The Emerging Role of Sleep in the Development of Alzheimer Disease

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Mon, 01/14/2019 - 00:00

 

More than 5 million Americans are living with Alzheimer disease (AD), making this the leading cause of dementia in the United States. This number is projected to nearly triple to 14 million people by 2060 (Matthews KA, et al. Alzheimers Dement. 2018 Sep 17. doi: 10.1016/j.jalz.2018.06.3063. [Epub ahead of print]).

Dr. Raman K. Malhotra


Experts predict estimated costs related to AD to be more than $500 billion annually starting in 2040 (Hurd MD, et al. N Engl J Med. 2013;368[14]:1326). AD is a neurodegenerative disorder characterized by gradual, progressive decline in memory along with other cognitive functions, eventually leading to impairment in activities of daily living. Most current treatments for AD are symptomatic and only minimally slow progression of disease. The increasing prevalence, overwhelming costs to society, and the absence of a cure for AD have created an impending national health crisis.

As the dementia progresses, sleep also tends to worsen. Currently, clinicians improve sleep in patients already diagnosed with AD through diagnosis and treatment of sleep disorders, such as insomnia and sleep apnea to improve overall functioning and quality of life. Treatment of obstructive sleep apnea (OSA) with continuous positive airway pressure (CPAP) in patients diagnosed with AD has shown to improve cognition and other neurocognitive measures (Ancoli-Israel S, et al. J Am Geriatr Soc. 2008;56[11]:2076).

However, there is mounting interest in evaluating how poor sleep could lead to future development of AD or serve as a marker for AD disease in preclinical or asymptomatic populations. Sleep symptoms can be a precursor of other neurological diseases; for example, dream enactment (REM sleep behavior disorder) can precede onset of neurodegenerative disease (Parkinson disease) by decades. Increasing evidence suggests that sleep disruption seen in early or even preclinical AD contributes to its onset and progression. In response to this growing body of research, in June 2018, the American Academy of Sleep Medicine (AASM) issued a health advisory to patients and providers to consider early intervention to ensure sufficient sleep and to treat sleep disorders to assist prevention or delaying onset of AD.
 

Poor Sleep as a Risk Factor for Alzheimer Disease

Epidemiologic studies (both cross-sectional and prospective studies) have demonstrated that fragmented sleep in cognitively normal individuals is a risk factor for the future development of symptomatic AD (Bubu OM, et al. Sleep. 2017[Jan]:1;40). The pathogenesis of AD includes abnormal accumulation of the protein, amyloid-β (Aβ), in the brain as insoluble extracellular plaques followed by intracellular aggregation of tau, neuronal loss, and cognitive dysfunction. Aβ deposition in the brain begins approximately15 to 20 years before the onset of cognitive impairment and serves as an early biomarker of AD. Accumulation of Aβ results from imbalance between production and clearance of the protein from the central nervous system.

Numerous studies have demonstrated that people with disrupted sleep may show early evidence of AD disease, such as Aβ deposition compared with healthy sleepers. In one study, cognitively normal people with Aβ plaque disease had worse sleep efficiency and increased nap frequency measured by actigraphy as compared with cognitively normal individuals without Aβ plaques (Ju YE, et al. JAMA Neurol. 2013 [May];70[5]:587). Further, a recent study found that self-reported daytime sleepiness was associated with longitudinal increases in Aβ deposition (Carvalho DZ, et al. JAMA Neurol. 2018[Jun];75[6]:672).
 

 

 

Possible Mechanisms

Possible mechanisms have been suggested to explain how poor sleep may lead to AD. Over the past 10 years, sleep deprivation was found to increase Aβ concentrations in both a mouse model (Kang JE, et al. Science. 2009; 326:1005) and humans, most likely through increased production and/or release of Aβ (Lucey BP, et al. Ann Neurol. 2018; 83[1]:197). Sleep also appears to increase clearance of proteins and other molecules via bulk fluid flow (“glymphatic” clearance). Glymphatic clearance may enable the removal of interstitial toxic proteins, such as Aβ, through a dynamic interaction between the cerebrospinal fluid and the interstitial fluid, where astrocytes facilitate extracellular fluid transit though the brain during sleep (Xie L, et al. Science. 2013;342:373). Since Aβ deposition in the brain is concentration-dependent, higher Aβ levels from sleep disturbance could lead to greater deposition in the brain.
 

Circadian Rhythm and Alzheimer Disease

Another mechanism linking sleep to the pathogenesis of AD includes disruption of the circadian rhythm, which is commonly seen in patients with AD. Studies have linked populations who suffer from circadian rhythm disorders to higher rates of dementia (Tranah GJ, et al. Ann Neurol. 2011;70[5]:722). Circadian disruption may predispose the brain to neurodegenerative conditions by altering immune function, disrupting endocrine function, increasing inflammation and oxidative stress, or affecting neurogenesis (in specific areas such as the hippocampus). Thus, inadequate sleep could prime the brain for neurodegeneration by multiple pathways.
 

