Association Between Slow-Wave Sleep Loss and Incident Dementia

IMPORTANCE: Slow-wave sleep (SWS) supports the aging brain in many ways, including facilitating the glymphatic clearance of proteins that aggregate in Alzheimer disease. However, the role of SWS in the development of dementia remains equivocal. OBJECTIVE: To determine whether SWS loss with aging is...

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Veröffentlicht in:Archives of neurology (Chicago) 2023-12, Vol.80 (12), p.1326-1333
Hauptverfasser: Himali, Jayandra J, Baril, Andree-Ann, Cavuoto, Marina G, Yiallourou, Stephanie, Wiedner, Crystal D, Himali, Dibya, DeCarli, Charles, Redline, Susan, Beiser, Alexa S, Seshadri, Sudha, Pase, Matthew P
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container_issue 12
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container_title Archives of neurology (Chicago)
container_volume 80
creator Himali, Jayandra J
Baril, Andree-Ann
Cavuoto, Marina G
Yiallourou, Stephanie
Wiedner, Crystal D
Himali, Dibya
DeCarli, Charles
Redline, Susan
Beiser, Alexa S
Seshadri, Sudha
Pase, Matthew P
description IMPORTANCE: Slow-wave sleep (SWS) supports the aging brain in many ways, including facilitating the glymphatic clearance of proteins that aggregate in Alzheimer disease. However, the role of SWS in the development of dementia remains equivocal. OBJECTIVE: To determine whether SWS loss with aging is associated with the risk of incident dementia and examine whether Alzheimer disease genetic risk or hippocampal volumes suggestive of early neurodegeneration were associated with SWS loss. DESIGN, SETTING, AND PARTICIPANTS: This prospective cohort study included participants in the Framingham Heart Study who completed 2 overnight polysomnography (PSG) studies in the time periods 1995 to 1998 and 1998 to 2001. Additional criteria for individuals in this study sample were an age of 60 years or older and no dementia at the time of the second overnight PSG. Data analysis was performed from January 2020 to August 2023. EXPOSURE: Changes in SWS percentage measured across repeated overnight sleep studies over a mean of 5.2 years apart (range, 4.8-7.1 years). MAIN OUTCOME: Risk of incident all-cause dementia adjudicated over 17 years of follow-up from the second PSG. RESULTS: From the 868 Framingham Heart Study participants who returned for a second PSG, this cohort included 346 participants with a mean age of 69 years (range, 60-87 years); 179 (52%) were female. Aging was associated with SWS loss across repeated overnight sleep studies (mean [SD] change, −0.6 [1.5%] per year; P 
doi_str_mv 10.1001/jamaneurol.2023.3889
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However, the role of SWS in the development of dementia remains equivocal. OBJECTIVE: To determine whether SWS loss with aging is associated with the risk of incident dementia and examine whether Alzheimer disease genetic risk or hippocampal volumes suggestive of early neurodegeneration were associated with SWS loss. DESIGN, SETTING, AND PARTICIPANTS: This prospective cohort study included participants in the Framingham Heart Study who completed 2 overnight polysomnography (PSG) studies in the time periods 1995 to 1998 and 1998 to 2001. Additional criteria for individuals in this study sample were an age of 60 years or older and no dementia at the time of the second overnight PSG. Data analysis was performed from January 2020 to August 2023. EXPOSURE: Changes in SWS percentage measured across repeated overnight sleep studies over a mean of 5.2 years apart (range, 4.8-7.1 years). MAIN OUTCOME: Risk of incident all-cause dementia adjudicated over 17 years of follow-up from the second PSG. RESULTS: From the 868 Framingham Heart Study participants who returned for a second PSG, this cohort included 346 participants with a mean age of 69 years (range, 60-87 years); 179 (52%) were female. Aging was associated with SWS loss across repeated overnight sleep studies (mean [SD] change, −0.6 [1.5%] per year; P &lt; .001). Over the next 17 years of follow-up, there were 52 cases of incident dementia. In Cox regression models adjusted for age, sex, cohort, positivity for at least 1 APOE ε4 allele, smoking status, sleeping medication use, antidepressant use, and anxiolytic use, each percentage decrease in SWS per year was associated with a 27% increase in the risk of dementia (hazard ratio, 1.27; 95% CI, 1.06-1.54; P = .01). SWS loss with aging was accelerated in the presence of Alzheimer disease genetic risk (ie, APOE ε4 allele) but not hippocampal volumes measured proximal to the first PSG. CONCLUSIONS AND RELEVANCE: This cohort study found that slow-wave sleep percentage declined with aging and Alzheimer disease genetic risk, with greater reductions associated with the risk of incident dementia. These findings suggest that SWS loss may be a modifiable dementia risk factor.