Actigraphic and melatonin alignment in older adults with varying dementia risk

ABSTRACT Circadian rhythms alter with ageing and may be aetiologically linked to neurodegeneration. This study explored the association between clinical markers and 1) dim light melatonin onset (DLMO) time and 2) phase angle derived from sleep midpoint, in older adults with varying dementia risks. Participants completed 14 days of actigraphy followed by in-lab measurement of salivary melatonin, from which DLMO time and phase angle were computed. Eighty participants (age = 65.5, SD = 9.6), 44 males (55%), MMSE (28.6, SD = 1.5) were included in the analysis. Sex (t = 2.15, p = .04), sleep onset (r = 0.49, p < .001) and midpoint (r = 0.44, p < .001) also correlated with DLMO time. Multiple linear regression showed chronotype, average actigraphy-derived light exposure during the DLMO window (window 2 h prior to DLMO to 2 h post), early biological day (6–10 h post DLMO time) and late biological day (10–14 h post DLMO time) were predictive of DLMO time (adjusted R2 = 0.75). Sleep offset, depression severity, average light exposure during the early biological night and early and late biological day were shown to be predictive variables in the estimation of phase angle (adjusted R2 = 0.78). The current study highlights the potential use of clinical variables, such as actigraphy-derived light, as circadian markers in ageing which could be easily implemented into existing clinical practice and could yield potential targets focusing on chronotherapeutic interventions.

[1]  A. Phillips,et al.  Light-based methods for predicting circadian phase in delayed sleep–wake phase disorder , 2021, Scientific Reports.

[2]  M. Albert,et al.  Associations of actigraphic sleep and circadian rest/activity rhythms with cognition in the early phase of Alzheimer’s disease , 2021, Sleep advances : a journal of the Sleep Research Society.

[3]  Marcela I. Cespedes,et al.  Rest-activity functioning is related to white matter microarchitecture and modifiable risk factors in older adults at-risk for dementia. , 2021, Sleep.

[4]  Daniel B. Forger,et al.  Predicting circadian misalignment with wearable technology: Validation of wrist-worn actigraphy and photometry in night shift workers. , 2020, Sleep.

[5]  J. Krieger,et al.  Early chronotype with advanced activity rhythms and dim light melatonin onset in a rural population , 2020, Journal of pineal research.

[6]  I. Hickie,et al.  Circadian rhythm and sleep alterations in older people with lifetime depression: a case-control study , 2020, BMC Psychiatry.

[7]  Cumulative Illness Rating Scale for Geriatrics , 2020, Definitions.

[8]  Andrew J. Zele,et al.  The accuracy of artificial and natural light measurements by actigraphs , 2019, Journal of sleep research.

[9]  K. Reid Assessment of Circadian Rhythms. , 2019, Neurologic clinics.

[10]  A. Payton,et al.  Longitudinal change of sleep timing: association between chronotype and longevity in older adults , 2019, Chronobiology international.

[11]  K. Yaffe,et al.  Association between circadian rhythms and neurodegenerative diseases , 2019, The Lancet Neurology.

[12]  M. Irwin,et al.  Implications of sleep disturbance and inflammation for Alzheimer's disease dementia , 2019, The Lancet Neurology.

[13]  F. Şahin,et al.  Evidence for an association of serum melatonin concentrations with recognition and circadian preferences in patients with schizophrenia , 2019, Metabolic Brain Disease.

[14]  B. Hankin,et al.  The relationship between depression and chronotype: A longitudinal assessment during childhood and adolescence , 2017, Depression and anxiety.

[15]  Akane Sano,et al.  Irregular sleep/wake patterns are associated with poorer academic performance and delayed circadian and sleep/wake timing , 2017, Scientific Reports.

[16]  L. Fogg,et al.  Sleep and circadian variability in people with delayed sleep-wake phase disorder versus healthy controls. , 2017, Sleep medicine.

