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Sleep quality mediates the relationship between frailty and cognitive dysfunction in non-demented middle aged to older adults

Published online by Cambridge University Press:  22 April 2019

Sonya Kaur
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Nikhil Banerjee
Affiliation:
Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA Department of Psychology, University of Miami, Miami, FL, USA
Michelle Miranda
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Mitchell Slugh
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Ni Sun-Suslow
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA
Katalina F. McInerney
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Xiaoyan Sun
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Alberto R. Ramos
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Tatjana Rundek
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA
Ralph L. Sacco
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
Bonnie E. Levin*
Affiliation:
Department of Neurology, University of Miami Miller School of Medicine, Miami, FL, USA Evelyn F. McKnight Brain Institute, University of Miami Miller School of Medicine, Miami, FL, USA
*
Correspondence should be addressed to: Bonnie E. Levin, Division of Neuropsychology, University of Miami Miller School of Medicine, 1120 NW 14th Street, Suite 1336, Miami, FL 33136, USA. Phone: (305) 243 7529. Email: Blevin@med.miami.edu.

Abstract

Objectives:

Frailty is associated with cognitive decline in older adults. However, the mechanisms explaining this relationship are poorly understood. We hypothesized that sleep quality may mediate the relationship between frailty and cognition.

Participants:

154 participants aged between 50-90 years (mean = 69.1 years, SD = 9.2 years) from the McKnight Brain Registry were included.

Measurements:

Participants underwent a full neuropsychological evaluation, frailty and subjective sleep quality assessments. Direct relationships between frailty and cognitive function were assessed using linear regression models. Statistical mediation of these relationships by sleep quality was assessed using nonparametric bootstrapping procedures.

Results:

Frailty severity predicted weaker executive function (B = −2.77, β = −0.30, 95% CI = −4.05 – −1.29) and processing speed (B = −1.57, β = −0.17, 95% CI = −3.10 – −0.16). Poor sleep quality predicted poorer executive function (B = −0.47, β = −0.21, 95% CI = −0.79 – −0.08), processing speed (B = −0.64, β = −0.28, 95% CI = −0.98 – −0.31), learning (B = −0.42, β = −0.19, 95% CI = −0.76 – −0.05) and delayed recall (B = −0.41, β = −0.16, 95% CI = −0.80 – −0.31). Poor sleep quality mediated the relationships between frailty severity and executive function (B = −0.66, β = −0.07, 95% CI = −1.48 – −0.39), learning (B = −0.85, β = −0.07, 95% CI = −1.85 – −0.12), delayed recall (B = −0.47, β = −0.08, 95% CI = −2.12 – −0.39) and processing speed (B = −0.90, β = −0.09, 95% CI = −1.85 – −0.20).

Conclusions:

Relationships between frailty severity and several cognitive outcomes were significantly mediated by poor sleep quality. Interventions to improve sleep quality may be promising avenues to prevent cognitive decline in frail older adults.

Type
Original Research Article
Copyright
© International Psychogeriatric Association 2019 

