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Pediatrics

Longitudinal associations between overweight/obesity and stress biology in low-income children

International Journal of Obesity volume 44, pages 646–655 (2020)Cite this article

Subjects

Abstract

Background/Objectives

Associations between overweight and altered stress biology have been reported cross-sectionally during childhood, but it is unclear whether overweight precedes altered stress biology or if altered stress biology predicts greater likelihood of overweight over time. The current longitudinal study investigates associations between overweight/obesity, salivary alpha amylase and cortisol morning intercept, diurnal slope, and reactivity to social stress in a cohort of low-income children during preschool and middle childhood.

Subjects/Methods

Children were recruited through Head Start and were observed and followed into middle childhood (N = 257; M = 8.0 years). Height and weight were measured at both time points. Saliva samples were collected across the day and in response to a social challenge at both ages for alpha amylase and cortisol determination.

Results

Cross-lagged panel analyses indicated that overweight/obesity at preschool predicted lower morning alpha amylase (β = −0.18, 95% CI: −0.34, −0.03; p = 0.023), lower morning cortisol (β = −0.22, 95% CI: −0.38, −0.06; p = 0.006), lower sAA diurnal slope (β = −0.18, 95% CI: −0.34, −0.03; p = 0.021), and lower cortisol stress reactivity (β = −0.19, 95% CI: −0.35, −0.02; p = 0.031) in middle childhood. Lower alpha amylase reactivity at preschool was the only biological factor that predicted higher likelihood of overweight/obesity at middle childhood (β = −0.20, 95% CI: −0.38, −0.01; p = 0.035).

Conclusions

These findings suggest that overweight/obesity may be driving changes in stress biology across early-to-middle childhood, particularly in downregulation of morning levels of stress hormones, diurnal sAA slope, and cortisol reactivity to stress, rather than stress biology driving overweight/obesity.

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References

  1. Ng M, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384:766–81.

    Article  Google Scholar 

  2. Pan L, May AL, Wethington H, Dalenius K, Grummer-Strawn LM. Incidence of obesity among young US children living in low-income families, 2008–2011. Pediatrics. 2013;132:1006–13.

    PubMed  PubMed Central  Google Scholar 

  3. Dallman MF, et al. Glucocorticoids, the etiology of obesity and the metabolic syndrome. Curr Alzheimer Res. 2007;4:199–204.

    CAS  PubMed  Google Scholar 

  4. Dallman MF. Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab. 2010;21:159–65.

    CAS  PubMed  Google Scholar 

  5. Vicennati V, et al. Cross-talk between adipose tissue and the HPA axis in obesity and overt hypercortisolemic states. Horm Mol Biol Clin Investig. 2014;17:63–77.

    CAS  PubMed  Google Scholar 

  6. Papafotiou C, et al. Hair cortisol concentrations exhibit a positive association with salivary cortisol profiles and are increased in obese prepubertal girls. Stress. 2017;20:217–22.

    CAS  PubMed  Google Scholar 

  7. Reinehr T, et al. Relationships between 24-hour urinary free cortisol concentrations and metabolic syndrome in obese children. J Clin Endocrinol Metab. 2014;99:2391–9.

    CAS  PubMed  Google Scholar 

  8. Kjölhede EA, Gustafsson PE, Gustafsson P, Nelson N. Overweight and obese children have lower cortisol levels than normal weight children. Acta Paediatr. 2014;103:295–9.

    PubMed  Google Scholar 

  9. Lumeng JC, et al. Diurnal cortisol pattern, eating behaviors and overweight in low-income preschool-aged children. Appetite. 2014;73:65–72.

    PubMed  Google Scholar 

  10. Veldhorst MA, et al. Increased scalp hair cortisol concentrations in obese children. J Clin Endocrinol Metab. 2014;99:285–90.

    CAS  PubMed  Google Scholar 

  11. Knutsson U, et al. Circadian cortisol rhythms in healthy boys and girls: relationship with age, growth, body composition, and pubertal development. J Clin Endocrinol Metab. 1997;82:536–40.

    CAS  Google Scholar 

  12. Törnhage C-J, Αlfvén G. Diurnal salivary cortisol concentration in school-aged children: increased morning cortisol concentration and total cortisol concentration negatively correlated to body mass index in children with recurrent abdominal pain of psychosomatic origin. J Pediatr Endocrinol Metab. 2006;19:843–54.

    PubMed  Google Scholar 

  13. Hillman JB, Dorn LD, Loucks TL, Berga SL. Obesity and the hypothalamic-pituitary-adrenal axis in adolescent girls. Metab-Clin Exp. 2012;61:341–8.

    CAS  PubMed  Google Scholar 

  14. Ruttle PL, et al. Concurrent and longitudinal associations between diurnal cortisol and body mass index across adolescence. J Adolesc Health. 2013;52:731–7.

