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Mid-life sleep is associated with cognitive performance later in life in aging American Indians: data from the Strong Heart Stud

Authors: Luciana Mascarenhas Fonseca|||Myles G Finlay|||Naomi S Chaytor|||Natalie G Morimoto|||Dedra Buchwald|||Hans P A Van Dongen|||Stuart F Quan|||Astrid Suchy-Dicey

Journal: Frontiers in aging neuroscience

Publication Type: Journal Article

Date: 2024

DOI: PMC11188442

ID: 38903901

Affiliations:

Affiliations

    Elson S. Floyd College of Medicine, Washington State University, Spokane, WA, United States.|||Elson S. Floyd College of Medicine, Washington State University, Spokane, WA, United States.|||Elson S. Floyd College of Medicine, Washington State University, Spokane, WA, United States.|||Elson S. Floyd College of Medicine, Washington State University, Spokane, WA, United States.|||Institute for Research and Education to Advance Community Health, Elson S. Floyd College of Medicine, Washington State University, Pullman, WA, United States.|||Elson S. Floyd College of Medicine, Washington State University, Spokane, WA, United States.|||Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, United States.|||Institute for Research and Education to Advance Community Health, Elson S. Floyd College of Medicine, Washington State University, Pullman, WA, United States.

Abstract

Sleep-related disorders have been associated with cognitive decline and neurodegeneration. American Indians are at increased risk for dementia. Here, we aim to characterize, for the first time, the associations between sleep characteristics and subsequent cognitive performance in a sample of aging American Indians.