Obstructive Sleep Apnea and Alzheimer’s Disease

Sleep disruption and chronic intermittent hypoxia secondary to untreated OSA has also been associated with AD. Numerous studies have shown that sleep-disordered breathing is associated with AD risk and that AD patients have higher rates of OSA. For instance, a study in older women found that moderate and severe sleep-disordered breathing was associated with an increased risk of future cognitive impairment and dementia (Yaffe K, et al. JAMA. 2011[Aug]:10;306[6]:613). In addition to sleep disruption from sleep apnea affecting Aβ as detailed above, hypoxia from sleep apnea may also alter risk of future AD.
 

Future Directions

Studies support a clear bidirectional relationship between AD and sleep. As researchers continue to investigate sleep as a marker for AD, others are exploring the implications of using sleep interventions to prevent and/or delay the onset of AD. Patients with poor and disrupted sleep may be the ideal candidates for sleep interventions to lower the risk of AD, such as treating OSA with CPAP therapy or insomnia with hypnotic medication or cognitive behavioral therapy. These therapies are already well-studied and approved for human use, allowing for rapid translation to future intervention trials.



Dr. Malhotra is Associate Professor, Sleep Medicine Section; and Dr. Lucey is Assistant Professor, Director-Sleep Medicine Section; Department of Neurology, Washington University School of Medicine, St Louis, Missouri.
 

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More than 5 million Americans are living with Alzheimer disease (AD), making this the leading cause of dementia in the United States. This number is projected to nearly triple to 14 million people by 2060 (Matthews KA, et al. Alzheimers Dement. 2018 Sep 17. doi: 10.1016/j.jalz.2018.06.3063. [Epub ahead of print]).

Dr. Raman K. Malhotra


Experts predict estimated costs related to AD to be more than $500 billion annually starting in 2040 (Hurd MD, et al. N Engl J Med. 2013;368[14]:1326). AD is a neurodegenerative disorder characterized by gradual, progressive decline in memory along with other cognitive functions, eventually leading to impairment in activities of daily living. Most current treatments for AD are symptomatic and only minimally slow progression of disease. The increasing prevalence, overwhelming costs to society, and the absence of a cure for AD have created an impending national health crisis.

As the dementia progresses, sleep also tends to worsen. Currently, clinicians improve sleep in patients already diagnosed with AD through diagnosis and treatment of sleep disorders, such as insomnia and sleep apnea to improve overall functioning and quality of life. Treatment of obstructive sleep apnea (OSA) with continuous positive airway pressure (CPAP) in patients diagnosed with AD has shown to improve cognition and other neurocognitive measures (Ancoli-Israel S, et al. J Am Geriatr Soc. 2008;56[11]:2076).

However, there is mounting interest in evaluating how poor sleep could lead to future development of AD or serve as a marker for AD disease in preclinical or asymptomatic populations. Sleep symptoms can be a precursor of other neurological diseases; for example, dream enactment (REM sleep behavior disorder) can precede onset of neurodegenerative disease (Parkinson disease) by decades. Increasing evidence suggests that sleep disruption seen in early or even preclinical AD contributes to its onset and progression. In response to this growing body of research, in June 2018, the American Academy of Sleep Medicine (AASM) issued a health advisory to patients and providers to consider early intervention to ensure sufficient sleep and to treat sleep disorders to assist prevention or delaying onset of AD.
 

Poor Sleep as a Risk Factor for Alzheimer Disease

Epidemiologic studies (both cross-sectional and prospective studies) have demonstrated that fragmented sleep in cognitively normal individuals is a risk factor for the future development of symptomatic AD (Bubu OM, et al. Sleep. 2017[Jan]:1;40). The pathogenesis of AD includes abnormal accumulation of the protein, amyloid-β (Aβ), in the brain as insoluble extracellular plaques followed by intracellular aggregation of tau, neuronal loss, and cognitive dysfunction. Aβ deposition in the brain begins approximately15 to 20 years before the onset of cognitive impairment and serves as an early biomarker of AD. Accumulation of Aβ results from imbalance between production and clearance of the protein from the central nervous system.

Numerous studies have demonstrated that people with disrupted sleep may show early evidence of AD disease, such as Aβ deposition compared with healthy sleepers. In one study, cognitively normal people with Aβ plaque disease had worse sleep efficiency and increased nap frequency measured by actigraphy as compared with cognitively normal individuals without Aβ plaques (Ju YE, et al. JAMA Neurol. 2013 [May];70[5]:587). Further, a recent study found that self-reported daytime sleepiness was associated with longitudinal increases in Aβ deposition (Carvalho DZ, et al. JAMA Neurol. 2018[Jun];75[6]:672).
 

