Main Article Content
Abstract
Background: High inflammation levels and obesity are each linked to worse health outcomes. Low-quality sleep is linked to higher inflammation.
Method: This cross-sectional study investigated whether: individuals with low-quality sleep have higher inflammation; regardless of BMI; low-quality sleep interacts with BMI regarding cross-sectional prediction of inflammation; and whether sleep quality questions could identify this association. We utilized linear regression with 500 African American and Caucasian adults from an Adventist Health Study-2 subset, who completed additional biological indicator testing.
Results: Higher total sleep disturbance (TSD) was associated with increased C-reactive Protein (CRP), p= 0.008, (95% CI = 0.22 to 1.42). The interaction of TSD and BMI was significant in a curvilinear association, p = 0.018,(95% CI = -0.05 to -0.01). As TSD increased, CRP increased; however, the association existed primarily in obese individuals (BMI >30). Low-quality sleep is associated with increased CRP levels, which is a consistent inflammation indicator.
Conclusion: Obesity was not a risk factor for significantly increased CRP until sleep disturbance was indicated as “often” or “almost every day”. This study supports asking sleep quality questions in primary care, for early identification of risk.
Keywords
Article Details
References
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- Bassett, S. M., Lupis, S. B., Gianferante, D., Rohleder, N., & Wolf, J. M. (2015). Sleep quality but not sleep quantity effects on cortisol responses to acute psychosocial stress. Stress: The International Journal on the Biology of Stress, 18(6), 638- 644. https://doi.org/10.3109/10253890.2015.1087503
- Budhiraja, R., Thomas, R., Kim, M., & Redline, S. (2016). The role of big data in the management of sleep-disordered breathing. Sleep Medicine Clinics, 11(2), 241-255. https://doi.org/10.1016/j.jsmc.2016.01.009
- Butler, T. L., Fraser, G. E., Beeson, W. L., Knutsen, S. F., Herring, R. P., Chan, J., Sabate, J., Montgomery, S., Haddad, E., Preston- Martin, S., Bennett, H., & Jaceldo-Siegl, K. (2008). Cohort profile: The Adventist Health Study-2 (AHS-2). International Journal of Epidemiology, 37(2), 260-265. https://doi.org/10.1093/ije/dym165
- Castro-Diehl, C., Diez Roux, A. V., Redline, S., Seeman, T., Shrager, S. E., & Shea, S. (2015). Association of sleep duration and quality with alterations in the hypothalamic-pituitary adrenocortical axis: The multi-ethnic study of atherosclerosis (MESA). The Journal of Clinical Endocrinology and Metabolism, 100(8), 3149-3158. https://doi.org/10.1210/jc.2015-1198
- Chattu, V. K., Manzar, M. D., Kumary, S., Burman, D., Spence, D. W., & Pandi- Perumal, S. R. (2018). The global problem of insufficient sleep and its serious public health implications. Healthcare (Basel), 7(1). https://doi.org/10.3390/healthcare7010001
- Cole, J. C., Motivala, S. J., Buysse, D. J., Oxman, M. N., Levin, M. J., & Irwin, M. R. (2006). Validation of a 3-factor scoring model for the Pittsburgh sleep quality index in older adults. Sleep, 29(1), 112-116. https://pubmed.ncbi.nlm.nih.gov/16453989/
- IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp
- Ding, C., Chan, Z., & Magkos, F. (2016). Lean, but not healthy: the ‘metabolically obese, normal-weight’ phenotype. Current Opinion in Clinical Nutrition and Metabolic Care, 19(6), 408-417. https://doi.org/10.1097/mco.0000000000000317
- Engin, A. (2017). The definition and prevalence of obesity and metabolic syndrome. Advances in Experimental Medicine and Biology, 960, 1-17. https://doi.org/10.1007/978-3-319-48382-5_1