Reference List

    Aloia M. S., Ilniczky N., Di Dio P., Perlis M. L., Greenblatt D. W., Giles D. E. (2003). Neuropsychological changes and treatment compliance in older adults with sleep apnea. J. Psychosom. Res. 54, 71–76. doi: 10.1016/s0022-3999(02)00548-2, PMID:|||Amiri S., Keffeler J. I., Crain D. R., Denney J. T., Buchwald D. (2024). Racial, ethnic, and rural disparities in distance to physicians among decedents with Alzheimer's disease and related dementias in Washington State. Alzheimers Dement. doi: 10.1002/alz.13756 (Epub ahead of print)., PMID:|||Bateman R. J., Wen G., Morris J. C., Holtzman D. M. (2007). Fluctuations of CSF amyloid-beta levels: implications for a diagnostic and therapeutic biomarker. Neurology 68, 666–669. doi: 10.1212/01.wnl.0000256043.50901.e3, PMID:|||Blackman J., Swirski M., Clynes J., Harding S., Leng Y., Coulthard E. (2021). Pharmacological and non-pharmacological interventions to enhance sleep in mild cognitive impairment and mild Alzheimer's disease: a systematic review. J. Sleep Res. 30:e13229. doi: 10.1111/jsr.13229, PMID:|||Bonanni E., Maestri M., Tognoni G., Fabbrini M., Nucciarone B., Manca M. L., et al. . (2005). Daytime sleepiness in mild and moderate Alzheimer's disease and its relationship with cognitive impairment. J. Sleep Res. 14, 311–317. doi: 10.1111/j.1365-2869.2005.00462.x, PMID:|||Borges C. R., Poyares D., Piovezan R., Nitrini R., Brucki S. (2019). Alzheimer's disease and sleep disturbances: a review. Arq. Neuropsiquiatr. 77, 815–824. doi: 10.1590/0004-282X20190149|||Buysse D. J., Reynolds C. F., Monk T. H., Berman S. R., Kupfer D. J. (1989). The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 28, 193–213. doi: 10.1016/0165-1781(89)90047-4|||Centers for Disease Control and Prevention (CDC) (2003). Diabetes prevalence among American Indians and Alaska natives and the overall population--United States, 1994-2002. MMWR Morb. Mortal Wkly. Rep. 52, 702–704.|||Centers for Disease Control and Prevention (CDC) (2006). Diagnosed diabetes among American Indians and Alaska Natives aged <35 years--United States, 1994-2004. MMWR Morb. Mortal Wkly. Rep. 55, 1201–1203.|||Chen X., Wang R., Zee P., Lutsey P. L., Javaheri S., Alcántara C., et al. . (2015). Racial/ethnic differences in sleep disturbances: the multi-ethnic study of atherosclerosis (MESA). Sleep 38, 877–888. doi: 10.5665/sleep.4732, PMID:|||Choe Y. M., Byun M. S., Yi D., Lee J. H., Jeon S. Y., Sohn B. K., et al. . (2019). Sleep experiences during different lifetime periods and in vivo Alzheimer pathologies. Alzheimers Res. Ther. 11:79. doi: 10.1186/s13195-019-0536-6, PMID:|||Cholerton B., Omidpanah A., Verney S. P., Nelson L. A., Baker L. D., Suchy-Dicey A., et al. . (2019). Type 2 diabetes and later cognitive function in older American Indians: the strong heart study. Int. J. Geriatr. Psychiatry 34, 1050–1057. doi: 10.1002/gps.5108, PMID:|||Cohen-Zion M., Stepnowsky C., Marler S. T., Kripke D. F., Ancoli-Israel S. (2001). Changes in cognitive function associated with sleep disordered breathing in older people. J. Am. Geriatr. Soc. 49, 1622–1627. doi: 10.1046/j.1532-5415.2001.t01-1-49270.x|||Davis C. J., Clinton J. M., Jewett K. A., Zielinski M. R., Krueger J. M. (2011). Delta wave power: an independent sleep phenotype or epiphenomenon? J. Clin. Sleep Med. 7, S16–S18. doi: 10.5664/JCSM.1346, PMID:|||de Souza-Talarico J. N., de Carvalho A. P., Brucki S. M., Nitrini R., Ferretti-Rebustini R. E. (2016). Dementia and cognitive impairment prevalence and associated factors in indigenous populations: a systematic review. Alzheimer Dis. Assoc. Disord. 30, 281–287. doi: 10.1097/WAD.0000000000000140, PMID:|||Delis D. C., Kramer J. H., Kaplan E., Ober B. A. C. V. L. T. (2000). California verbal learning test. 2nd Edn. San Antonio, TX: Psychological Corporation.