</description><identifier>ISSN: 2168-6149</identifier><identifier>ISSN: 2168-6157</identifier><identifier>EISSN: 2168-6157</identifier><identifier>DOI: 10.1001/jamaneurol.2023.3889</identifier><identifier>PMID: 37902739</identifier><language>eng</language><publisher>United States: American Medical Association</publisher><subject>Age ; Aged ; Aging ; Alleles ; Alzheimer Disease - genetics ; Alzheimer's disease ; Antidepressants ; Apolipoprotein E ; Apolipoprotein E4 - genetics ; Cohort analysis ; Cohort Studies ; Comments ; Data analysis ; Dementia ; Dementia disorders ; Female ; Health risk assessment ; Health risks ; Hippocampus ; Humans ; Male ; Middle Aged ; Neurodegenerative diseases ; Online First ; Original Investigation ; Prospective Studies ; Regression analysis ; Regression models ; Risk factors ; Sleep ; Sleep deprivation ; Sleep, Slow-Wave</subject><ispartof>Archives of neurology (Chicago), 2023-12, Vol.80 (12), p.1326-1333</ispartof><rights>Copyright American Medical Association Dec 2023</rights><rights>Copyright 2023 American Medical Association. All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a410t-d5e4571c492dd40c069da2b5a94f48b871a4335ac79206d3a8bbf7c38864a7ff3</citedby><cites>FETCH-LOGICAL-a410t-d5e4571c492dd40c069da2b5a94f48b871a4335ac79206d3a8bbf7c38864a7ff3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://jamanetwork.com/journals/jamaneurology/articlepdf/10.1001/jamaneurol.2023.3889$$EPDF$$P50$$Gama$$H</linktopdf><linktohtml>$$Uhttps://jamanetwork.com/journals/jamaneurology/fullarticle/10.1001/jamaneurol.2023.3889$$EHTML$$P50$$Gama$$H</linktohtml><link.rule.ids>64,230,314,776,780,881,3327,27901,27902,76458,76461</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37902739$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Himali, Jayandra J</creatorcontrib><creatorcontrib>Baril, Andree-Ann</creatorcontrib><creatorcontrib>Cavuoto, Marina G</creatorcontrib><creatorcontrib>Yiallourou, Stephanie</creatorcontrib><creatorcontrib>Wiedner, Crystal D</creatorcontrib><creatorcontrib>Himali, Dibya</creatorcontrib><creatorcontrib>DeCarli, Charles</creatorcontrib><creatorcontrib>Redline, Susan</creatorcontrib><creatorcontrib>Beiser, Alexa S</creatorcontrib><creatorcontrib>Seshadri, Sudha</creatorcontrib><creatorcontrib>Pase, Matthew P</creatorcontrib><title>Association Between Slow-Wave Sleep Loss and Incident Dementia</title><title>Archives of neurology (Chicago)</title><addtitle>JAMA Neurol</addtitle><description>IMPORTANCE: Slow-wave sleep (SWS) supports the aging brain in many ways, including facilitating the glymphatic clearance of proteins that aggregate in Alzheimer disease. However, the role of SWS in the development of dementia remains equivocal. OBJECTIVE: To determine whether SWS loss with aging is associated with the risk of incident dementia and examine whether Alzheimer disease genetic risk or hippocampal volumes suggestive of early neurodegeneration were associated with SWS loss. DESIGN, SETTING, AND PARTICIPANTS: This prospective cohort study included participants in the Framingham Heart Study who completed 2 overnight polysomnography (PSG) studies in the time periods 1995 to 1998 and 1998 to 2001. Additional criteria for individuals in this study sample were an age of 60 years or older and no dementia at the time of the second overnight PSG. Data analysis was performed from January 2020 to August 2023. EXPOSURE: Changes in SWS percentage measured across repeated overnight sleep studies over a mean of 5.2 years apart (range, 4.8-7.1 years). MAIN OUTCOME: Risk of incident all-cause dementia adjudicated over 17 years of follow-up from the second PSG. RESULTS: From the 868 Framingham Heart Study participants who returned for a second PSG, this cohort included 346 participants with a mean age of 69 years (range, 60-87 years); 179 (52%) were female. Aging was associated with SWS loss across repeated overnight sleep studies (mean [SD] change, −0.6 [1.5%] per year; P &lt; .001). Over the next 17 years of follow-up, there were 52 cases of incident dementia. In Cox regression models adjusted for age, sex, cohort, positivity for at least 1 APOE ε4 allele, smoking status, sleeping medication use, antidepressant use, and anxiolytic use, each percentage decrease in SWS per year was associated with a 27% increase in the risk of dementia (hazard ratio, 1.27; 95% CI, 1.06-1.54; P = .01). SWS loss with aging was accelerated in the presence of Alzheimer disease genetic risk (ie, APOE ε4 allele) but not hippocampal volumes measured proximal to the first PSG. CONCLUSIONS AND RELEVANCE: This cohort study found that slow-wave sleep percentage declined with aging and Alzheimer disease genetic risk, with greater reductions associated with the risk of incident dementia. 