- Fair, B., Mellon, S. H., Epel, E. S., Lin, J., Révész, D., Verhoeven, J. E., Penninx, B. W., Reus, V. I., Rosser, R., Hough, C. M., Mahan, L., Burke, H. M., Blackburn, E. H., & Wolkowitz, O. M. (2017). Telomere length is inversely correlated with urinary stress hormone levels in healthy controls but not in un-medicated depressed individuals-preliminary findings. Journal of Psychosomatic Research, 99, 177-180. https://doi.org/https://doi.org/10.1016/j.jpsychores.2017.06.009
- Floam, S., Simpson, N., Nemeth, E., Scott- Sutherland, J., Gautam, S., & Haack, M. (2015). Sleep characteristics as predictor variables of stress systems markers in insomnia disorder. Journal of Sleep Research, 24(3), 296-304. https://doi.org/10.1111/jsr.12259
- Gaines, J., Vgontzas, A. N., Fernandez-Mendoza, J., & Bixler, E. O. (2018). Obstructive sleep apnea and the metabolic syndrome: The road to clinically-meaningful phenotyping, improved prognosis, and personalized treatment. Sleep Medicine Reviews, 42, 211-219. https://doi.org/10.1016/j.smrv.2018.08.009
- Grandner, M. A., Sands-Lincoln, M. R., Pak, V. M., & Garland, S. N. (2013). Sleep duration, cardiovascular disease, and proinflammatory biomarkers. Nat Sci Sleep, 5, 93. https://pubmed.ncbi.nlm.nih.gov/23901303/
- Guilleminault, C., Kirisoglu, C., & Ohayon, M. M. (2004). C-reactive protein and sleep-disordered breathing. Sleep, 27(8), 1507-1517. https://doi.org/10.1093/ sleep/27.8.1507
- Huang, T., Goodman, M., Li, X., Sands, S. A., Li, J., Stampfer, M. J., Saxena, R., Tworoger, S. S., & Redline, S. (2021). C-reactive protein and risk of OSA in four US cohorts. Chest, 159(6), 2439-2448. https://doi.org/https://doi.org/10.1016/j.chest.2021.01.060]
- Huang, W. Y., Huang, C. C., Chang, C. C., Kor, C. T., Chen, T. Y., & Wu, H. M. (2017). Associations of self-reported sleep quality with circulating interferon gamma-inducible protein 10, interleukin 6, and high-sensitivity c-reactive protein in healthy menopausal women. PloS One, 12(1), e0169216. https://doi.org/10.1371/journal.pone.0169216
- Jaiswal, S. J., Owens, R. L., & Malhotra, A. (2017). Raising awareness about sleep disorders. Lung India, 34(3), 262-268. https://doi.org/10.4103/0970-2113.205331
- Jennum, P., & Kjellberg, J. (2011). Health, social and economical consequences of sleep-disordered breathing: A controlled national study. Thorax, 66(7), 560-566. https://doi.org/10.1136/thx.2010.143958
- Kaplan, G. A. (2006). Alameda County [California] health and ways of living study, 1999 panel inter-university consortium for political and social research [distributor]. https://doi.org/10.3886/ICPSR04432.v1
- Kaufmann, C. N., Canham, S. L., Mojtabai, R., Gum, A. M., Dautovich, N. D., Kohn, R., & Spira, A. P. (2013). Insomnia and health services utilization in middle-aged and older adults: Results from the health and retirement study. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 68(12), 1512-1517. https://doi.org/10.1093/gerona/glt050
- Kushida, C. A., Chang, A., Gadkary, C., Guilleminault, C., Carrillo, O., & Dement, C. (2001). Comparison of actigraphic, polysomnographic, and subjective assessment of sleep parameters in sleep-disordered patients. Sleep Medicine, 2(5), 389-396. https://doi.org/10.1016/s1389-9457(00)00098-8
- Lee, J. W., Morton, K. R., Walters, J., Bellinger, D. L., Butler, T. L., Wilson, C., Walsh, E., Ellison, C. G., McKenzie, M. M., & Fraser, G. E. (2009). Cohort profile: The biopsychosocial religion and health study (BRHS). International Journal of Epidemiology, 38(6), 1470-1478. https://doi.org/10.1093/ije/dyn244