    PubMed  PubMed Central  Google Scholar 

  15. Dockray S, Susman EJ, Dorn LD. Depression, cortisol reactivity and obesity in childhood and adolescence. J Adolesc Health. 2009;45:344–50.

    PubMed  PubMed Central  Google Scholar 

  16. Francis L, Granger D, Susman E. Adrenocortical regulation, eating in the absence of hunger and BMI in young children. Appetite. 2013;64:32–8.

    CAS  PubMed  Google Scholar 

  17. Miller AL, et al. Blunted cortisol response to stress is associated with higher body mass index in low-income preschool-aged children. Psychoneuroendocrinology. 2013;38:2611–7.

    CAS  PubMed  Google Scholar 

  18. Davy KP, Orr JS. Sympathetic nervous system behavior in human obesity. Neurosci Biobehav Rev. 2009;33:116–24.

    PubMed  Google Scholar 

  19. Tataranni PA, Young JB, Bogardus C, Ravussin E. A low sympathoadrenal activity is associated with body weight gain and development of central adiposity in Pima Indian men. Obesity. 1997;5:341–7.

    CAS  Google Scholar 

  20. Tentolouris N, Liatis S, Katsilambros N. Sympathetic system activity in obesity and metabolic syndrome. Ann N Y Acad Sci. 2006;1083:129–52.

    CAS  PubMed  Google Scholar 

  21. Latchman PL, Mathur M, Bartels MN, Axtell RS, De Meersman RE. Impaired autonomic function in normotensive obese children. Clin Autonomic Res. 2011;21:319–23.

    Google Scholar 

  22. Kuebler U, et al. Norepinephrine infusion with and without alpha-adrenergic blockade by phentolamine increases salivary alpha amylase in healthy men. Psychoneuroendocrinology. 2014;49:290–8.

    CAS  PubMed  Google Scholar 

  23. Nater UM, Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology. 2009;34:486–96.

    CAS  PubMed  Google Scholar 

  24. Nater UM, Rohleder N, Schlotz W, Ehlert U, Kirschbaum C. Determinants of the diurnal course of salivary alpha-amylase. Psychoneuroendocrinology. 2007;32:392–401.

    CAS  PubMed  Google Scholar 

  25. Hill-Soderlund AL, et al. The developmental course of salivary alpha-amylase and cortisol from 12 to 36 months: Relations with early poverty and later behavior problems. Psychoneuroendocrinology. 2015;52:311–23.

    CAS  PubMed  Google Scholar 

  26. Morrison SF. Differential control of sympathetic outflow. Am J Physiol-Regulatory Integr Comp Physiol. 2001;281:R683–98.

    CAS  Google Scholar 

  27. Alkon A, et al. Latino children’s body mass index at 2–3.5 years predicts sympathetic nervous system activity at 5 years. Child Obes. 2014;10:214–24.

    PubMed  PubMed Central  Google Scholar 

  28. Rodríguez-Colón SM, Bixler EO, Li X, Vgontzas AN, Liao D. Obesity is associated with impaired cardiac autonomic modulation in children. Pediatr Obes. 2011;6:128–34.

    Google Scholar 

  29. Soares-Miranda L, et al. Central fat influences cardiac autonomic function in obese and overweight girls. Pediatr Cardiol. 2011;32:924–8.

    PubMed  Google Scholar 

  30. Vanderlei LCM, Pastre CM, Freitas Júnior IF, Godoy MFd. Analysis of cardiac autonomic modulation in obese and eutrophic children. Clinics. 2010;65:789–92.

    PubMed  PubMed Central  Google Scholar 

  31. Baum P, Petroff D, Classen J, Kiess W, Blüher S. Dysfunction of autonomic nervous system in childhood obesity: a cross-sectional study. PLoS ONE. 2013;8:e54546.

    PubMed  PubMed Central  Google Scholar 

  32. Papafotiou C, et al. Increased salivary and hair cortisol and decreased salivary alpha-amylase concentrations in obese prepubertal girls. 55th Annual European Society for Paediatric Endocrinology. 2016.

  33. Miller AL, et al. Salivary alpha amylase diurnal pattern and stress response are associated with body mass index in low-income preschool-aged children. Psychoneuroendocrinology. 2015;53:40–8.

    CAS  PubMed  Google Scholar 

  34. Miller AL, et al. Associations between stress biology indicators and overweight across toddlerhood. Psychoneuroendocrinology. 2017;79:98–106.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Miller AL, et al. Early childhood stress and child age predict longitudinal increases in obesogenic eating among low-income children. Acad Pediatr. 2018;18:685–91.

    PubMed  PubMed Central  Google Scholar 

  36. Kuczmarski RJ, et al. CDC growth charts for the United States: methods and development. Vital- health Stat Ser 11. 2000;2002:1–190.