|||Denney J. T., Zamora-Kapoor A., Hansen D. A., Whitney P. (2023). Race/ethnicity, sleep duration, and mortality risk in the United States. SSM Popul. Health 21:101350. doi: 10.1016/j.ssmph.2023.101350, PMID:|||Drager L. F., McEvoy R. D., Barbe F., Lorenzi-Filho G., Redline S., INCOSACT Initiative (International Collaboration of Sleep Apnea Cardiovascular Trialists) (2017). Sleep apnea and cardiovascular disease: lessons from recent trials and need for team science. Circulation 136, 1840–1850. doi: 10.1161/CIRCULATIONAHA.117.029400, PMID:|||Egan K. J., Knutson K. L., Pereira A. C., von Schantz M. (2017). The role of race and ethnicity in sleep, circadian rhythms and cardiovascular health. Sleep Med. Rev. 33, 70–78. doi: 10.1016/j.smrv.2016.05.004, PMID:|||Eichenbaum H. (2004). Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109–120. doi: 10.1016/j.neuron.2004.08.028|||El-Sheikh M., Philbrook L. E., Kelly R. J., Hinnant J. B., Buckhalt J. A. (2019). What does a good night's sleep mean? Nonlinear relations between sleep and children's cognitive functioning and mental health. Sleep 42:zsz078. doi: 10.1093/sleep/zsz078|||Elwood P. C., Bayer A. J., Fish M., Pickering J., Mitchell C., Gallacher J. E. (2011). Sleep disturbance and daytime sleepiness predict vascular dementia. J. Epidemiol. Community Health 65, 820–824. doi: 10.1136/jech.2009.100503, PMID:|||Fiorillo L., Puiatti A., Papandrea M., Ratti P. L., Favaro P., Roth C., et al. . (2019). Automated sleep scoring: a review of the latest approaches. Sleep Med. Rev. 48:101204. doi: 10.1016/j.smrv.2019.07.007, PMID:|||Foley D., Monjan A., Masaki K., Ross W., Havlik R., White L., et al. . (2001). Daytime sleepiness is associated with 3-year incident dementia and cognitive decline in older Japanese-American men. J. Am. Geriatr. Soc. 49, 1628–1632. doi: 10.1046/j.1532-5415.2001.t01-1-49271.x, PMID:|||Folstein M. F., Folstein S. E., McHugh P. R. (1975). "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189–198. doi: 10.1016/0022-3956(75)90026-6|||Fonseca L. M., Mattar G. P., Haddad G. G., Burduli E., McPherson S. M., Guilhoto L. M. F. F., et al. . (2021). Neuropsychiatric symptoms of Alzheimer’s disease in down syndrome and its impact on caregiver distress. J. Alzheimers Dis. 81, 137–154. doi: 10.3233/JAD-201009, PMID:|||Fultz N. E., Bonmassar G., Setsompop K., Stickgold R. A., Rosen B. R., Polimeni J. R., et al. . (2019). Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep. Science 366, 628–631. doi: 10.1126/science.aax5440|||Gharbi-Meliani A., Dugravot A., Sabia S., Regy M., Fayosse A., Schnitzler A., et al. . (2021). The association of APOE ε4 with cognitive function over the adult life course and incidence of dementia: 20 years follow-up of the Whitehall II study. Alzheimers Res. Ther. 13:5. doi: 10.1186/s13195-020-00740-0, PMID:|||Hale L., Troxel W., Buysse D. J. (2020). Sleep health: an opportunity for public health to address health equity. Annu. Rev. Public Health 41, 81–99. doi: 10.1146/annurev-publhealth-040119-094412, PMID:|||Harris R., Nelson L. A., Muller C., Buchwald D. (2015). Stroke in American Indians and Alaska natives: a systematic review. Am. J. Public Health 105, e16–e26. doi: 10.2105/AJPH.2015.302698, PMID:|||Hope T., Keene J., Gedling K., Fairburn C. G., Jacoby R. (1998). Predictors of institutionalization for people with dementia living at home with a carer. Int. J. Geriatr. Psychiatry 13, 682–690. doi: 10.1002/(sici)1099-1166(1998100)13:10<682::aid-gps847>3.0.co;2-y|||Hutchinson R. N., Shin S. (2014). Systematic review of health disparities for cardiovascular diseases and associated factors among American Indian and Alaska native populations. PLoS One 9:e80973. doi: 10.1371/journal.pone.0080973, PMID:|||Ju G., Yoon I. Y., Lee S. D., Kim T. H., Choe J. Y., Kim K. W. (2012). Effects of sleep apnea syndrome on delayed memory and executive function in elderly adults. J. Am. Geriatr. Soc. 60, 1099–1103. doi: 10.1111/j.1532-5415.2012.03961.x, PMID:|||Kalliny M., McKenzie J. G. (2017). Occupational health and sleep issues in underserved populations. Prim. Care 44, e73–e97. doi: 10.1016/j.pop.2016.09.010, PMID:|||Kocevska D., Lysen T. S., Dotinga A., Koopman-Verhoeff M. E., Luijk M. P. C. M., Antypa N., et al. . (2021). Sleep characteristics across the lifespan in 1.1 million people from the Netherlands, United Kingdom and United States: a systematic review and meta-analysis. Nat. Hum. Behav. 