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References

Bacci, M. R. et al. (2017). Obstructive sleep apnea syndrome and sleep quality in hypertensive patients. Revista da Associação Médica Brasileira, 63, 10551060.CrossRefGoogle ScholarPubMed
Barzilay, J. I. et al. (2007). Insulin resistance and inflammation as precursors of frailty: the Cardiovascular Health Study. Archives of Internal Medicine, 167, 635641.CrossRefGoogle ScholarPubMed
Beck, A. T., Steer, R. A. and Carbin, M. G. (1988). Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clinical psychology review, 8, 77100.CrossRefGoogle Scholar
Bennett, D. A. et al. (2003). Education modifies the relation of AD pathology to level of cognitive function in older persons. Neurology, 60, 19091915.CrossRefGoogle ScholarPubMed
Black, S. A. and Rush, R. D. (2002). Cognitive and functional decline in adults aged 75 and older. Journal of the American Geriatrics Society, 50, 19781986.CrossRefGoogle ScholarPubMed
Buchman, A. S. et al. (2014). Brain pathology contributes to simultaneous change in physical frailty and cognition in old age. The Journals of Gerontology: Series A, 69, 15361544. doi: 10.1093/gerona/glu117.CrossRefGoogle ScholarPubMed
Butterfield, D. A., Drake, J., Pocernich, C. and Castegna, A. (2001). Evidence of oxidative damage in Alzheimer’s disease brain: central role for amyloid B-peptide. Trends in Molecular Medicine, 7, 548554. doi: 10.1016/S1471-4914(01)02173-6.CrossRefGoogle Scholar
Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R. and Kupfer, D. J. (1989). The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry research, 28, 193213.CrossRefGoogle ScholarPubMed
Carlson, L. E. and Garland, S. N. (2005). Impact of mindfulness-based stress reduction (MBSR) on sleep, mood, stress and fatigue symptoms in cancer outpatients. International journal of behavioral medicine, 12, 278285.CrossRefGoogle ScholarPubMed
Control, C. f. D. & Prevention. (2003). Trends in aging–United States and worldwide. MMWR. Morbidity and Mortality Weekly Report, 52, 101.Google Scholar
Dam, T. T. L., Ewing, S., Ancoli-Israel, S., Ensrud, K., Redline, S. and Stone, K. (2008). Association between sleep and physical function in older men: the osteoporotic fractures in men sleep study. Journal of the American Geriatrics Society, 56, 16651673. doi: 10.1111/j.1532-5415.2008.01846.xCrossRefGoogle ScholarPubMed
Desideri, G. et al. (2012). Benefits in cognitive function, blood pressure, and insulin resistance through cocoa flavanol consumption in elderly subjects with mild cognitive impairment: the Cocoa, Cognition, and Aging (CoCoA) study. Hypertension, 60, 794801.CrossRefGoogle ScholarPubMed
Donga, E. et al. (2010). A single night of partial sleep deprivation induces insulin resistance in multiple metabolic pathways in healthy subjects. The Journal of Clinical Endocrinology & Metabolism, 95, 29632968.CrossRefGoogle ScholarPubMed
Doyle, P., Cusin, I., Rohner-Jeanrenaud, F. and Jeanrenaud, B. (1995). Four-day hyperinsulinemia in euglycemic conditions alters local cerebral glucose utilization in specific brain nuclei of freely moving rats. Brain research, 684, 4755.CrossRefGoogle ScholarPubMed
Droge, W. (2002). Free radicals in the physiological control of cell function. Physiological reviews, 82, 4795.CrossRefGoogle ScholarPubMed
Endeshaw, Y. W., Unruh, M. L., Kutner, M., Newman, A. B. and Bliwise, D. L. (2009). Sleep-disordered breathing and frailty in the cardiovascular health study cohort. American Journal of Epidemiology, 170, 193202. doi: 10.1093/aje/kwp108.CrossRefGoogle ScholarPubMed
Ensrud, K.E. et al. (2009). Sleep disturbances and frailty status in older community-dwelling men. Journal of the American Geriatrics Society, 57, 20852093.CrossRefGoogle ScholarPubMed
Ensrud, K. E. et al. (2012). Sleep disturbances and risk of frailty and mortality in older men. Sleep Medicine, 13, 12171225. doi: 10.1016/j.sleep.2012.04.010.CrossRefGoogle ScholarPubMed
Everson, C. A., Laatsch, C. D. and Hogg, N. (2005). Antioxidant defense responses to sleep loss and sleep recovery. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288, R374R383.CrossRefGoogle ScholarPubMed
