, Peile, E, Stranges, S, et al. Meta-analysis of short sleep duration and obesity in children and adults. Sleep 2008;31:619–26. https://doi.org/10.1093/sleep/31.5.619.10.1093/sleep/31.5.619Search in Google Scholar
2. Patel, SR, Blackwell, T, Redline, S, Ancoli-Israel, S, Cauley, JA, Hillier, TA, et al. The association between sleep duration and obesity in older adults. Int J Obes 2005;32:1825–34. https://doi.org/10.1038/ijo.2008.198.10.1038/ijo.2008.198Search in Google Scholar
3. Cespedes Feliciano, EM, Quante, M, Rifas-Shiman, SL, Redline, S, Oken, E, Taveras, EM. Objective sleep characteristics and cardiometabolic health in young adolescents. Pediatrics 2018;142. https://doi.org/10.1542/peds.2017-4085.10.1542/peds.2017-4085Search in Google Scholar
4. Guilleminault, C, Korobkin, R, Winkle, R. A review of 50 children with obstructive sleep apnea syndrome. Lung 1981;159:275–87. https://doi.org/10.1007/bf02713925.10.1007/BF02713925Search in Google Scholar
5. Marcus, CL, Curtis, S, Koerner, CB, Joffe, A, Serwint, JR, Loughlin, GM. Evaluation of pulmonary function and polysomnography in obese children and adolescents. Pediatr Pulmonol 1996;21:176–83. https://doi.org/10.1002/(sici)1099-0496(199603)21:3<176::aid-ppul5>3.0.co;2-o.10.1002/(SICI)1099-0496(199603)21:3<176::AID-PPUL5>3.0.CO;2-OSearch in Google Scholar
6. Alonso-Álvarez, ML, Cordero-Guevara, JA, Terán-Santos, J, Gonzalez-Martinez, M, Jurado-Luque, MJ, Corral-Peñafiel, J, et al. Obstructive sleep apnea in obese community-dwelling children: the NANOS study. Sleep 2014;37:943–9. https://doi.org/10.5665/sleep.3666.10.5665/sleep.3666Search in Google Scholar
7. Alonso-Alvarez, ML, Teran-Santos, J, Gonzalez Martinez, M, Cordero-Guevara, JA, Jurado-Luque, MJ, Corral-Penafiel, J, et al. Metabolic biomarkers in community obese children: effect of obstructive sleep apnea and its treatment. Sleep Med 2017;37:1–9. https://doi.org/10.1016/j.sleep.2017.06.002.10.1016/j.sleep.2017.06.002Search in Google Scholar
8. Hakim, F, Kheirandish-Gozal, L, Gozal, D. Obesity and altered sleep: a pathway to metabolic derangements in children?. Semin Pediatr Neurol 2015;22:77–85. https://doi.org/10.1016/j.spen.2015.04.006.10.1016/j.spen.2015.04.006Search in Google Scholar
9. Montag, SE, Knutson, KL, Zee, PC, Goldberger, JJ, Ng, J, Kim, KA, et al. Association of sleep characteristics with cardiovascular and metabolic risk factors in a population sample: the Chicago area sleep study. Sleep Health 2017;3:107–12. https://doi.org/10.1016/j.sleh.2017.01.003.10.1016/j.sleh.2017.01.003Search in Google Scholar
10. Vgontzas, AN, Bixler, EO, Tan, TL, Kantner, D, Martin, LF, Kales, A. Obesity without sleep apnea is associated with daytime sleepiness. Arch Intern Med 1998;158:1333–7. https://doi.org/10.1001/archinte.158.12.1333.10.1001/archinte.158.12.1333Search in Google Scholar
11. Resta, O, Foschino Barbaro, MP, Bonfitto, P, Giliberti, T, Depalo, A, Pannacciulli, N, et al. Low sleep quality and daytime sleepiness in obese patients without obstructive sleep apnoea syndrome. J Intern Med 2003;253:536–43. https://doi.org/10.1046/j.1365-2796.2003.01133.x.10.1046/j.1365-2796.2003.01133.xSearch in Google Scholar PubMed
12. Lyytikäinen, P, Lallukka, T, Lahelma, E, Rahkonen, O. Sleep problems and major weight gain: a follow-up study. Int J Obes 2011;35:109–14. https://doi.org/10.1038/ijo.2010.113.10.1038/ijo.2010.113Search in Google Scholar PubMed