5, 113–122. doi: 10.1038/s41562-020-00965-x, PMID:|||Lim M. M., Gerstner J. R., Holtzman D. M. (2014). The sleep-wake cycle and Alzheimer's disease: what do we know? Neurodegener. Dis. Manag. 4, 351–362. doi: 10.2217/nmt.14.33, PMID:|||Liu J., Ghastine L., Um P., Rovit E., Wu T. (2021). Environmental exposures and sleep outcomes: a review of evidence, potential mechanisms, and implications. Environ. Res. 196:110406. doi: 10.1016/j.envres.2020.110406, PMID:|||Lyketsos C. G., Lopez O., Jones B., Fitzpatrick A. L., Breitner J., DeKosky S. (2002). Prevalence of neuropsychiatric symptoms in dementia and mild cognitive impairment: results from the cardiovascular health study. JAMA 288, 1475–1483. doi: 10.1001/jama.288.12.1475|||Malhotra A., Ayappa I., Ayas N., Collop N., Kirsch D., Mcardle N., et al. . (2021). Metrics of sleep apnea severity: beyond the apnea-hypopnea index. Sleep 44:zsab030. doi: 10.1093/sleep/zsab030|||Manson S. M., Buchwald D. S. (2021). Aging and health of American Indians and Alaska natives: contributions from the native investigator development program. J. Aging Health 33, 3S–9S. doi: 10.1177/08982643211014399, PMID:|||Mascarenhas Fonseca L., Sage Chaytor N., Olufadi Y., Buchwald D., Galvin J. E., Schmitter-Edgecombe M., et al. . (2023). Intraindividual cognitive variability and magnetic resonance imaging in aging American Indians: data from the strong heart study. J. Alzheimers Dis. 91, 1395–1407. doi: 10.3233/JAD-220825, PMID:|||Matthews E. E., Li C., Long C. R., Narcisse M. R., Martin B. C., McElfish P. A. (2018). Sleep deficiency among native Hawaiian/Pacific Islander, Black, and White Americans and the association with cardiometabolic diseases: analysis of the National Health Interview Survey Data. Sleep Health 4, 273–283. doi: 10.1016/j.sleh.2018.01.004, PMID:|||McCoy J. G., Strecker R. E. (2011). The cognitive cost of sleep lost. Neurobiol. Learn. Mem. 96, 564–582. doi: 10.1016/j.nlm.2011.07.004, PMID:|||Mei X., Zhao Z., Qiu Z., Wang J., Yu H., Zheng C. (2023). Association of sleep disorders with clinical symptoms and age in Chinese older adult patients with and without cognitive decline. Front. Aging Neurosci. 15:1189837. doi: 10.3389/fnagi.2023.1189837, PMID:|||Merlino G., Piani A., Gigli G. L., Cancelli I., Rinaldi A., Baroselli A., et al. . (2010). Daytime sleepiness is associated with dementia and cognitive decline in older Italian adults: a population-based study. Sleep Med. 11, 372–377. doi: 10.1016/j.sleep.2009.07.018, PMID:|||Moran M., Lynch C. A., Walsh C., Coen R., Coakley D., Lawlor B. A. (2005). Sleep disturbance in mild to moderate Alzheimer's disease. Sleep Med. 6, 347–352. doi: 10.1016/j.sleep.2004.12.005|||Mullins A. E., Kam K., Parekh A., Bubu O. M., Osorio R. S., Varga A. W. (2020). Obstructive sleep apnea and its treatment in aging: effects on Alzheimer's disease biomarkers, cognition, brain structure and neurophysiology. Neurobiol. Dis. 145:105054. doi: 10.1016/j.nbd.2020.105054, PMID:|||Muto V., Koshmanova E., Ghaemmaghami P., Jaspar M., Meyer C., Elansary M., et al. . (2020). Alzheimer's disease genetic risk and sleep phenotypes: association with more slow-waves and daytime sleepiness. Sleep 44:zsaa137. doi: 10.1093/sleep/zsaa137, PMID:|||Nelson K. L., Davis J. E., Corbett C. F. (2022). Sleep quality: an evolutionary concept analysis. Nurs. Forum 57, 144–151. doi: 10.1111/nuf.12659, PMID:|||Ohayon M. M., Vecchierini M. F. (2002). Daytime sleepiness and cognitive impairment in the elderly population. Arch. Intern. Med. 162, 201–208. doi: 10.1001/archinte.162.2.201|||Oonk M., Tucker A., Belenky G., Van Dongen H. (2008). Excessive sleepiness: determinants, outcomes, and context. Int. J. Sleep Wakefulness. 1, 141–147,|||Pandi-Perumal S. R., Abumuamar A. M., Spence D. W., Chattu V. K., Moscovitch A., BaHammam A. S. (2017). Racial/ethnic and social inequities in sleep medicine: the tip of the iceberg? J. Natl. Med. Assoc. 