The relationship between sleep and salivary and serum inflammatory biomarkers in adolescents

Hend Alqaderi; Abeer Abdullah; Matthew Finkelman; Mohamed Abufarha; Sriraman Devarajan; Jehad Abubaker; Nikitha Ramesh; Mary Tavares; Fahd Al-Mulla; Saadoun Bin-Hasan

doi:10.3389/fmed.2023.1175483

The relationship between sleep and salivary and serum inflammatory biomarkers in adolescents

Front Med (Lausanne). 2023 May 26:10:1175483. doi: 10.3389/fmed.2023.1175483. eCollection 2023.

Authors

Affiliations

¹ Dasman Diabetes Institute, Dasman, Kuwait.
² Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, Boston, MA, United States.
³ Department of Preventive Dental Sciences, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia.
⁴ Department of Public Health and Community Service, Tufts University School of Dental Medicine, Boston, MA, United States.
⁵ Boston University School of Public Health, Boston, MA, United States.
⁶ Department of Health Policy and Health Services Research, Boston University Henry M. Goldman School of Dental Medicine, Boston, MA, United States.
⁷ Farwaniya Hospital, Ministry of Health, Al Farwaniyah, Kuwait.

Abstract

Objectives: Poor sleep behavior can trigger an inflammatory response and contribute to the development of inflammatory diseases. Cytokines can act as indicators of inflammation and may precede the onset of inflammatory diseases. This study aimed to determine the association between sleep timing parameters (bedtime, sleep duration, sleep debt, and social jetlag) and the levels of nine serum and salivary inflammatory and metabolic biomarkers.

Methods: Data were collected from 352 adolescents aged 16-19 years enrolled in Kuwait's public high schools. The levels of C-reactive protein (CRP), interleukin-6 (IL-6), interleukin-8 (IL-8), interleukin-10 (IL-10), vascular endothelial growth factor (VEGF), monocyte chemoattractant protein-1 (MCP-1), adiponectin, leptin, and insulin were measured from saliva and serum samples. We conducted mixed-effect multiple linear regression modeling to account for the school variable as a random effect to assess the relationship between the sleep variables and salivary and serum biomarkers. Mediation analysis was conducted to check if BMI was a mediator between bedtime and the biomarkers.

Results: There was a statistically significant elevation in serum IL-6 level associated with later bedtime (0.05 pg./mL, p = 0.01). Adolescents with severe sleep debt of ≥2 h had an increase in salivary IL-6 biomarker levels (0.38 pg./mL, p = 0.01) compared to those who had sleep debt of <1 h. Adolescents with sleep debt of ≥2 h had significantly higher levels of serum CRP (0.61 μg/mL, p = 0.02) than those without sleep debt. Additionally, we found that the inflammatory biomarkers (CRP, IL-6, IL-8, IL-10, VEGF, and MCP-1) and metabolic biomarkers (adiponectin, leptin, and insulin) had more statistically significant associations with the bedtime variables than with sleep duration variables. CRP, IL-6, and IL-8 were associated with sleep debt, and IL-6, VEGF, adiponectin, and leptin levels were associated with social jetlag. BMIz was a full mediator in the relationship between late bedtime and increased serum levels of CRP, IL-6, and insulin.

Conclusion: Adolescents who go to bed at or later than midnight had dysregulated levels of salivary and serum inflammatory biomarkers, suggesting that disrupted circadian rhythm can trigger higher levels of systemic inflammation and potentially exacerbate chronic inflammation and the risk of metabolic diseases.

Keywords: cytokin; inflammation; saliva; serum; sleep.