[17]  Lisa A. Ostrin Objectively Measured Light Exposure in Emmetropic and Myopic Adults. , 2017, Optometry and vision science : official publication of the American Academy of Optometry.

[18]  D. Holtzman,et al.  Mechanisms linking circadian clocks, sleep, and neurodegeneration , 2016, Science.

[19]  M. LeBourgeois,et al.  Bedtime and evening light exposure influence circadian timing in preschool-age children: A field study , 2016, Neurobiology of sleep and circadian rhythms.

[20]  Manuel Schabus,et al.  ‘nparACT’ package for R: A free software tool for the non-parametric analysis of actigraphy data , 2016, MethodsX.

[21]  Joanna Mattis,et al.  Circadian Rhythms, Sleep, and Disorders of Aging , 2016, Trends in Endocrinology & Metabolism.

[22]  Gordon Jackson-Koku,et al.  Beck Depression Inventory. , 2016, Occupational medicine.

[23]  I. Hickie,et al.  Clinical correlates of chronotypes in young persons with mental disorders , 2015, Chronobiology international.

[24]  T. Kantermann,et al.  Comparing the Morningness-Eveningness Questionnaire and Munich ChronoType Questionnaire to the Dim Light Melatonin Onset , 2015, Journal of biological rhythms.

[25]  S. Sorbi,et al.  Sleep and Cognitive Decline: A Strong Bidirectional Relationship. It Is Time for Specific Recommendations on Routine Assessment and the Management of Sleep Disorders in Patients with Mild Cognitive Impairment and Dementia , 2015, European Neurology.

[26]  T. Fehr,et al.  The effect of bright light therapy on sleep and circadian rhythms in renal transplant recipients: a pilot randomized, multicentre wait‐list controlled trial , 2015, Transplant international : official journal of the European Society for Organ Transplantation.

[27]  J. Duffy,et al.  Why the dim light melatonin onset (DLMO) should be measured before treatment of patients with circadian rhythm sleep disorders. , 2014, Sleep medicine reviews.

[28]  B. Middleton,et al.  Circadian phase asessment by ambulatory monitoring in humans: Correlation with dim light melatonin onset , 2014, Chronobiology international.

[29]  I. Hickie,et al.  Circadian misalignment and sleep disruption in mild cognitive impairment. , 2013, Journal of Alzheimer's disease : JAD.

[30]  Lia Fernandes,et al.  Aging, circadian rhythms and depressive disorders: a review. , 2013, American journal of neurodegenerative disease.

[31]  S. Crowley Assessment of Circadian Rhythms , 2013 .

[32]  Evan D. Chinoy,et al.  Entrainment of the Human Circadian Clock to the Natural Light-Dark Cycle , 2013, Current Biology.

[33]  Jenny Lee,et al.  Cognitive deficit is associated with phase advance of sleep–wake rhythm, daily napping, and prolonged sleep duration—a cross-sectional study in 2,947 community-dwelling older adults , 2013, AGE.

[34]  I. Hickie,et al.  The neurobiology of depression in later-life: Clinical, neuropsychological, neuroimaging and pathophysiological features , 2012, Progress in Neurobiology.

[35]  S. Cummings,et al.  Circadian activity rhythms and risk of incident dementia and mild cognitive impairment in older women , 2011, Annals of neurology.

[36]  C. Looman,et al.  Evaluation of salivary melatonin measurements for Dim Light Melatonin Onset calculations in patients with possible sleep-wake rhythm disorders. , 2011, Clinica chimica acta; international journal of clinical chemistry.

[37]  S. Nowakowski,et al.  Relationship of morningness–eveningness questionnaire score to melatonin and sleep timing, body mass index and atypical depressive symptoms in peri- and post-menopausal women , 2011, Psychiatry Research.

[38]  Nick C Fox,et al.  The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer's disease , 2011, Alzheimer's & Dementia.