- Lin, H., Zhang, L., Zheng, R., & Zheng, Y. (2017). The prevalence, metabolic risk and effects of lifestyle intervention for metabolically healthy obesity: a systematic review and meta-analysis: A PRISMA- compliant article. Medicine (Baltimore), 96(47), e8838. https://doi.org/10.1097/md.0000000000008838
- Liu, R., Liu, X., Zee, P. C., Hou, L., Zheng, Z., Wei, Y., & Du, J. (2014). Association between sleep quality and C-reactive protein: results from national health and nutrition examination survey, 2005-2008. PloS One, 9(3), e92607. https://journals.plos.org/plosone/article?id=10.1371/journal. pone.0092607
- Massar, S. A. A., Liu, J. C. J., Mohammad, N. B., & Chee, M. W. L. (2017). Poor habitual sleep efficiency is associated with increased cardiovascular and cortisol stress reactivity in men. Psychoneuroendocrinology, 81, 151-156. https://doi.org/10.1016/j.psyneuen.2017.04.013
- National Heart, L., & Institute, B. (1998). Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report. Obesity Res, 6, 51S-210S. https://www.ncbi.nlm.nih.gov/ books/NBK2003/ https://www.nhlbi.nih. gov/files/docs/guidelines/prctgd_c.pdf
- Nowakowski, S., Matthews, K. A., von Känel, R., Hall, M. H., & Thurston, R. C. (2018). Sleep characteristics and inflammatory biomarkers among midlife women. Sleep, 41(5). https://doi.org/10.1093/sleep/zsy049
- Potts, K. J., Butterfield, D. T., Sims, P., Henderson, M., & Shames, C. B. (2013). Cost savings associated with an education campaign on the diagnosis and management of sleep-disordered breathing: a retrospective, claims-based US study. Population Health Management, 16(1), 7-13. https://doi.org/10.1089/pop.2011.0102
- Punjabi, N. M., & Beamer, B. A. (2007). C-reactive protein is associated with sleep disordered breathing independent of adiposity. Sleep, 30(1), 29-34. https://doi.org/10.1093/sleep/30.1.29
- Singh-Manoux, A., Shipley, M. J., Bell, J. A., Canonico, M., Elbaz, A., & Kivimaki, M. (2017). Association between inflammatory biomarkers and all-cause, cardiovascular and cancer-related mortality. Canadian Medical Association Journal, 189(10), E384-e390. https://doi.org/10.1503/cmaj.160313
- Tomiyama, A. J., O’Donovan, A., Lin, J., Puterman, E., Lazaro, A., Chan, J., Dhabhar, F. S., Wolkowitz, O., Kirschbaum, C., Blackburn, E., & Epel, E. (2012). Does cellular aging relate to patterns of allostasis? An examination of basal and stress reactive HPA axis activity and telomere length. Physiology and Behavior, 106(1), 40-45. https://doi.org/10.1016/j.physbeh.2011.11.016
References
Åkerstedt, T., Schwarz, J., Gruber, G., Lindberg, E., & Theorell-Haglöw, J. (2016). The relation between polysomnography and subjective sleep and its dependence on age - poor sleep may become good sleep. Journal of sleep research, 25(5), 565–570. https://doi.org/10.1111/jsr.12407
Bassett, S. M., Lupis, S. B., Gianferante, D., Rohleder, N., & Wolf, J. M. (2015). Sleep quality but not sleep quantity effects on cortisol responses to acute psychosocial stress. Stress: The International Journal on the Biology of Stress, 18(6), 638- 644. https://doi.org/10.3109/10253890.2015.1087503
Budhiraja, R., Thomas, R., Kim, M., & Redline, S. (2016). The role of big data in the management of sleep-disordered breathing. Sleep Medicine Clinics, 11(2), 241-255. https://doi.org/10.1016/j.jsmc.2016.01.009
Butler, T. L., Fraser, G. E., Beeson, W. L., Knutsen, S. F., Herring, R. P., Chan, J., Sabate, J., Montgomery, S., Haddad, E., Preston- Martin, S., Bennett, H., & Jaceldo-Siegl, K. (2008). Cohort profile: The Adventist Health Study-2 (AHS-2). International Journal of Epidemiology, 37(2), 260-265. https://doi.org/10.1093/ije/dym165