 

 

Possible Mechanisms

Possible mechanisms have been suggested to explain how poor sleep may lead to AD. Over the past 10 years, sleep deprivation was found to increase Aβ concentrations in both a mouse model (Kang JE, et al. Science. 2009; 326:1005) and humans, most likely through increased production and/or release of Aβ (Lucey BP, et al. Ann Neurol. 2018; 83[1]:197). Sleep also appears to increase clearance of proteins and other molecules via bulk fluid flow (“glymphatic” clearance). Glymphatic clearance may enable the removal of interstitial toxic proteins, such as Aβ, through a dynamic interaction between the cerebrospinal fluid and the interstitial fluid, where astrocytes facilitate extracellular fluid transit though the brain during sleep (Xie L, et al. Science. 2013;342:373). Since Aβ deposition in the brain is concentration-dependent, higher Aβ levels from sleep disturbance could lead to greater deposition in the brain.
 

Circadian Rhythm and Alzheimer Disease

Another mechanism linking sleep to the pathogenesis of AD includes disruption of the circadian rhythm, which is commonly seen in patients with AD. Studies have linked populations who suffer from circadian rhythm disorders to higher rates of dementia (Tranah GJ, et al. Ann Neurol. 2011;70[5]:722). Circadian disruption may predispose the brain to neurodegenerative conditions by altering immune function, disrupting endocrine function, increasing inflammation and oxidative stress, or affecting neurogenesis (in specific areas such as the hippocampus). Thus, inadequate sleep could prime the brain for neurodegeneration by multiple pathways.
 

Obstructive Sleep Apnea and Alzheimer’s Disease

Sleep disruption and chronic intermittent hypoxia secondary to untreated OSA has also been associated with AD. Numerous studies have shown that sleep-disordered breathing is associated with AD risk and that AD patients have higher rates of OSA. For instance, a study in older women found that moderate and severe sleep-disordered breathing was associated with an increased risk of future cognitive impairment and dementia (Yaffe K, et al. JAMA. 2011[Aug]:10;306[6]:613). In addition to sleep disruption from sleep apnea affecting Aβ as detailed above, hypoxia from sleep apnea may also alter risk of future AD.
 

Future Directions

Studies support a clear bidirectional relationship between AD and sleep. As researchers continue to investigate sleep as a marker for AD, others are exploring the implications of using sleep interventions to prevent and/or delay the onset of AD. Patients with poor and disrupted sleep may be the ideal candidates for sleep interventions to lower the risk of AD, such as treating OSA with CPAP therapy or insomnia with hypnotic medication or cognitive behavioral therapy. These therapies are already well-studied and approved for human use, allowing for rapid translation to future intervention trials.



Dr. Malhotra is Associate Professor, Sleep Medicine Section; and Dr. Lucey is Assistant Professor, Director-Sleep Medicine Section; Department of Neurology, Washington University School of Medicine, St Louis, Missouri.
 

 

More than 5 million Americans are living with Alzheimer disease (AD), making this the leading cause of dementia in the United States. This number is projected to nearly triple to 14 million people by 2060 (Matthews KA, et al. Alzheimers Dement. 2018 Sep 17. doi: 10.1016/j.jalz.2018.06.3063. [Epub ahead of print]).

Dr. Raman K. Malhotra


Experts predict estimated costs related to AD to be more than $500 billion annually starting in 2040 (Hurd MD, et al. N Engl J Med. 2013;368[14]:1326). AD is a neurodegenerative disorder characterized by gradual, progressive decline in memory along with other cognitive functions, eventually leading to impairment in activities of daily living. Most current treatments for AD are symptomatic and only minimally slow progression of disease. The increasing prevalence, overwhelming costs to society, and the absence of a cure for AD have created an impending national health crisis.

As the dementia progresses, sleep also tends to worsen. Currently, clinicians improve sleep in patients already diagnosed with AD through diagnosis and treatment of sleep disorders, such as insomnia and sleep apnea to improve overall functioning and quality of life. Treatment of obstructive sleep apnea (OSA) with continuous positive airway pressure (CPAP) in patients diagnosed with AD has shown to improve cognition and other neurocognitive measures (Ancoli-Israel S, et al. J Am Geriatr Soc. 2008;56[11]:2076).