[39]  J. Redman,et al.  Timing of Sleep and Its Relationship with the Endogenous Melatonin Rhythm , 2010, Front. Neur..

[40]  J. Emens,et al.  Circadian misalignment in major depressive disorder , 2009, Psychiatry Research.

[41]  J. Emens,et al.  Phase Angle of Entrainment in Morning‐ and Evening‐Types under Naturalistic Conditions , 2009, Chronobiology international.

[42]  Helen J. Burgess,et al.  Individual Differences in the Amount and Timing of Salivary Melatonin Secretion , 2008, PloS one.

[43]  Richard E Kronauer,et al.  Addition of a non-photic component to a light-based mathematical model of the human circadian pacemaker. , 2007, Journal of theoretical biology.

[44]  J. Paquet,et al.  Daily Light Exposure in Morning-Type and Evening-Type Individuals , 2007, Journal of biological rhythms.

[45]  Gahan Fallone,et al.  Estimating dim light melatonin onset (DLMO) phase in adolescents using summer or school-year sleep/wake schedules. , 2006, Sleep.

[46]  R. Bootzin,et al.  Relationship between dim light melatonin onset and the timing of sleep in sleep onset insomniacs , 2006 .

[47]  C. Eastman,et al.  The dim light melatonin onset following fixed and free sleep schedules , 2005, Journal of sleep research.

[48]  Kenneth P. Wright,et al.  Entrainment of the Human Circadian System by Light , 2005, Journal of biological rhythms.

[49]  Claude Gronfier,et al.  Intrinsic Period and Light Intensity Determine the Phase Relationship between Melatonin and Sleep in Humans , 2005, Journal of biological rhythms.

[50]  C. Jack,et al.  Mild cognitive impairment – beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment , 2004, Journal of internal medicine.

[51]  E. Noell-Waggoner Lighting solutions for contemporary problems of older adults. , 2004, Journal of psychosocial nursing and mental health services.

[52]  J. Paquet,et al.  Phase Relationships between Sleep-Wake Cycle and Underlying Circadian Rhythms in Morningness-Eveningness , 2004, Journal of biological rhythms.

[53]  Simon Lovestone,et al.  Is MCI really just early dementia? A systematic review of conversion studies , 2004, International Psychogeriatrics.

[54]  Christian Cajochen,et al.  A Phase Response Curve to Single Bright Light Pulses in Human Subjects , 2003, The Journal of physiology.

[55]  A. Pack,et al.  The validity and feasibility of saliva melatonin assessment in the elderly , 2003, Journal of pineal research.

[56]  Richard E Kronauer,et al.  Comparisons of the Variability of Three Markers of the Human Circadian Pacemaker , 2002, Journal of biological rhythms.

[57]  C. Eastman,et al.  SLEEP LOGS OF YOUNG ADULTS WITH SELF-SELECTED SLEEP TIMES PREDICT THE DIM LIGHT MELATONIN ONSET , 2002, Chronobiology international.

[58]  R. Kronauer,et al.  Stability, precision, and near-24-hour period of the human circadian pacemaker. , 1999, Science.

[59]  D. Dawson,et al.  Salivary Melatonin as a Circadian Phase Marker: Validation and Comparison to Plasma Melatonin , 1997, Journal of biological rhythms.

[60]  M. Okawa,et al.  Circadian rhythm disorders in sleep-waking and body temperature in elderly patients with dementia and their treatment. , 1991, Sleep.

[61]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[62]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[63]  Serge Daan,et al.  A functional analysis of circadian pacemakers in nocturnal rodents , 2005, Journal of comparative physiology.

[64]  M. First,et al.  The Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I) and the Structured Clinical Interview for DSM-IV Axis II Disorders (SCID-II). , 2004 .

[65]  E. Byrne,et al.  The effect of bright light therapy on sleep. , 2003 .

[66]  E. V. van Someren,et al.  Functional plasticity of the circadian timing system in old age: light exposure. , 2002, Progress in brain research.

[67]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.