    Google Scholar 

  37. Hu L-t, Bentler PM. Fit indices in covariance structure modeling: Sensitivity to underparameterized model misspecification. Psychological Methods. 1998;3:424.

    Google Scholar 

  38. Browne MW, Cudeck R. Alternative ways of assessing model fit. In: Long KABJS, editor. Testing structural equation models. Newbury Park, CA: Sage; 1993. p. 136–62.

  39. Björntorp P. Do stress reactions cause abdominal obesity and comorbidities? Obes Rev. 2001;2:73–86.

    PubMed  Google Scholar 

  40. Björntorp P. Endocrine abnormalities of obesity. Metab-Clin Exp. 1995;44:21–3.

    PubMed  Google Scholar 

  41. Rosmond R, Dallman MF, Björntorp P. Stress-related cortisol secretion in men: Relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab. 1998;83:1853–9.

    CAS  PubMed  Google Scholar 

  42. Lee M-J, Pramyothin P, Karastergiou K, Fried SK. Deconstructing the roles of glucocorticoids in adipose tissue biology and the development of central obesity. Biochimica et Biophysica Acta. 2014;1842:473–81.

    CAS  PubMed  Google Scholar 

  43. Miller GE, Chen E, Zhou ES. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bull. 2007;133:25–45.

    Google Scholar 

  44. Gunnar MR, Vazquez DM. Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Dev Psychopathol. 2001;13:515–38.

    CAS  PubMed  Google Scholar 

  45. Heim C, Ehlert U, Hellhammer DH. The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology. 2000;25:1–35.

    CAS  PubMed  Google Scholar 

  46. Ouellet-Morin I, et al. Blunted cortisol responses to stress signal social and behavioral problems among maltreated/bullied 12-year-old children. Biol Psychiatry. 2011;70:1016–23.

    CAS  PubMed  Google Scholar 

  47. Lumeng JC, Gannon K, Cabral HJ, Frank DA, Zuckerman B. Association between clinically meaningful behavior problems and overweight in children. Pediatrics. 2003;112:1138–45.

    PubMed  Google Scholar 

  48. Meaney MJ, Szyf M, Seckl JR. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med. 2007;13:269–77.

    CAS  PubMed  Google Scholar 

  49. Steptoe A, van Jaarsveld CH, Semmler C, Plomin R, Wardle J. Heritability of daytime cortisol levels and cortisol reactivity in children. Psychoneuroendocrinology. 2009;34:273–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Locke AE, et al. Genetic studies of body mass index yield new insights for obesity biology. Nature. 2015;518:197.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Evans GW, Kim P. Childhood poverty and health: cumulative risk exposure and stress dysregulation. Psychol Sci. 2007;18:953–7.

    PubMed  Google Scholar 

  52. Harthoorn LF, Dransfield E. Periprandial changes of the sympathetic–parasympathetic balance related to perceived satiety in humans. Eur J Appl Physiol. 2008;102:601–8.

    PubMed  Google Scholar 

  53. Taşçılar ME, et al. Cardiac autonomic functions in obese children. J Clin Res Pediatr Endocrinol. 2011;3:60.

    PubMed  PubMed Central  Google Scholar 

  54. Altuncu ME, Baspinar O, Keskin M. The use of short-term analysis of heart rate variability to assess autonomic function in obese children and its relationship with metabolic syndrome. Cardiol J. 2012;19:501–6.

    PubMed  Google Scholar 

  55. Rothman KJ. Six persistent research misconceptions. J Gen Intern Med. 2014;29:1060–4.

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by funding from F32HD088029 (PI: JRD), NICHD/NIDDK R01 DK095695 (PI: ALM and JCL), NIDDK R21DK090718 (PI: ALM and JCL), American Heart Association 10GRNT4460043 (PI: ALM), and NIDDK RC1DK086376 (PI: JCL).

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Authors and Affiliations

  1. Department of Psychology, University of Denver, Denver, CO, USA

    Jenalee R. Doom

  2. Department of Pediatrics, University of Michigan Medical School, Ann Arbor, MI, USA

    Jenalee R. Doom, Julie C. Lumeng, Julie Sturza & Delia M. Vazquez

  3. Center for Human Growth & Development, University of Michigan, Ann Arbor, MI, USA

    Jenalee R. Doom, Julie C. Lumeng, Julie Sturza, Niko Kaciroti, Delia M. Vazquez & Alison L. Miller

  4. Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA

    Julie C. Lumeng

  5. Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA

    Niko Kaciroti

  6. Department of Health Behavior and Health Education, University of Michigan School of Public Health, Ann Arbor, MI, USA

    Alison L. Miller

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Correspondence to Jenalee R. Doom.

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Doom, J.R., Lumeng, J.C., Sturza, J. et al. Longitudinal associations between overweight/obesity and stress biology in low-income children. Int J Obes 44, 646–655 (2020). https://doi.org/10.1038/s41366-019-0447-4

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