13. Jarrin, DC, McGrath, JJ, Drake, CL. Beyond sleep duration: distinct sleep dimensions are associated with obesity in children and adolescents. Int J Obes 2013;37:552–8. https://doi.org/10.1038/ijo.2013.4.10.1038/ijo.2013.4Search in Google Scholar PubMed PubMed Central
14. Cespedes Feliciano, EM, Rifas-Shiman, SL, Quante, M, Redline, S, Oken, E, Taveras, EM. Chronotype, social jet lag, and cardiometabolic risk factors in early adolescence. JAMA Pediatr 2019;173:1049–57. https://doi.org/10.1001/jamapediatrics.2019.3089.10.1001/jamapediatrics.2019.3089Search in Google Scholar PubMed PubMed Central
15. Darchia, N, Cervena, K. The journey through the world of adolescent sleep. Rev Neurosci 2014;25:585–604. https://doi.org/10.1515/revneuro-2013-0065.10.1515/revneuro-2013-0065Search in Google Scholar PubMed
16. Quante, M, Hesse, M, Döhnert, M, Fuchs, M, Hirsch, C, Sergeyev, E, et al. The LIFE child study: a life course approach to disease and health. BMC Public Health 2012;12:1021. https://doi.org/10.1186/1471-2458-12-1021.10.1186/1471-2458-12-1021Search in Google Scholar PubMed PubMed Central
17. Poulain, T, Baber, R, Vogel, M, Pietzner, D, Kirsten, T, Jurkutat, A, et al. The LIFE child study: a population-based perinatal and pediatric cohort in Germany. Eur J Epidemiol 2017;32:145–58. https://doi.org/10.1007/s10654-016-0216-9.10.1007/s10654-016-0216-9Search in Google Scholar PubMed
18. Daxer, J, Herttrich, T, Zhao, YY, Vogel, M, Hiemisch, A, Scheuermann, K, et al. Nocturnal levels of chemerin and progranulin in adolescents: influence of sex, body mass index, glucose metabolism and sleep. J Pediatr Endocrinol Metab 2017;30:57–61. https://doi.org/10.1515/jpem-2016-0378.10.1515/jpem-2016-0378Search in Google Scholar PubMed
19. Kromeyer-Hauschild, K, Wabitsch, M, Kunze, D, Geller, F, Geiß, HC, Hesse, V, et al. Perzentile für den Body-mass-Index für das Kindes- und Jugendalter unter Heranziehung verschiedener deutscher Stichproben. Monatsschr Kinderh 2001;149:807–18. https://doi.org/10.1007/s001120170107.10.1007/s001120170107Search in Google Scholar
20. Reinehr, T, Holl, RW, Wabitsch, M. The German working group of obesity in childhood and adolescence (AGA): improving the quality of care for overweight and obese children in Germany. Obes Facts 2008;1:26–32. https://doi.org/10.1159/000113405.10.1159/000113405Search in Google Scholar PubMed PubMed Central
21. Slaughter, MH, Lohman, TG, Boileau, RA, Horswill, CA, Stillman, RJ, Van Loan, MD, et al. Skinfold equations for estimation of body fatness in children and youth. Hum Biol 1988;60:709–23.Search in Google Scholar
22. Berry, RB, Budhiraja, R, Gottlieb, DJ, Gozal, D, Iber, C, Kapur, VK, et al. Rules for scoring respiratory events in sleep: update of the 2007 AASM manual for the scoring of sleep and associated events. Deliberations of the sleep apnea definitions task force of the American academy of sleep medicine. J Clin Sleep Med : JCSM : Official Publ Am Acad Sleep Med 2012;08:597–619. https://doi.org/10.5664/jcsm.2172.10.5664/jcsm.2172Search in Google Scholar PubMed PubMed Central
23. Swinscow, TDV, Campbell, MJ. Statistics at square one: Chapter 11. Correlation and regression, 9th ed. London: BMJ Publishing Group; 1997.Search in Google Scholar