Foley, D., Ancoli-Israel, S., Britz, P. and Walsh, J. (2004). Sleep disturbances and chronic disease in older adults: results of the 2003 National Sleep Foundation Sleep in America Survey. Journal of psychosomatic research, 56, 497502.CrossRefGoogle ScholarPubMed
Fried, L. P. et al. (2001). Frailty in older adults evidence for a phenotype. The Journals of Gerontology: Series A, 56, M146M157. doi: 10.1093/gerona/56.3.M146.CrossRefGoogle ScholarPubMed
Goldman, S. E. et al. (2008). Sleep problems and associated daytime fatigue in community-dwelling older individuals. Journals of Gerontology - Series A Biological Sciences and Medical Sciences, 63, 10691075. doi: 10.1093/gerona/63.10.1069.CrossRefGoogle ScholarPubMed
Gulec, M. et al. (2012). Oxidative stress in patients with primary insomnia. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 37, 247251.CrossRefGoogle ScholarPubMed
Gutman, G. M., Stark, A., Donald, A. and Beattie, B. L. (2001). Contribution of self-reported health ratings to predicting frailty, institutionalization, and death over a 5-year period. International Psychogeriatrics, 13, 223231.CrossRefGoogle Scholar
Haimov, I., Hanuka, E. and Horowitz, Y. (2008). Chronic Insomnia and Cognitive Functioning Among Older Adults. Behavioral Sleep Medicine, 6, 3254. doi: 10.1080/15402000701796080.CrossRefGoogle ScholarPubMed
Hayes, A. F. (2009). Beyond Baron and Kenny: statistical mediation analysis in the new millennium. Communication monographs, 76, 408420.CrossRefGoogle Scholar
Hayes, A. F. (2012). PROCESS: A versatile computational tool for observed variable mediation, moderation, and conditional process modeling. KS: University of Kansas.Google Scholar
Hayes, A. F. (2018). Introduction to mediation, moderation and conditional process analysis. A regression-based approach. New York: Guilford Press.Google Scholar
Inglés, M. et al. (2014). Oxidative stress is related to frailty, not to age or sex, in a geriatric population: lipid and protein oxidation as biomarkers of frailty. Journal of the American Geriatrics Society, 62, 13241328.CrossRefGoogle Scholar
Jennings, J. R., Muldoon, M. F., Hall, M., Buysse, D. J. and Manuck, S. B. (2007). Self-reported sleep quality is associated with the metabolic syndrome. Sleep, 30, 219223.CrossRefGoogle ScholarPubMed
Johns, M. W. (1991). A New Method for Measuring Daytime Sleepiness: The Epworth Sleepiness Scale. Sleep, 14, 540545. doi: 10.1093/sleep/14.6.540.CrossRefGoogle ScholarPubMed
Kline, C. E. et al. (2012). Dose–response effects of exercise training on the subjective sleep quality of postmenopausal women: exploratory analyses of a randomised controlled trial. BMJ open, 2, e001044.CrossRefGoogle ScholarPubMed
Kukull, W., Larson, E., Teri, L., Bowen, J., McCormick, W. and Pfanschmidt, M. (1994). The Mini-Mental State Examination score and the clinical diagnosis of dementia. Journal of clinical epidemiology, 47, 10611067.CrossRefGoogle ScholarPubMed
Langlois, F., Vu, T. T. M., Kergoat, M. J., Chassé, K., Dupuis, G. and Bherer, L. (2012). The multiple dimensions of frailty: physical capacity, cognition, and quality of life. International Psychogeriatrics, 24, 14291436. doi: 10.1017/S1041610212000634.CrossRefGoogle Scholar
Lezak, M., Howieson, D., Loring, D., Hannay, H. and Fischer, J.S. (2004). Neuropsychological Assessment (4 ed.). New York: Oxford University Press.Google Scholar
Ling, A., Lim, M. L., Gwee, X., Ho, R. C. M., Collinson, S. L. and Ng, T.-P. (2016). Insomnia and daytime neuropsychological test performance in older adults. Sleep Medicine, 17, 712. doi: 10.1016/j.sleep.2015.07.037.CrossRefGoogle ScholarPubMed
Maggio, M. et al. (2012). The hormonal pathway to cognitive impairment in older men. Journal of Nutrition, Health and Aging, 16, 4054. doi: 10.1007/s12603-012-0002-7.CrossRefGoogle ScholarPubMed
Miyata, S., Noda, A., Iwamoto, K., Kawano, N., Okuda, M. and Ozaki, N. (2013). Poor sleep quality impairs cognitive performance in older adults. Journal of sleep research, 22, 535541.CrossRefGoogle ScholarPubMed