However, there is mounting interest in evaluating how poor sleep could lead to future development of AD or serve as a marker for AD disease in preclinical or asymptomatic populations. Sleep symptoms can be a precursor of other neurological diseases; for example, dream enactment (REM sleep behavior disorder) can precede onset of neurodegenerative disease (Parkinson disease) by decades. Increasing evidence suggests that sleep disruption seen in early or even preclinical AD contributes to its onset and progression. In response to this growing body of research, in June 2018, the American Academy of Sleep Medicine (AASM) issued a health advisory to patients and providers to consider early intervention to ensure sufficient sleep and to treat sleep disorders to assist prevention or delaying onset of AD.
 

Poor Sleep as a Risk Factor for Alzheimer Disease

Epidemiologic studies (both cross-sectional and prospective studies) have demonstrated that fragmented sleep in cognitively normal individuals is a risk factor for the future development of symptomatic AD (Bubu OM, et al. Sleep. 2017[Jan]:1;40). The pathogenesis of AD includes abnormal accumulation of the protein, amyloid-β (Aβ), in the brain as insoluble extracellular plaques followed by intracellular aggregation of tau, neuronal loss, and cognitive dysfunction. Aβ deposition in the brain begins approximately15 to 20 years before the onset of cognitive impairment and serves as an early biomarker of AD. Accumulation of Aβ results from imbalance between production and clearance of the protein from the central nervous system.

Numerous studies have demonstrated that people with disrupted sleep may show early evidence of AD disease, such as Aβ deposition compared with healthy sleepers. In one study, cognitively normal people with Aβ plaque disease had worse sleep efficiency and increased nap frequency measured by actigraphy as compared with cognitively normal individuals without Aβ plaques (Ju YE, et al. JAMA Neurol. 2013 [May];70[5]:587). Further, a recent study found that self-reported daytime sleepiness was associated with longitudinal increases in Aβ deposition (Carvalho DZ, et al. JAMA Neurol. 2018[Jun];75[6]:672).
 

 

 

Possible Mechanisms

Possible mechanisms have been suggested to explain how poor sleep may lead to AD. Over the past 10 years, sleep deprivation was found to increase Aβ concentrations in both a mouse model (Kang JE, et al. Science. 2009; 326:1005) and humans, most likely through increased production and/or release of Aβ (Lucey BP, et al. Ann Neurol. 2018; 83[1]:197). Sleep also appears to increase clearance of proteins and other molecules via bulk fluid flow (“glymphatic” clearance). Glymphatic clearance may enable the removal of interstitial toxic proteins, such as Aβ, through a dynamic interaction between the cerebrospinal fluid and the interstitial fluid, where astrocytes facilitate extracellular fluid transit though the brain during sleep (Xie L, et al. Science. 2013;342:373). Since Aβ deposition in the brain is concentration-dependent, higher Aβ levels from sleep disturbance could lead to greater deposition in the brain.
 

Circadian Rhythm and Alzheimer Disease

Another mechanism linking sleep to the pathogenesis of AD includes disruption of the circadian rhythm, which is commonly seen in patients with AD. Studies have linked populations who suffer from circadian rhythm disorders to higher rates of dementia (Tranah GJ, et al. Ann Neurol. 2011;70[5]:722). Circadian disruption may predispose the brain to neurodegenerative conditions by altering immune function, disrupting endocrine function, increasing inflammation and oxidative stress, or affecting neurogenesis (in specific areas such as the hippocampus). Thus, inadequate sleep could prime the brain for neurodegeneration by multiple pathways.
 

Obstructive Sleep Apnea and Alzheimer’s Disease

Sleep disruption and chronic intermittent hypoxia secondary to untreated OSA has also been associated with AD. Numerous studies have shown that sleep-disordered breathing is associated with AD risk and that AD patients have higher rates of OSA. For instance, a study in older women found that moderate and severe sleep-disordered breathing was associated with an increased risk of future cognitive impairment and dementia (Yaffe K, et al. JAMA. 2011[Aug]:10;306[6]:613). In addition to sleep disruption from sleep apnea affecting Aβ as detailed above, hypoxia from sleep apnea may also alter risk of future AD.
 

Future Directions

Studies support a clear bidirectional relationship between AD and sleep. As researchers continue to investigate sleep as a marker for AD, others are exploring the implications of using sleep interventions to prevent and/or delay the onset of AD. Patients with poor and disrupted sleep may be the ideal candidates for sleep interventions to lower the risk of AD, such as treating OSA with CPAP therapy or insomnia with hypnotic medication or cognitive behavioral therapy. These therapies are already well-studied and approved for human use, allowing for rapid translation to future intervention trials.



Dr. Malhotra is Associate Professor, Sleep Medicine Section; and Dr. Lucey is Assistant Professor, Director-Sleep Medicine Section; Department of Neurology, Washington University School of Medicine, St Louis, Missouri.
 

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