24. Lesser, DJ, Bhatia, R, Tran, WH, Oliveira, F, Ortega, R, Keens, TG, et al. Sleep fragmentation and intermittent hypoxemia are associated with decreased insulin sensitivity in obese adolescent Latino males. Pediatr Res 2012;72:293–8. https://doi.org/10.1038/pr.2012.73.10.1038/pr.2012.73Search in Google Scholar PubMed PubMed Central
25. Stamatakis, KA, Punjabi, NM. Effects of sleep fragmentation on glucose metabolism in normal subjects. Chest 2010;137:95–101. https://doi.org/10.1378/chest.09-0791.10.1378/chest.09-0791Search in Google Scholar PubMed PubMed Central
26. Perry, JC, Bergamaschi, CT, Campos, RR, Andersen, ML, Casarini, DE, Tufik, S. Differential sympathetic activation induced by intermittent hypoxia and sleep loss in rats: action of angiotensin (1–7). Auton Neurosci : Basic Clin 2011;160:32–6. https://doi.org/10.1016/j.autneu.2010.11.006.10.1016/j.autneu.2010.11.006Search in Google Scholar PubMed
27. Bhatia, R, Lesser, DJ, Oliveira, FG, Tran, WH, Keens, TG, Khoo, MC, et al. Body fat composition: a predictive factor for sleep related breathing disorder in obese children. J Clin Sleep Med 2015;11:1039–45. https://doi.org/10.5664/jcsm.5022.10.5664/jcsm.5022Search in Google Scholar PubMed PubMed Central
28. Beebe, DW, Lewin, D, Zeller, M, McCabe, M, MacLeod, K, Daniels, SR, et al. Sleep in overweight adolescents: shorter sleep, poorer sleep quality, sleepiness, and sleep-disordered breathing. J Pediatr Psychol 2007;32:69–79. https://doi.org/10.1093/jpepsy/jsj104.10.1093/jpepsy/jsj104Search in Google Scholar PubMed
29. Kalra, M, Mannaa, M, Fitz, K, Kumar, S, Chakraborty, R, Sheng, X, et al. Effect of surgical weight loss on sleep architecture in adolescents with severe obesity. Obes Surg 2008;18:675–9. https://doi.org/10.1007/s11695-008-9472-4.10.1007/s11695-008-9472-4Search in Google Scholar PubMed
30. Lesser, DJ, Bhatia, R, Tran, WH, Oliveira, F, Ortega, R, Keens, TG, et al. Sleep fragmentation and intermittent hypoxemia are associated with decreased insulin sensitivity in obese adolescent Latino males. Pediatr Res. 2012;72:293–8. https://doi.org/10.1038/pr.2012.73.10.1038/pr.2012.73Search in Google Scholar
31. de la, Eva RC, Baur, LA, Donaghue, KC, Waters, KA. Metabolic correlates with obstructive sleep apnea in obese subjects. J Pediatr. 2002;140:654–9.10.1067/mpd.2002.123765Search in Google Scholar PubMed
32. Tauman, R, O'Brien, LM, Ivanenko, A, Gozal, D. Obesity rather than severity of sleep-disordered breathing as the major determinant of insulin resistance and altered lipidemia in snoring children. Pediatrics 2005;116:e66–73.10.1542/peds.2004-2527Search in Google Scholar PubMed
33. Carskadon, MA, Wolfson, AR, Acebo, C, Tzischinsky, O, Seifer, R. Adolescent sleep patterns, circadian timing, and sleepiness at a transition to early school days. Sleep 1998;21:871–81. https://doi.org/10.1093/sleep/21.8.871.10.1093/sleep/21.8.871Search in Google Scholar PubMed
34. Tobisch, B, Blatniczky, L, Barkai, L. Cardiometabolic risk factors and insulin resistance in obese children and adolescents: relation to puberty. Pediatr Obes 2015;10:37–44. https://doi.org/10.1111/j.2047-6310.2013.00202.x.10.1111/j.2047-6310.2013.00202.xSearch in Google Scholar PubMed
35. Reinehr, T, Wolters, B, Knop, C, Lass, N, Holl, RW. Strong effect of pubertal status on metabolic health in obese children: a longitudinal study. J Clin Endocrinol Metab 2015;100:301–8. https://doi.org/10.1210/jc.2014-2674.10.1210/jc.2014-2674Search in Google Scholar PubMed
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/j_jpem-2019-0517).