109, 279–286. doi: 10.1016/j.jnma.2017.04.005, PMID:|||Petersen R. C., Caracciolo B., Brayne C., Gauthier S., Jelic V., Fratiglioni L. (2014). Mild cognitive impairment: a concept in evolution. J. Intern. Med. 275, 214–228. doi: 10.1111/joim.12190|||Petersen R. C., Doody R., Kurz A., Mohs R. C., Morris J. C., Rabins P. V., et al. . (2001). Current concepts in mild cognitive impairment. Arch. Neurol. 58, 1985–1992. doi: 10.1001/archneur.58.12.1985|||Prasad B., Saxena R., Goel N., Patel S. R. (2018). Genetic ancestry for sleep research: leveraging health inequalities to identify causal genetic variants. Chest 153, 1478–1496. doi: 10.1016/j.chest.2018.03.024, PMID:|||Quan S. F., Howard B. V., Iber C., Kiley J. P., Nieto F. J., O'Connor G. T., et al. . (1997). The sleep heart health study: design, rationale, and methods. Sleep 20, 1077–1085, PMID:|||Quan S. F., O’Connor G. T., Quan J. S., Redline S., Resnick H. E., Shahar E., et al. . (2007). Association of physical activity with sleep-disordered breathing. Sleep Breath. 11, 149–157. doi: 10.1007/s11325-006-0095-5|||Quan S. F., Wright R., Baldwin C. M., Kaemingk K. L., Goodwin J. L., Kuo T. F., et al. . (2006). Obstructive sleep apnea-hypopnea and neurocognitive functioning in the sleep heart health study. Sleep Med. 7, 498–507. doi: 10.1016/j.sleep.2006.02.005, PMID:|||Radloff L. S. (1977). The CES-D scale: a self-report depression scale for research in the general population. Appl. Psychol. Meas. 1, 385–401. doi: 10.1177/014662167700100306|||Rechtschaffen A., Kales A. (1968). A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Washington, DC: Public Health Service, US Government Printing Office.|||Redline S., Kapur V. K., Sanders M. H., Quan S. F., Gottlieb D. J., Rapoport D. M., et al. . (2000). Effects of varying approaches for identifying respiratory disturbances on sleep apnea assessment. Am. J. Respir. Crit. Care Med. 161, 369–374. doi: 10.1164/ajrccm.161.2.9904031, PMID:|||Redline S., Sanders M. H., Lind B. K., Quan S. F., Iber C., Gottlieb D. J., et al. . (1998). Methods for obtaining and analyzing unattended polysomnography data for a multicenter study. Sleep heart Health Research Group. Sleep 21, 759–767, PMID:|||Robbins R., Quan S. F., Weaver M. D., Bormes G., Barger L. K., Czeisler C. A. (2021a). Examining sleep deficiency and disturbance and their risk for incident dementia and all-cause mortality in older adults across 5 years in the United States. Aging 13, 3254–3268. doi: 10.18632/aging.202591, PMID:|||Robbins R., Weaver M. D., Barger L. K., Wang W., Quan S. F., Czeisler C. A. (2021b). Sleep difficulties, incident dementia and all-cause mortality among older adults across 8 years: findings from the National Health and aging trends study. J. Sleep Res. 30:e13395. doi: 10.1111/jsr.13395, PMID:|||Ruff R. M., Light R. H., Parker S. B., Levin H. S. (1996). Benton controlled oral word association test: reliability and updated norms. Arch. Clin. Neuropsychol. 11, 329–338. doi: 10.1093/arclin/11.4.329, PMID:|||Ruiter M. E., DeCoster J., Jacobs L., Lichstein K. L. (2010). Sleep disorders in African Americans and Caucasian Americans: a meta-analysis. Behav. Sleep Med. 8, 246–259. doi: 10.1080/15402002.2010.509251, PMID:|||Ruiter M. E., Decoster J., Jacobs L., Lichstein K. L. (2011). Normal sleep in African-Americans and Caucasian-Americans: a meta-analysis. Sleep Med. 12, 209–214. doi: 10.1016/j.sleep.2010.12.010, PMID:|||Sabia S., Fayosse A., Dumurgier J., van Hees V. T., Paquet C., Sommerlad A., et al. . (2021). Association of sleep duration in middle and old age with incidence of dementia. Nat. Commun. 12:2289. doi: 10.1038/s41467-021-22354-2, PMID:|||Schlosser Covell G. E., Dhawan P. S., Lee Iannotti J. K., Hoffman-Snyder C. R., Wellik K. E., Caselli R. J., et al. . (2012). Disrupted daytime activity and altered sleep-wake patterns may predict transition to mild cognitive impairment or dementia: a critically appraised topic. Neurologist 18, 426–429. doi: 10.1097/NRL.0b013e318272f7ef|||Shin H. Y., Han H. J., Shin D. J., Park H. M., Lee Y. B., Park K. H. (2014). Sleep problems associated with behavioral and psychological symptoms as well as cognitive functions in Alzheimer's disease. J. Clin. Neurol. 