Digital Sleep Measures and White Matter Health in the Framingham Heart Study

Overview

Journal Explor Med

Date 2021 Dec 20

PMID 34927164

Citations 6

Authors

Robert Joseph Thomas

Hyun Kim

Pauline Maillard

Charles S DeCarli

Eric James Heckman

Cody Karjadi

Ting Fang Alvin Ang

Rhoda Au

Affiliations

Soon will be listed here.

Abstract

Aim: Impaired sleep quality and sleep oxygenation are common sleep pathologies. This study assessed the impact of these abnormalities on white matter (WM) integrity in an epidemiological cohort.

Methods: The target population was the Framingham Heart Study Generation-2/Omni-1 Cohorts. Magnetic resonance imaging (diffusion tensor imaging) was used to assess WM integrity. Wearable digital devices were used to assess sleep quality: the (M1-SleepImage system) and the Nonin WristOx for nocturnal oxygenation. The M1 device collects trunk actigraphy and the electrocardiogram (ECG); sleep stability indices were computed using cardiopulmonary coupling using the ECG. Two nights of recording were averaged.

Results: Stable sleep was positively associated with WM health. Actigraphic periods of wake during the sleep period were associated with increased mean diffusivity. One marker of sleep fragmentation which covaries with respiratory chemoreflex activation was associated with reduced fractional anisotropy and increased mean diffusivity. Both oxygen desaturation index and oxygen saturation time under 90% were associated with pathological directions of diffusion tensor imaging signals. Gender differences were noted across most variables, with female sex showing the larger and significant impact.

Conclusions: Sleep quality assessed by a novel digital analysis and sleep hypoxia was associated with WM injury, especially in women.

Citing Articles

Sleep apnea physiological burdens and markers of white matter injury: the Multi-Ethnic Study of Atherosclerosis.

Hajipour M, Hu W, Esmaeili N, Sands S, Wellman A, Kwon Y J Clin Sleep Med. 2024; 21(3):457-466.

PMID: 39436388 PMC: 11874092. DOI: 10.5664/jcsm.11422.

Association Between Acoustic Features and Brain Volumes: the Framingham Heart Study.

Ding H, Hamel A, Karjadi C, Ang T, Lu S, Thomas R Front Dement. 2024; 2.

PMID: 38911669 PMC: 11192548. DOI: 10.3389/frdem.2023.1214940.

Traditional Chinese medicine improved diabetic kidney disease through targeting gut microbiota.

Wu X, Zhao L, Zhao Y, He X, Zou L, Zhao Y Pharm Biol. 2024; 62(1):423-435.

PMID: 38757785 PMC: 11104709. DOI: 10.1080/13880209.2024.2351946.

Neuroscience meets behavior: A systematic literature review on magnetic resonance imaging of the brain combined with real-world digital phenotyping.

Triana A, Saramaki J, Glerean E, Hayward N Hum Brain Mapp. 2024; 45(4):e26620.

PMID: 38436603 PMC: 10911114. DOI: 10.1002/hbm.26620.

Shifting From Active to Passive Monitoring of Alzheimer Disease: The State of the Research.

Popp Z, Low S, Igwe A, Rahman M, Kim M, Khan R J Am Heart Assoc. 2024; 13(2):e031247.

PMID: 38226518 PMC: 10926806. DOI: 10.1161/JAHA.123.031247.

References

Kertesz A, Polk M, Carr T . Cognition and white matter changes on magnetic resonance imaging in dementia. Arch Neurol. 1990; 47(4):387-91. DOI: 10.1001/archneur.1990.00530040029015. View

Bigler E, Lowry C, Kerr B, Tate D, Hessel C, Earl H . Role of white matter lesions, cerebral atrophy, and APOE on cognition in older persons with and without dementia: the Cache County, Utah, study of memory and aging. Neuropsychology. 2003; 17(3):339-52. DOI: 10.1037/0894-4105.17.3.339. View

Thomas R, Mietus J, Peng C, Guo D, Gozal D, Montgomery-Downs H . Relationship between delta power and the electrocardiogram-derived cardiopulmonary spectrogram: possible implications for assessing the effectiveness of sleep. Sleep Med. 2013; 15(1):125-31. PMC: 4114218. DOI: 10.1016/j.sleep.2013.10.002. View

Bonnet M . The effect of sleep fragmentation on sleep and performance in younger and older subjects. Neurobiol Aging. 1989; 10(1):21-5. DOI: 10.1016/s0197-4580(89)80006-5. View