© 2020 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Review Articles
- Definition and early diagnosis of metabolic syndrome in children
- Cystic fibrosis-related diabetes: an update on pathophysiology, diagnosis, and treatment
- Original Articles
- Association of sleep characteristics with adiposity markers in children
- Prevalence of abdominal obesity in non-obese adolescents: a North Indian adolescent study
- Utility of estimated glucose disposal rate for predicting metabolic syndrome in children and adolescents with type-1 diabetes
- Continuous glucose monitoring reduces pubertal hyperglycemia of type 1 diabetes
- Association between eating behavior, anthropometric and biochemical measurements, and peptide YY (PYY) hormone levels in obese adolescents in outpatient care
- Autoimmune hyperthyroidism in children & adolescents in Sudan: a 13 years’ experience of a Paediatric Endocrinology Clinic
- Timing, prevalence, and dynamics of thyroid disorders in children and adolescents affected with Down syndrome
- Assessment of the most common CYP21A2 point mutations in a cohort of congenital adrenal hyperplasia patients from Egypt
- Quality of life and associated factors in parents of children with late diagnosed phenylketonuria. A cross sectional study in a developing country (Tunisia)
- Genetic analysis and long-term treatment monitoring of 11 children with glycogen storage disease type IIIa
- Growth and metabolic effects of long-term recombinant human growth hormone (rhGH) treatment in short children born small for gestational age: GH-RAST study
- Menstrual cycle, reproductive function, body mass index, and metabolic profiles of women with former central precocious puberty: 10–20-year longitudinal cohort study in southern Thailand
- Letter to the Editors
- European Society of Paediatric Radiology (ESPR) Child Abuse Taskforce Committee: a response to Miller et al.
- The correct formula to calculate triglyceride-glucose index (TyG)
- Case Reports
- Octreotide-related exocrine pancreatic insufficiency (EPI) in congenital hyperinsulinism
- Improvement in glycaemic parameters using SGLT-2 inhibitor and GLP-1 agonist in combination in an adolescent with diabetes mellitus and Prader-Willi syndrome: a case report
- Three patients with glucose-6 phosphatase catalytic subunit 3 deficiency
- Efficacy and safety of denosumab treatment in a prepubertal patient with cherubism
Articles in the same Issue
- Frontmatter
- Review Articles
- Definition and early diagnosis of metabolic syndrome in children
- Cystic fibrosis-related diabetes: an update on pathophysiology, diagnosis, and treatment
- Original Articles
- Association of sleep characteristics with adiposity markers in children
- Prevalence of abdominal obesity in non-obese adolescents: a North Indian adolescent study
- Utility of estimated glucose disposal rate for predicting metabolic syndrome in children and adolescents with type-1 diabetes
- Continuous glucose monitoring reduces pubertal hyperglycemia of type 1 diabetes
- Association between eating behavior, anthropometric and biochemical measurements, and peptide YY (PYY) hormone levels in obese adolescents in outpatient care
- Autoimmune hyperthyroidism in children & adolescents in Sudan: a 13 years’ experience of a Paediatric Endocrinology Clinic
- Timing, prevalence, and dynamics of thyroid disorders in children and adolescents affected with Down syndrome
- Assessment of the most common CYP21A2 point mutations in a cohort of congenital adrenal hyperplasia patients from Egypt
- Quality of life and associated factors in parents of children with late diagnosed phenylketonuria. A cross sectional study in a developing country (Tunisia)
- Genetic analysis and long-term treatment monitoring of 11 children with glycogen storage disease type IIIa
- Growth and metabolic effects of long-term recombinant human growth hormone (rhGH) treatment in short children born small for gestational age: GH-RAST study
- Menstrual cycle, reproductive function, body mass index, and metabolic profiles of women with former central precocious puberty: 10–20-year longitudinal cohort study in southern Thailand
- Letter to the Editors
- European Society of Paediatric Radiology (ESPR) Child Abuse Taskforce Committee: a response to Miller et al.
- The correct formula to calculate triglyceride-glucose index (TyG)
- Case Reports
- Octreotide-related exocrine pancreatic insufficiency (EPI) in congenital hyperinsulinism
- Improvement in glycaemic parameters using SGLT-2 inhibitor and GLP-1 agonist in combination in an adolescent with diabetes mellitus and Prader-Willi syndrome: a case report
- Three patients with glucose-6 phosphatase catalytic subunit 3 deficiency
- Efficacy and safety of denosumab treatment in a prepubertal patient with cherubism