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Medical Complete (Alumni)</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Archives of neurology (Chicago)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Himali, Jayandra J</au><au>Baril, Andree-Ann</au><au>Cavuoto, Marina G</au><au>Yiallourou, Stephanie</au><au>Wiedner, Crystal D</au><au>Himali, Dibya</au><au>DeCarli, Charles</au><au>Redline, Susan</au><au>Beiser, Alexa S</au><au>Seshadri, Sudha</au><au>Pase, Matthew P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Association Between Slow-Wave Sleep Loss and Incident Dementia</atitle><jtitle>Archives of neurology (Chicago)</jtitle><addtitle>JAMA Neurol</addtitle><date>2023-12-01</date><risdate>2023</risdate><volume>80</volume><issue>12</issue><spage>1326</spage><epage>1333</epage><pages>1326-1333</pages><issn>2168-6149</issn><issn>2168-6157</issn><eissn>2168-6157</eissn><abstract>IMPORTANCE: Slow-wave sleep (SWS) supports the aging brain in many ways, including facilitating the glymphatic clearance of proteins that aggregate in Alzheimer disease. However, the role of SWS in the development of dementia remains equivocal. OBJECTIVE: To determine whether SWS loss with aging is associated with the risk of incident dementia and examine whether Alzheimer disease genetic risk or hippocampal volumes suggestive of early neurodegeneration were associated with SWS loss. DESIGN, SETTING, AND PARTICIPANTS: This prospective cohort study included participants in the Framingham Heart Study who completed 2 overnight polysomnography (PSG) studies in the time periods 1995 to 1998 and 1998 to 2001. Additional criteria for individuals in this study sample were an age of 60 years or older and no dementia at the time of the second overnight PSG. Data analysis was performed from January 2020 to August 2023. EXPOSURE: Changes in SWS percentage measured across repeated overnight sleep studies over a mean of 5.2 years apart (range, 4.8-7.1 years). MAIN OUTCOME: Risk of incident all-cause dementia adjudicated over 17 years of follow-up from the second PSG. RESULTS: From the 868 Framingham Heart Study participants who returned for a second PSG, this cohort included 346 participants with a mean age of 69 years (range, 60-87 years); 179 (52%) were female. Aging was associated with SWS loss across repeated overnight sleep studies (mean [SD] change, −0.6 [1.5%] per year; P &lt; .001). Over the next 17 years of follow-up, there were 52 cases of incident dementia. In Cox regression models adjusted for age, sex, cohort, positivity for at least 1 APOE ε4 allele, smoking status, sleeping medication use, antidepressant use, and anxiolytic use, each percentage decrease in SWS per year was associated with a 27% increase in the risk of dementia (hazard ratio, 1.27; 95% CI, 1.06-1.54; P = .01). SWS loss with aging was accelerated in the presence of Alzheimer disease genetic risk (ie, APOE ε4 allele) but not hippocampal volumes measured proximal to the first PSG. CONCLUSIONS AND RELEVANCE: This cohort study found that slow-wave sleep percentage declined with aging and Alzheimer disease genetic risk, with greater reductions associated with the risk of incident dementia. These findings suggest that SWS loss may be a modifiable dementia risk factor.</abstract><cop>United States</cop><pub>American Medical Association</pub><pmid>37902739</pmid><doi>10.1001/jamaneurol.2023.3889</doi><tpages>8</tpages></addata></record>
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identifier ISSN: 2168-6149
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subjects Age
Aged
Aging
Alleles
Alzheimer Disease - genetics
Alzheimer's disease
Antidepressants
Apolipoprotein E
Apolipoprotein E4 - genetics
Cohort analysis
Cohort Studies
Comments
Data analysis
Dementia
Dementia disorders
Female
Health risk assessment
Health risks
Hippocampus
Humans
Male
Middle Aged
Neurodegenerative diseases
Online First
Original Investigation
Prospective Studies
Regression analysis
Regression models
Risk factors
Sleep
Sleep deprivation
Sleep, Slow-Wave
title Association Between Slow-Wave Sleep Loss and Incident Dementia
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