Castro-Diehl, C., Diez Roux, A. V., Redline, S., Seeman, T., Shrager, S. E., & Shea, S. (2015). Association of sleep duration and quality with alterations in the hypothalamic-pituitary adrenocortical axis: The multi-ethnic study of atherosclerosis (MESA). The Journal of Clinical Endocrinology and Metabolism, 100(8), 3149-3158. https://doi.org/10.1210/jc.2015-1198
Chattu, V. K., Manzar, M. D., Kumary, S., Burman, D., Spence, D. W., & Pandi- Perumal, S. R. (2018). The global problem of insufficient sleep and its serious public health implications. Healthcare (Basel), 7(1). https://doi.org/10.3390/healthcare7010001
Cole, J. C., Motivala, S. J., Buysse, D. J., Oxman, M. N., Levin, M. J., & Irwin, M. R. (2006). Validation of a 3-factor scoring model for the Pittsburgh sleep quality index in older adults. Sleep, 29(1), 112-116. https://pubmed.ncbi.nlm.nih.gov/16453989/
IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp
Ding, C., Chan, Z., & Magkos, F. (2016). Lean, but not healthy: the ‘metabolically obese, normal-weight’ phenotype. Current Opinion in Clinical Nutrition and Metabolic Care, 19(6), 408-417. https://doi.org/10.1097/mco.0000000000000317
Engin, A. (2017). The definition and prevalence of obesity and metabolic syndrome. Advances in Experimental Medicine and Biology, 960, 1-17. https://doi.org/10.1007/978-3-319-48382-5_1
Fair, B., Mellon, S. H., Epel, E. S., Lin, J., Révész, D., Verhoeven, J. E., Penninx, B. W., Reus, V. I., Rosser, R., Hough, C. M., Mahan, L., Burke, H. M., Blackburn, E. H., & Wolkowitz, O. M. (2017). Telomere length is inversely correlated with urinary stress hormone levels in healthy controls but not in un-medicated depressed individuals-preliminary findings. Journal of Psychosomatic Research, 99, 177-180. https://doi.org/https://doi.org/10.1016/j.jpsychores.2017.06.009
Floam, S., Simpson, N., Nemeth, E., Scott- Sutherland, J., Gautam, S., & Haack, M. (2015). Sleep characteristics as predictor variables of stress systems markers in insomnia disorder. Journal of Sleep Research, 24(3), 296-304. https://doi.org/10.1111/jsr.12259
Gaines, J., Vgontzas, A. N., Fernandez-Mendoza, J., & Bixler, E. O. (2018). Obstructive sleep apnea and the metabolic syndrome: The road to clinically-meaningful phenotyping, improved prognosis, and personalized treatment. Sleep Medicine Reviews, 42, 211-219. https://doi.org/10.1016/j.smrv.2018.08.009
Grandner, M. A., Sands-Lincoln, M. R., Pak, V. M., & Garland, S. N. (2013). Sleep duration, cardiovascular disease, and proinflammatory biomarkers. Nat Sci Sleep, 5, 93. https://pubmed.ncbi.nlm.nih.gov/23901303/
Guilleminault, C., Kirisoglu, C., & Ohayon, M. M. (2004). C-reactive protein and sleep-disordered breathing. Sleep, 27(8), 1507-1517. https://doi.org/10.1093/ sleep/27.8.1507
Huang, T., Goodman, M., Li, X., Sands, S. A., Li, J., Stampfer, M. J., Saxena, R., Tworoger, S. S., & Redline, S. (2021). C-reactive protein and risk of OSA in four US cohorts. Chest, 159(6), 2439-2448. https://doi.org/https://doi.org/10.1016/j.chest.2021.01.060]
Huang, W. Y., Huang, C. C., Chang, C. C., Kor, C. T., Chen, T. Y., & Wu, H. M. (2017). Associations of self-reported sleep quality with circulating interferon gamma-inducible protein 10, interleukin 6, and high-sensitivity c-reactive protein in healthy menopausal women. PloS One, 12(1), e0169216. https://doi.org/10.1371/journal.pone.0169216
Jaiswal, S. J., Owens, R. L., & Malhotra, A. (2017). Raising awareness about sleep disorders. Lung India, 34(3), 262-268. https://doi.org/10.4103/0970-2113.205331
Jennum, P., & Kjellberg, J. (2011). Health, social and economical consequences of sleep-disordered breathing: A controlled national study. Thorax, 66(7), 560-566. https://doi.org/10.1136/thx.2010.143958
Kaplan, G. A. (2006). Alameda County [California] health and ways of living study, 1999 panel inter-university consortium for political and social research [distributor]. https://doi.org/10.3886/ICPSR04432.v1
Kaufmann, C. N., Canham, S. L., Mojtabai, R., Gum, A. M., Dautovich, N. D., Kohn, R., & Spira, A. P. (2013). Insomnia and health services utilization in middle-aged and older adults: Results from the health and retirement study. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 68(12), 1512-1517. https://doi.org/10.1093/gerona/glt050
Kushida, C. A., Chang, A., Gadkary, C., Guilleminault, C., Carrillo, O., & Dement, C. (2001). Comparison of actigraphic, polysomnographic, and subjective assessment of sleep parameters in sleep-disordered patients. Sleep Medicine, 2(5), 389-396. https://doi.org/10.1016/s1389-9457(00)00098-8
Lee, J. W., Morton, K. R., Walters, J., Bellinger, D. L., Butler, T. L., Wilson, C., Walsh, E., Ellison, C. G., McKenzie, M. M., & Fraser, G. E. (2009). Cohort profile: The biopsychosocial religion and health study (BRHS). International Journal of Epidemiology, 38(6), 1470-1478. https://doi.org/10.1093/ije/dyn244
Lin, H., Zhang, L., Zheng, R., & Zheng, Y. (2017). The prevalence, metabolic risk and effects of lifestyle intervention for metabolically healthy obesity: a systematic review and meta-analysis: A PRISMA- compliant article. Medicine (Baltimore), 96(47), e8838. https://doi.org/10.1097/md.0000000000008838
Liu, R., Liu, X., Zee, P. C., Hou, L., Zheng, Z., Wei, Y., & Du, J. (2014). Association between sleep quality and C-reactive protein: results from national health and nutrition examination survey, 2005-2008. PloS One, 9(3), e92607. https://journals.plos.org/plosone/article?id=10.1371/journal. pone.0092607
Massar, S. A. A., Liu, J. C. J., Mohammad, N. B., & Chee, M. W. L. (2017). Poor habitual sleep efficiency is associated with increased cardiovascular and cortisol stress reactivity in men. Psychoneuroendocrinology, 81, 151-156. https://doi.org/10.1016/j.psyneuen.2017.04.013
National Heart, L., & Institute, B. (1998). Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report. Obesity Res, 6, 51S-210S. https://www.ncbi.nlm.nih.gov/ books/NBK2003/ https://www.nhlbi.nih. gov/files/docs/guidelines/prctgd_c.pdf
Nowakowski, S., Matthews, K. A., von Känel, R., Hall, M. H., & Thurston, R. C. (2018). Sleep characteristics and inflammatory biomarkers among midlife women. Sleep, 41(5). https://doi.org/10.1093/sleep/zsy049
Potts, K. J., Butterfield, D. T., Sims, P., Henderson, M., & Shames, C. B. (2013). Cost savings associated with an education campaign on the diagnosis and management of sleep-disordered breathing: a retrospective, claims-based US study. Population Health Management, 16(1), 7-13. https://doi.org/10.1089/pop.2011.0102
Punjabi, N. M., & Beamer, B. A. (2007). C-reactive protein is associated with sleep disordered breathing independent of adiposity. Sleep, 30(1), 29-34. https://doi.org/10.1093/sleep/30.1.29
Singh-Manoux, A., Shipley, M. J., Bell, J. A., Canonico, M., Elbaz, A., & Kivimaki, M. (2017). Association between inflammatory biomarkers and all-cause, cardiovascular and cancer-related mortality. Canadian Medical Association Journal, 189(10), E384-e390. https://doi.org/10.1503/cmaj.160313
Tomiyama, A. J., O’Donovan, A., Lin, J., Puterman, E., Lazaro, A., Chan, J., Dhabhar, F. S., Wolkowitz, O., Kirschbaum, C., Blackburn, E., & Epel, E. (2012). Does cellular aging relate to patterns of allostasis? An examination of basal and stress reactive HPA axis activity and telomere length. Physiology and Behavior, 106(1), 40-45. https://doi.org/10.1016/j.physbeh.2011.11.016