Kraus M, Susmaras T, Caughlin B, Walker C, Sweeney J, Little D . White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain. 2007; 130(Pt 10):2508-19. DOI: 10.1093/brain/awm216. View

Chondrogiorgi M, Astrakas L, Zikou A, Weis L, Xydis V, Antonini A . Multifocal alterations of white matter accompany the transition from normal cognition to dementia in Parkinson's disease patients. Brain Imaging Behav. 2018; 13(1):232-240. DOI: 10.1007/s11682-018-9863-7. View

Mielke M . Sex and Gender Differences in Alzheimer's Disease Dementia. Psychiatr Times. 2019; 35(11):14-17. PMC: 6390276. View

Chen H, Lu C, Lin H, Chen P, Chou K, Lin W . White matter damage and systemic inflammation in obstructive sleep apnea. Sleep. 2014; 38(3):361-70. PMC: 4335530. DOI: 10.5665/sleep.4490. View

Birkenhager A, van den Meiracker A . Causes and consequences of a non-dipping blood pressure profile. Neth J Med. 2007; 65(4):127-31. View

10.

Munch M, Knoblauch V, Blatter K, Wirz-Justice A, Cajochen C . Is homeostatic sleep regulation under low sleep pressure modified by age?. Sleep. 2007; 30(6):781-92. PMC: 1978345. DOI: 10.1093/sleep/30.6.781. View

11.

Kumar R, Chavez A, Macey P, Woo M, Yan-Go F, Harper R . Altered global and regional brain mean diffusivity in patients with obstructive sleep apnea. J Neurosci Res. 2012; 90(10):2043-52. PMC: 3418429. DOI: 10.1002/jnr.23083. View

12.

Beck D, de Lange A, Maximov I, Richard G, Andreassen O, Nordvik J . White matter microstructure across the adult lifespan: A mixed longitudinal and cross-sectional study using advanced diffusion models and brain-age prediction. Neuroimage. 2020; 224:117441. DOI: 10.1016/j.neuroimage.2020.117441. View

13.

Ferretti M, Martinkova J, Biskup E, Benke T, Gialdini G, Nedelska Z . Sex and gender differences in Alzheimer's disease: current challenges and implications for clinical practice: Position paper of the Dementia and Cognitive Disorders Panel of the European Academy of Neurology. Eur J Neurol. 2020; 27(6):928-943. DOI: 10.1111/ene.14174. View

14.

ODonoghue F, Wellard R, Rochford P, Dawson A, Barnes M, Ruehland W . Magnetic resonance spectroscopy and neurocognitive dysfunction in obstructive sleep apnea before and after CPAP treatment. Sleep. 2012; 35(1):41-8. PMC: 3242686. DOI: 10.5665/sleep.1582. View

15.

Morrell M, Finn L, Kim H, Peppard P, Badr M, Young T . Sleep fragmentation, awake blood pressure, and sleep-disordered breathing in a population-based study. Am J Respir Crit Care Med. 2000; 162(6):2091-6. DOI: 10.1164/ajrccm.162.6.9904008. View

16.

Stepanski E . The effect of sleep fragmentation on daytime function. Sleep. 2002; 25(3):268-76. DOI: 10.1093/sleep/25.3.268. View

17.

Bankir L, Bochud M, Maillard M, Bovet P, Gabriel A, Burnier M . Nighttime blood pressure and nocturnal dipping are associated with daytime urinary sodium excretion in African subjects. Hypertension. 2008; 51(4):891-8. DOI: 10.1161/HYPERTENSIONAHA.107.105510. View

18.

Unruh M, Redline S, An M, Buysse D, Nieto F, Yeh J . Subjective and objective sleep quality and aging in the sleep heart health study. J Am Geriatr Soc. 2008; 56(7):1218-27. DOI: 10.1111/j.1532-5415.2008.01755.x. View

19.

Nicolas R, Hiba B, Dilharreguy B, Barse E, Baillet M, Edde M . Changes Over Time of Diffusion MRI in the White Matter of Aging Brain, a Good Predictor of Verbal Recall. Front Aging Neurosci. 2020; 12:218. PMC: 7456903. DOI: 10.3389/fnagi.2020.00218. View

20.

Ogawa Y, Kanbayashi T, Saito Y, Takahashi Y, Kitajima T, Takahashi K . Total sleep deprivation elevates blood pressure through arterial baroreflex resetting: a study with microneurographic technique. Sleep. 2004; 26(8):986-9. DOI: 10.1093/sleep/26.8.986. View