Mondal, P., Gjevre, J. A., Taylor-Gjevre, R. M. and Lim, H. J. (2013). Relationship between the Pittsburgh Sleep Quality Index and the Epworth Sleepiness Scale in a sleep laboratory referral population. Nature and Science of Sleep, 5, 15.Google Scholar
Nebes, R. D., Buysse, D. J., Halligan, E. M., Houck, P. R. and Monk, T. H. (2009). Self-reported sleep quality predicts poor cognitive performance in healthy older adults. The Journals of Gerontology: Series B, 64B, 180187. doi: 10.1093/geronb/gbn037.CrossRefGoogle Scholar
Potvin, O. et al. (2012). Sleep quality and 1-year incident cognitive impairment in community-dwelling older adults. Sleep, 35, 491499. doi: 10.5665/sleep.1732.CrossRefGoogle ScholarPubMed
Praticò, D., Clark, C. M., Liun, F., Lee, V. Y.-M. and Trojanowski, J. Q. (2002). Increase of brain oxidative stress in mild cognitive impairment: a possible predictor of Alzheimer disease. Archives of Neurology, 59, 972976.CrossRefGoogle ScholarPubMed
Preacher, K. J. and Hayes, A. F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments & Computers, 36, 717731.CrossRefGoogle ScholarPubMed
Rockwood, K., Stolee, P. and McDowell, I. (1996). Factors associated with institutionalization of older people in Canada: testing a multifactorial definition of frailty. Journal of the American Geriatrics Society, 44, 578582.CrossRefGoogle ScholarPubMed
Šidák, Z. (1967). Rectangular confidence regions for the means of multivariate normal distributions. Journal of the American Statistical Association, 62, 626633.Google Scholar
Solfrizzi, V. et al. (2013). Frailty syndrome and the risk of vascular dementia: the Italian Longitudinal Study on Aging. Alzheimer’s & Dementia, 9, 113122.CrossRefGoogle ScholarPubMed
Spira, A. P., for the Osteoporotic Fractures in Men, S., Beaudreau, S. A., for the Osteoporotic Fractures in Men, S., Stone, K. L., for the Osteoporotic Fractures in Men, S., … for the Osteoporotic Fractures in Men, S. (2012). Reliability and validity of the Pittsburgh Sleep Quality Index and the Epworth sleepiness scale in older men. The Journals of Gerontology: Series A, 67A, 433439. doi: 10.1093/gerona/glr172.CrossRefGoogle Scholar
Stewart, A. L., Mills, K.M., King, A.C., Haskell, W.L., Gillis, D. and Ritter, P.L. (2001). CHAMPS Physical Activities Questionnaire for Older Adults: outcomes for interventions. Medicine and Science in Sports and Exercise, 33, 11261141.CrossRefGoogle ScholarPubMed
Stranahan, A. M. et al. (2008). Diet–induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle–aged rats. Hippocampus, 18, 10851088.CrossRefGoogle ScholarPubMed
Vignola, A. L. C, Bastien, C. H. and Morin, C. M. (2000). Effects of chronic insomnia and use of benzodiazepines on daytime performance in older adults. The Journals of Gerontology: Series B, 55, P54P62. doi: 10.1093/geronb/55.1.P54.Google ScholarPubMed
Waller, K. L. et al. (2016). Subjective sleep quality and daytime sleepiness in late midlife and their association with age-related changes in cognition. Sleep Medicine, 17, 165173. doi: 10.1016/j.sleep.2015.01.004CrossRefGoogle ScholarPubMed
Wang, C. et al. (2017). Frailty in relation to the risk of Alzheimer’s disease, dementia, and death in older Chinese adults: a seven-year prospective study. Journal of Nutrition Health & Aging, 21, 648654. doi: 10.1007/s12603-016-0798-7.CrossRefGoogle ScholarPubMed
World Health Organization (2015). World report on aging and health. Geneva, Switzerland: World Health Organization.Google Scholar
Winocur, G. et al. (2005). Memory impairment in obese Zucker rats: an investigation of cognitive function in an animal model of insulin resistance and obesity. Behavioral Neuroscience, 119, 1389.CrossRefGoogle Scholar
Wu, Y. H. et al. (2015). Cognitive function in individuals with physical frailty but without dementia or cognitive complaints: results from the I-Lan Longitudinal Aging Study. Journal of the American Medical Directors Association, 16, 899–e9.CrossRefGoogle ScholarPubMed
Young, T. et al. (2002). Predictors of sleep-disordered breathing in community-dwelling adults: the sleep heart health study. Archives of Internal Medicine, 162, 893900. doi: 10.1001/archinte.162.8.893.CrossRefGoogle ScholarPubMed