10, 203–209. doi: 10.3988/jcn.2014.10.3.203, PMID:|||Spira A. P., Blackwell T., Stone K. L., Redline S., Cauley J. A., Ancoli-Israel S., et al. . (2008). Sleep-disordered breathing and cognition in older women. J. Am. Geriatr. Soc. 56, 45–50. doi: 10.1111/j.1532-5415.2007.01506.x|||Suchy-Dicey A. M., Shibata D., Best L. G., Verney S. P., Longstreth W. T., Jr., Lee E. T., et al. . (2016). Cranial magnetic resonance imaging in elderly American Indians: design, methods, and implementation of the cerebrovascular disease and its consequences in American Indians study. Neuroepidemiology 47, 67–75. doi: 10.1159/000443277, PMID:|||Suchy-Dicey A. M., Shibata D. K., Madhyastha T. M., Grabowski T. J., Longstreth W. T., Buchwald D. S. (2017). Findings of vascular brain injury and structural loss from cranial magnetic resonance imaging in elderly American Indians: the strong heart study. Neuroepidemiology 48, 39–47. doi: 10.1159/000459624, PMID:|||Suh S. W., Han J. W., Lee J. R., Byun S., Kwon S. J., Oh S. H., et al. . (2018). Sleep and cognitive decline: a prospective nondemented elderly cohort study. Ann. Neurol. 83, 472–482. doi: 10.1002/ana.25166|||Tarokh L., Saletin J. M., Carskadon M. A. (2016). Sleep in adolescence: physiology, cognition and mental health. Neurosci. Biobehav. Rev. 70, 182–188. doi: 10.1016/j.neubiorev.2016.08.008, PMID:|||Teng E. L., Chui H. C. (1987). The modified mini-mental state (3MS) examination. J. Clin. Psychiatry 48, 314–318, PMID:|||Terzano M. G., Parrino L., Smerieri A., Chervin R., Chokroverty S., Guilleminault C., et al. . (2002). Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. Sleep Med. 3, 187–199. doi: 10.1016/s1389-9457(02)00003-5, PMID:|||Tsapanou A., Gu Y., O'Shea D., Eich T., Tang M. X., Schupf N., et al. . (2016). Daytime somnolence as an early sign of cognitive decline in a community-based study of older people. Int. J. Geriatr. Psychiatry 31, 247–255. doi: 10.1002/gps.4318, PMID:|||Tsapanou A., Scarmeas N., Stern Y. (2020). Sleep and the aging brain. A multifaceted approach. Sleep Sci 13, 152–156. doi: 10.5935/1984-0063.20190128, PMID:|||Tucker A. M., Dinges D. F., Van Dongen H. P. (2007). Trait interindividual differences in the sleep physiology of healthy young adults. J. Sleep Res. 16, 170–180. doi: 10.1111/j.1365-2869.2007.00594.x, PMID:|||van Straten A., van der Zweerde T., Kleiboer A., Cuijpers P., Morin C. M., Lancee J. (2018). Cognitive and behavioral therapies in the treatment of insomnia: a meta-analysis. Sleep Med. Rev. 38, 3–16. doi: 10.1016/j.smrv.2017.02.001|||Walker M. P. (2009). The role of sleep in cognition and emotion. Ann. N. Y. Acad. Sci. 1156, 168–197. doi: 10.1111/j.1749-6632.2009.04416.x, PMID:|||Wechsler D. (2008). Wechsler adult intelligence scale. 4th Edn: Pearson.|||Woods C. E., Usher K., Maguire G. P. (2015). Obstructive sleep apnoea in adult indigenous populations in high-income countries: an integrative review. Sleep Breath. 19, 45–53. doi: 10.1007/s11325-014-1032-7, PMID:|||Yamout K., Goldstein F. C., Lah J. J., Levey A. I., Bliwise D. L. (2012). Neurocognitive correlates of nocturnal oxygen desaturation in a memory clinic population. J. Clin. Exp. Neuropsychol. 34, 325–332. doi: 10.1080/13803395.2011.642849, PMID:|||Zhao Q. F., Tan L., Wang H. F., Jiang T., Tan M. S., Tan L., et al. . (2016). The prevalence of neuropsychiatric symptoms in Alzheimer's disease: systematic review and meta-analysis. J. Affect. Disord. 190, 264–271. doi: 10.1016/j.jad.2015.09.069|||Zuma B. Z., Parizo J. T., Valencia A., Spencer-Bonilla G., Blum M. R., Scheinker D., et al. . (2021). County-level factors associated with cardiovascular mortality by race/ethnicity. J. Am. Heart Assoc. 10:e018835. doi: 10.1161/JAHA.120.018835, PMID: