Age-Related Changes in Slow Wave Sleep and REM Sleep and Relationship With Growth Hormone and Cortisol Levels in Healthy Men
Abstract
CONTEXT: In young adults, sleep affects the regulation of growth hormone (GH) and cortisol. The relationship between decreased sleep quality in older adults and age-related changes in the regulation of GH and cortisol is unknown. OBJECTIVE: To determine the chronology of age-related changes in sleep duration and quality (sleep stages) in healthy men and whether concomitant alterations occur in GH and cortisol levels. DESIGN AND SETTING: Data combined from a series of studies conducted between 1985 and 1999 at 4 laboratories. SUBJECTS: A total of 149 healthy men, aged 16 to 83 years, with a mean (SD) body mass index of 24.1 (2.3) kg/m( 2), without sleep complaints or histories of endocrine, psychiatric, or sleep disorders. MAIN OUTCOME MEASURES: Twenty-four-hour profiles of plasma GH and cortisol levels and polygraphic sleep recordings. RESULTS: The mean (SEM) percentage of deep slow wave sleep decreased from 18.9% (1.3%) during early adulthood (age 16-25 years) to 3.4% (1.0%) during midlife (age 36-50 years) and was replaced by lighter sleep (stages 1 and 2) without significant increases in sleep fragmentation or decreases in rapid eye movement (REM) sleep. The transition from midlife to late life (age 71-83 years) involved no further significant decrease in slow wave sleep but an increase in time awake of 28 minutes per decade at the expense of decreases in both light non-REM sleep (-24 minutes per decade; P<.001) and REM sleep (-10 minutes per decade; P<.001). The decline in slow wave sleep from early adulthood to midlife was paralleled by a major decline in GH secretion (-372 microg per decade; P<.001). From midlife to late life, GH secretion further declined at a slower rate (-43 microg per decade; P<.02). Independently of age, the amount of GH secretion was significantly associated with slow wave sleep (P<.001). Increasing age was associated with an elevation of evening cortisol levels (+19. 3 nmol/L per decade; P<.001) that became significant only after age 50 years, when sleep became more fragmented and REM sleep declined. A trend for an association between lower amounts of REM sleep and higher evening cortisol concentrations independent of age was detected (P<.10). CONCLUSIONS: In men, age-related changes in slow wave sleep and REM sleep occur with markedly different chronologies and are each associated with specific hormonal alterations. Future studies should evaluate whether strategies to enhance sleep quality may have beneficial hormonal effects. JAMA. 2000;284:861-868
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Age-related changes are associated with a dysregulation of the circadian rhythm of the HPA axis, further leading to sleep problems.
“age-related changes are associated with a dysregulation of the circadian rhythm of the HPA axis (Al-Turk and Al-Dujaili, 2016;Heaney et al., 2012), further leading to sleep problems (Van Cauter et al., 2000).”
From The effects of physical activity on cortisol and sleep: A systematic review and meta-analysis. (2022) · cites this paper as Van Cauter et al., 2000
A decrease in the amount of REM sleep occurs in synchrony with an elevation of evening cortisol levels.
“it was observed that a decrease in the amount of REM sleep (stable and unchanged until 50 years of age, decreased by approximately 50% in late life compared with young adulthood) occurred in synchrony with an elevation of evening cortisol levels.”
From Impact of Sleep and Its Disturbances on Hypothalamo-Pituitary-Adrenal Axis Activity (2010) · cites this paper as [49]
There is a trend for an association between lower amounts of REM sleep and higher evening cortisol concentrations, independently of age.
“A trend for an association between lower amounts of REM sleep and higher evening cortisol concentrations, independently of age, was also detected [49].”
From Impact of Sleep and Its Disturbances on Hypothalamo-Pituitary-Adrenal Axis Activity (2010) · cites this paper as [49]
Cites
Rechtschaffen, A. (1968) · Medical Entomology and Zoology · Cited by 11,772 · see citing works
Stress, adaptation, and disease. Allostasis and allostatic load
McEWEN, B. S. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09546.x · Cited by 5,092 · see citing works
McEwen, B. S., & Sapolsky, R. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80028-x · Cited by 1,889 · see citing works
Dijk, D., & Czeisler, C. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03526.1995 · Cited by 1,356 · see citing works
Vgontzas, A. N., Papanicolaou, D. A., Bixler, E. O., Hopper, K. D., Lotsikas, A. J., LIN, H., Kales, A., & Chrousos, G. P. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.3.6484 · Cited by 1,196 · see citing works
Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol
Van Cauter, E. (1996) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.7.2468 · Cited by 951 · see citing works
HO, K. Y., EVANS, W. S., BLIZZARD, R. M., VELDHUIS, J. D., MERRIAM, G. R., SAMOJLIK, E., FURLANETTO, R., ROGOL, A. D., KAISER, D. L., & THORNER, M. O. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-64-1-51 · Cited by 921 · see citing works
Human growth hormone and human aging
CORPAS, E., HARMAN, S. M., & BLACKMAN, M. R. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-1-20 · Cited by 911 · see citing works
Feast and Famine: Critical Role of Glucocorticoids with Insulin in Daily Energy Flow
Dallman, M. F., Strack, A. M., Akana, S. F., Bradbury, M. J., Hanson, E. S., Scribner, K. A., & Smith, M. (1993) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1993.1010 · Cited by 796 · cited 2× · see citing works
“Studies in both animals and humans have indicated that deleterious effects of HPA hyperactivity are more pronounced at the time of the trough of the rhythm than at the time of the peak.(25,54) Thus, modest elevations in evening cortisol levels could facilitate the development of central and peripheral disturbances ass…”
BackgroundSleep Loss Results in an Elevation of Cortisol Levels the Next Evening
(1997) · Sleep · doi:10.1093/sleep/20.10.865 · Cited by 745 · cited 1× · see citing works
“Furthermore, even partial sleep deprivation results in an elevation of cortisol levels the following evening.(21) Thus, both decreased SW sleep and sleep loss resulting from increased sleep fragmentation could contribute to elevating cortisol levels.”
BackgroundEEG sleep patterns as a function of normal and pathological aging in man
Feinberg, I., Koresko, R. L., & Heller, N. (1967) · Journal of Psychiatric Research · doi:10.1016/0022-3956(67)90027-1 · Cited by 457 · see citing works
Modulation of glucose regulation and insulin secretion by circadian rhythmicity and sleep
Van Cauter, E., Blackman, J. D., Roland, D., Spire, J. P., Refetoff, S., & Polonsky, K. S. (1991) · Journal of Clinical Investigation · doi:10.1172/jci115396 · Cited by 448 · see citing works
The 24-Hour Profile of Adrenocorticotropin and Cortisol in Major Depressive Illness*
Linkowski, P., MENDLEWICZ, J., Leclercq, R., Brasseur, M., Hubain, P., GOLSTEIN, J., Copinschi, G., & Cauter, E. V. (1985) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-61-3-429 · Cited by 404 · see citing works
The growth hormone deficiency syndrome in adults
Cuneo, R. C., Salomon, F., McGauley, G. A., & Sönksen, P. H. (1992) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1992.tb02347.x · Cited by 375 · see citing works
Landolt, H.-P., Dijk, D.-J., Achermann, P., & Borbély, A. A. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00770-6 · Cited by 350 · see citing works
Neuroendocrine rhythms and sleep in aging men
van Coevorden, A., Mockel, J., Laurent, E., Kerkhofs, M., L'Hermite-Baleriaux, M., Decoster, C., Neve, P., & Van Cauter, E. (1991) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1991.260.4.e651 · Cited by 336 · see citing works
Aging and Hypothalamic-Pituitary-Adrenal Response to Challenge in Humans*
Seeman, T. E., & Robbins, R. J. (1994) · Endocrine Reviews · doi:10.1210/edrv-15-2-233 · Cited by 335 · see citing works
Neuroendocrine Aspects of Primary Endogenous Depression
Rubín, R. T. (1987) · Archives of General Psychiatry · doi:10.1001/archpsyc.1987.01800160032006 · Cited by 287 · see citing works
Sleep and psychiatric disorders
Billiard, M. M., Partinen, M., Roth, T. G., & Shapiro, C. M. (1994) · Journal of Psychosomatic Research · doi:10.1016/0022-3999(94)90129-5 · Cited by 278 · see citing works
Cortisol Secretion Is Inhibited during Sleep in Normal Man*
WEITZMAN, E. D., ZIMMERMAN, J. C., CZEISLER, C. A., & RONDA, J. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-2-352 · Cited by 265 · see citing works
Holsboer, F., von Bardeleben, U., & Steiger, A. (2008) · Neuroendocrinology · doi:10.1159/000124986 · Cited by 255 · cited 1× · see citing works
“Indeed, elevated cortisol levels may promote awakenings.(55,56) Elevated evening cortisol levels in late life probably reflect an impairment of the negative feedback control of the HPA axis in aging.”
BackgroundInterrelations Between Sleep and the Somatotropic Axis
Cauter, E. V., Plat, L., & Copinschi, G. (1998) · SLEEP · doi:10.1093/sleep/21.6.553 · Cited by 243 · see citing works
Van Cauter, E., Plat, L., Scharf, M. B., Leproult, R., Cespedes, S., L'Hermite-Balériaux, M., & Copinschi, G. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119587 · Cited by 234 · see citing works
Sex Differences in the Sleep EEG of Young Adults: Visual Scoring and Spectral Analysis
Dijk, D., Beersma, D. G. M., & Bloem, G. M. (1989) · SLEEP · doi:10.1093/sleep/12.6.500 · Cited by 206 · see citing works
Reduced bone mineral content in adult patients with growth hormone deficiency
Rosén, T., HANSSON, T. H., Granhed, H., Szücs, J., & Bengtsson, B. (1993) · European Journal of Endocrinology · doi:10.1530/acta.0.1290201 · Cited by 203 · see citing works
Age and Gender Affect Different Characteristics of Slow Waves in the Sleep EEG
Mourtazaev, M. S., Kemp, B., Zwinderman, A. H., & KAMPHUISEN, H. A. C. (1995) · SLEEP · doi:10.1093/sleep/18.7.557 · Cited by 189 · see citing works
Estimating false-positive and false-negative errors in analyses of hormonal pulsatility
Cauter, E. V. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.254.6.e786 · Cited by 177 · see citing works
Jan Born, A., Späth‐Schwalbe, E., SCHWAKENHOFER, H., Kern, W., & Fehm, H. L. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-68-5-904 · Cited by 171 · see citing works
Slow‐wave sleep: do young adult men and women age differently?
Ehlers, C. L., & Kupfer, D. J. (1997) · Journal of Sleep Research · doi:10.1046/j.1365-2869.1997.00041.x · Cited by 167 · see citing works
Effects of age on delta and REM sleep parameters
Ehlers, C. L., & Kupfer, D. J. (1989) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(89)90172-7 · Cited by 163 · see citing works
Cooper, B. G., White, J., Ashworth, L., Alberti, K. G. M. M., & Gibson, G. J. (1995) · SLEEP · doi:10.1093/sleep/18.3.172 · Cited by 152 · see citing works
Gronfier, C., Luthringer, R., FOLLENIUS, M., Schaltenbrand, N., Macher, J. P., Muzet, A. G., & BRANDENBERGER, G. (1996) · SLEEP · doi:10.1093/sleep/19.10.817 · Cited by 142 · see citing works
Sleep in Older Persons: Sleep Structures of 50- to 60-year-old Men and Women
Webb, W. B. (1982) · Journal of Gerontology · doi:10.1093/geronj/37.5.581 · Cited by 116 · see citing works
Sleep and Sleep Disorders in Older Adults
Prinz, P. N. (1995) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-199503000-00004 · Cited by 115 · see citing works
Slow Wave Sleep Drives Inhibition of Pituitary‐AdrenalSecretion in Humans
Bierwolf, C., Struve, K., Marshall, L., Born, J., & Fehm, H. L. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.00605.x · Cited by 104 · see citing works
Processes Underlying Sleep Regulation
Borbély, A. A. (1998) · Hormone Research in Paediatrics · doi:10.1159/000023156 · Cited by 104 · see citing works
Continuous Positive Airway Pressure Treatment
Saini, J., Krieger, J., BRANDENBERGER, G., Wittersheim, G., Simon, C., & FOLLENIUS, M. (1993) · Hormone and Metabolic Research · doi:10.1055/s-2007-1002123 · Cited by 98 · see citing works
Spath-Schwalbe, E. (1993) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.77.5.1170 · Cited by 86 · see citing works
COPINSCHI, G., Leproult, R., Onderbergen, A. V., Caufriez, A., Cole, K. Y., Schilling, L. M., Mendel, C. M., Lepeleire, I. D., Bolognese, J. A., & Cauter, E. V. (2008) · Neuroendocrinology · doi:10.1159/000127249 · Cited by 85 · see citing works
Changes in Cortisol and Growth Hormone Secretion During Nocturnal Sleep in the Course of Aging
Kern, W., Dodt, C., Born, J., & Fehm, H. L. (1996) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/51a.1.m3 · Cited by 81 · see citing works
Rubín, R. T., Poland, R. E., Lesser, I. M., & Martin, D. J. (1989) · Biological Psychiatry · doi:10.1016/0006-3223(89)90142-x · Cited by 63 · see citing works
Copinschi, G., Onderbergen, A. V., L’Hermite‐Balériaux, M., Szyper, M., Caufriez, A., Bosson, D., L'Hermite, M., Robyn, C., Turek, F. W., & Cauter, E. V. (1990) · SLEEP · doi:10.1093/sleep/13.3.232 · Cited by 59 · see citing works
Gronfier, C., Luthringer, R., Follenius, M., Schaltenbrand, N., Macher, J. P., Muzet, A., & Brandenberger, G. (1997) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/s0013-4694(97)00013-1 · Cited by 50 · see citing works
Radioimmunoassay of human growth hormone using a charcoal-dextran separation procedure
Virasoro, E., Copinschi, G., Bruno, O. D., & Leclercq, R. (1971) · Clinica Chimica Acta · doi:10.1016/0009-8981(71)90392-5 · Cited by 44 · see citing works
Åström, C. (1995) · PubMed · Cited by 41 · see citing works
Effects of aging on glucose regulation during wakefulness and sleep
Frank, S. A., Roland, D. C., Sturis, J., Byrne, M. M., Refetoff, S., Polonsky, K. S., & Cauter, E. V. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.269.6.e1006 · Cited by 38 · see citing works
Genetic and environmental influences on prolactin secretion during wake and during sleep
Linkowski, P., Spiegel, K., Kerkhofs, M., L’Hermite‐Balériaux, M., Onderbergen, A. V., Leproult, R., Mendlewicz, J., & Cauter, E. V. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.274.5.e909 · Cited by 37 · see citing works
Diurnal Variations in Cardiovascular Function and Glucose Regulation in Normotensive Humans
Biston, P., Cauter, E. V., Ofek, G., Linkowski, P., Polonsky, K. S., & Degaute, J.-P. (1996) · Hypertension · doi:10.1161/01.hyp.28.5.863 · Cited by 34 · see citing works
Späth‐Schwalbe, E., Uthgenannt, D., Körting, N., Fehm, H., & Jan Born, A. (2008) · Neuroendocrinology · doi:10.1159/000126793 · Cited by 20 · see citing works
Jarrett, D. B., Pollock, B. G., Miewald, J. M., & Kupfer, D. J. (1991) · Biological Psychiatry · doi:10.1016/0006-3223(91)90206-2 · Cited by 16 · see citing works
Growth hormone assays: early to latest test generations compared
L’Hermite‐Balériaux, M., Copinschi, G., & Cauter, E. V. (1996) · Clinical Chemistry · doi:10.1093/clinchem/42.11.1789 · Cited by 13 · see citing works
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1 of the 52 references couldn’t be matched to a known paper.
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Adler, N. E., Epel, E. S., Castellazzo, G., & Ickovics, J. R. (2000) · Health Psychology · doi:10.1037/0278-6133.19.6.586 · Cited by 3,979 · see citing works
Ohayon, M. M., Carskadon, M. A., Guilleminault, C., & Vitiello, M. V. (2004) · Sleep · doi:10.1093/sleep/27.7.1255 · Cited by 3,349 · see citing works
A marker for the end of adolescence
Roenneberg, T., Kuehnle, T., Pramstaller, P. P., Ricken, J., Havel, M., Guth, A., & Merrow, M. (2004) · Current Biology · doi:10.1016/j.cub.2004.11.039 · Cited by 1,585 · see citing works
Epidemiology of the human circadian clock
Roenneberg, T., Kuehnle, T., Juda, M., Kantermann, T., Allebrandt, K., Gordijn, M., & Merrow, M. (2007) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2007.07.005 · Cited by 1,545 · see citing works
Mander, B. A., Winer, J. R., & Walker, M. P. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.004 · Cited by 1,214 · see citing works
Slow-wave sleep and the risk of type 2 diabetes in humans
Tasali, E., Leproult, R., Ehrmann, D. A., & Van Cauter, E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706446105 · Cited by 921 · see citing works
Metabolic consequences of sleep and sleep loss
Van Cauter, E., Spiegel, K., Tasali, E., & Leproult, R. (2008) · Sleep Medicine · doi:10.1016/s1389-9457(08)70013-3 · Cited by 812 · see citing works
Li, J., Vitiello, M. V., & Gooneratne, N. S. (2018) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2017.09.001 · Cited by 742 · see citing works
The effects of age, sex, ethnicity, and sleep-disordered breathing on sleep architecture
Redline, S., Kirchner, H. L., Quan, S. F., Gottlieb, D. J., Kapur, V., & Newman, A. (2004) · Archives of Internal Medicine · doi:10.1001/archinte.164.4.406 · Cited by 732 · see citing works
The aging clock: circadian rhythms and later life
Hood, S., & Amir, S. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90328 · Cited by 621 · see citing works
Stranges, S., Tigbe, W., Gómez-Olivé, F. X., Thorogood, M., & Kandala, N.-B. (2012) · Sleep · doi:10.5665/sleep.2012 · Cited by 592 · see citing works
Wang, C., & Holtzman, D. M. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0478-5 · Cited by 589 · see citing works
Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging
Mander, B. A., Rao, V. R., Lu, B. S., Saletin, J., Lindquist, J. R., Ancoli‐Israel, S., Jagust, W. J., & Walker, M. P. (2013) · Nature Neuroscience · doi:10.1038/nn.3324 · Cited by 565 · see citing works
β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation
Mander, B. A., Marks, S. M., Vogel, J. W., Rao, V. R., Lu, B. S., Saletin, J., Ancoli‐Israel, S., Jagust, W. J., & Walker, M. P. (2015) · Nature Neuroscience · doi:10.1038/nn.4035 · Cited by 546 · see citing works
The Functional and Clinical Significance of the 24-Hour Rhythm of Circulating Glucocorticoids
Oster, H., Challet, E., Ott, V., Arvat, E., de Kloet, E. R., Dijk, D.-J., Lightman, S., Vgontzas, A., & Van Cauter, E. (2017) · Endocrine Reviews · doi:10.1210/er.2015-1080 · Cited by 548 · see citing works
Epidemiology of obstructive sleep apnea: a population-based perspective
Lee, W. J., Nagubadi, S., Kryger, M. H., & Mokhlesi, B. (2008) · Expert Review of Respiratory Medicine · doi:10.1586/17476348.2.3.349 · Cited by 517 · see citing works
Beccuti, G., & Pannain, S. (2011) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e3283479109 · Cited by 507 · see citing works
Black, D. S., O’Reilly, G. A., Olmstead, R., Breen, E. C., & Irwin, M. R. (2015) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2014.8081 · Cited by 491 · see citing works
Peter‐Derex, L., Yammine, P., Bastuji, H., & Croisile, B. (2014) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2014.03.007 · Cited by 457 · see citing works
Daily nighttime melatonin reduces blood pressure in male patients with essential hypertension
Scheer, F. A. J. L., Van Montfrans, G. A., van Someren, E. J. W., Mairuhu, G., & Buijs, R. M. (2004) · Hypertension · doi:10.1161/01.hyp.0000113293.15186.3b · Cited by 451 · see citing works
Sleep Disorders in the Older Adult – A Mini-Review
Neikrug, A. B., & Ancoli‐Israel, S. (2009) · Gerontology · doi:10.1159/000236900 · Cited by 438 · see citing works
Psychological and metabolic stress: A recipe for accelerated cellular aging?
Epel, E. S. (2009) · HORMONES · doi:10.14310/horm.2002.1217 · Cited by 422 · see citing works
A meta-analysis of cortisol response to challenge in human aging: importance of gender
Otte, C., Hart, S. L., Neylan, T. C., Marmar, C. R., Yaffe, K. S., & Mohr, D. C. (2004) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.06.002 · Cited by 417 · see citing works
Vgontzas, A. N., & Chrousos, G. P. (2002) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(01)00005-6 · Cited by 414 · see citing works
Impact of Sleep and Its Disturbances on Hypothalamo-Pituitary-Adrenal Axis Activity
Balbo, M., Leproult, R., & Van Cauter, E. (2010) · International Journal of Endocrinology · doi:10.1155/2010/759234 · Cited by 408 · see citing works
“Most early studies investigating this topic, limited by small sample sizes and heterogeneous composition, seemed to indicate that there are no major sex and age differences in basal functioning of the HPA axis [27–29].”
BackgroundInvited Review: Integration of human sleep-wake regulation and circadian rhythmicity
Dijk, D., & Lockley, S. W. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00924.2001 · Cited by 394 · see citing works
Multilevel functional principal component analysis
Di, C., Crainiceanu, C. M., Caffo, B. S., & Punjabi, N. M. (2009) · The Annals of Applied Statistics · doi:10.1214/08-aoas206 · Cited by 376 · see citing works
Obstructive sleep apnea basics
Rundo, J. V. (2019) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.86.s1.02 · Cited by 381 · see citing works
Understanding sleep disturbance in athletes prior to important competitions
Juliff, L. E., Halson, S. L., & Peiffer, J. J. (2014) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2014.02.007 · Cited by 372 · see citing works
Reduced non–rapid eye movement sleep is associated with tau pathology in early Alzheimer’s disease
Lucey, B. P., McCullough, A. A., Landsness, E. C., Toedebusch, C. D., McLeland, J., Zaza, A., Fagan, A. M., McCue, L. M., Xiong, C., Morris, J. C., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aau6550 · Cited by 369 · see citing works
Risk factors for sleep disturbances in older adults: Evidence from prospective studies
Smagula, S. F., Stone, K. L., Fabio, A., & Cauley, J. A. (2015) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.01.003 · Cited by 342 · see citing works
Sleep benefits subsequent hippocampal functioning
Van Der Werf, Y. D., Altena, E., Schoonheim, M. M., Sanz-Arigita, E. J., Vis, J. C., De Rijke, W., & Van Someren, E. J. W. (2009) · Nature Neuroscience · doi:10.1038/nn.2253 · Cited by 313 · see citing works
Aging of the Immune System as a Prognostic Factor for Human Longevity
Larbi, A., Franceschi, C., Mazzatti, D. J., Solana, R., Wikby, A., & Pawelec, G. (2008) · Physiology · doi:10.1152/physiol.00040.2007 · Cited by 316 · see citing works
Concurrent Impairments in Sleep and Memory in Amnestic Mild Cognitive Impairment
Westerberg, C. E., Mander, B. A., Florczak, S. M., Weıntraub, S., Mesulam, M. M., Zee, P. C., & Paller, K. A. (2012) · Journal of the International Neuropsychological Society · doi:10.1017/s135561771200001x · Cited by 305 · see citing works
von Kries, R., Toschke, A. M., Wurmser, H., Sauerwald, T. U., & Koletzko, B. V. (2002) · International Journal of Obesity · doi:10.1038/sj.ijo.0801980 · Cited by 300 · see citing works
Karishma, K. K., & Herbert, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02099.x · Cited by 297 · see citing works
Sleep disturbances are correlated with decreased morning awakening salivary cortisol
Backhaus, J., Junghanns, K., & Hohagen, F. (2004) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.01.010 · Cited by 287 · see citing works
Insomnia Symptoms in Older Adults: Associated Factors and Gender Differences
Jaussent, I., Dauvilliers, Y., Ancelin, M.-L., Dartigues, J.-F., Tavernier, B., Touchon, J., Ritchie, K., & Besset, A. (2011) · The American Journal of Geriatric Psychiatry · doi:10.1097/jgp.0b013e3181e049b6 · Cited by 286 · see citing works
The effects of physical activity on cortisol and sleep: A systematic review and meta-analysis.
De Nys, L., Anderson, K., Ofosu, E. F., Ryde, G. C., Connelly, J., & Whittaker, A. C. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105843 · Cited by 279 · see citing works
Espiritu, J. R. D. (2007) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2007.08.007 · Cited by 276 · see citing works
Subjective and Objective Sleep Quality and Aging in the Sleep Heart Health Study
Unruh, M. L., Redline, S. S., An, M., Buysse, D. J., Nieto, F. J., Yeh, J.-L., & Newman, A. B. (2008) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2008.01755.x · Cited by 271 · see citing works
Age-Related Reduction in Daytime Sleep Propensity and Nocturnal Slow Wave Sleep
Dijk, D., Groeger, J. A., Stanley, N., & Deacon, S. (2010) · SLEEP · doi:10.1093/sleep/33.2.211 · Cited by 268 · see citing works
Slow-wave sleep: From the cell to the clinic
Léger, D., Debellemanière, E., Rabat, A., Bayon, V., Benchenane, K., & Chennaoui, M. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2018.01.008 · Cited by 261 · see citing works
Sleep, Anesthesiology, and the Neurobiology of Arousal State Control
Lydic, R., & Baghdoyan, H. A. (2005) · Anesthesiology · doi:10.1097/00000542-200512000-00024 · Cited by 251 · see citing works
Social relationships, sleep quality, and interleukin-6 in aging women
Friedman, E. M., Hayney, M. S., Love, G. D., Urry, H. L., Rosenkranz, M. A., Davidson, R. J., Singer, B. H., & Ryff, C. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509281102 · Cited by 247 · see citing works
Aging and Sleep: Physiology and Pathophysiology
Edwards, B. A., O’Driscoll, D. M., Ali, A., Jordan, A. S., Trinder, J. C., & Malhotra, A. (2010) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0030-1265902 · Cited by 247 · see citing works
Does inadequate sleep play a role in vulnerability to obesity?
Knutson, K. L. (2012) · American Journal of Human Biology · doi:10.1002/ajhb.22219 · Cited by 241 · see citing works
Timing and Consolidation of Human Sleep, Wakefulness, and Performance by a Symphony of Oscillators
Dijk, D., & von Schantz, M. (2005) · Journal of Biological Rhythms · doi:10.1177/0748730405278292 · Cited by 243 · see citing works
Vgontzas, A. N., Zoumakis, M., Bixler, E. O., Lin, H.-M., Prolo, P., Vela‐Bueno, A., Kales, A., & Chrousos, G. P. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021176 · Cited by 235 · see citing works
Spectral Analysis of the Sleep Electroencephalogram During Adolescence
(2004) · Sleep · doi:10.1093/sleep/27.4.774 · Cited by 231 · see citing works
The Bidirectional Relationship between Sleep and Immunity against Infections
Ibarra‐Coronado, E., Pantaleón-Martínez, A. M., Velázquez‐Moctezuma, J., Prospero-Garcia, O. E., Méndez‐Díaz, M., Pérez-Tapia, M., Pavón, L., & Morales‐Montor, J. (2015) · Journal of Immunology Research · doi:10.1155/2015/678164 · Cited by 228 · see citing works
Sleep Complaints in Community‐Living Older Persons: A Multifactorial Geriatric Syndrome
Fragoso, C. A. V., & Gill, T. M. (2007) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2007.01399.x · Cited by 224 · see citing works
Women's sleep in health and disease
Dzaja, A., Arber, S., Hislop, J., Kerkhofs, M., Kopp, C., Pollmächer, T., Polo‐Kantola, P., Skene, D. J., Stenuit, P., Tobler, I., et al. (2004) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2004.05.008 · Cited by 223 · see citing works
Sex Differences in the Association between Sleep and Body Mass Index in Adolescents
Knutson, K. L. (2005) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2005.07.019 · Cited by 223 · see citing works
Backhaus, J., Junghanns, K., Born, J., Hohaus, K., Faasch, F., & Hohagen, F. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.051 · Cited by 265 · see citing works
BRUXISM AND OROFACIAL MOVEMENTS DURING SLEEP
Kato, T., Thie, N. M. R., Montplaisir, J. Y., & Lavigne, G. J. (2001) · Dental Clinics of North America · doi:10.1016/s0011-8532(22)00487-6 · Cited by 215 · see citing works
Sleep and sleep disturbances: biological basis and clinical implications
Zisapel, N. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6529-9 · Cited by 216 · see citing works
The impact of sleep on age-related sarcopenia: Possible connections and clinical implications
Piovezan, R. D., Abucham, J., dos Santos, R. V. T., de Mello, M. T., Tufik, S., & Poyares, D. R. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.003 · Cited by 215 · see citing works
Sleep associated regulation of T helper 1/T helper 2 cytokine balance in humans
Dimitrov, S., Lange, T., Tieken, S., Fehm, H. L., & Born, J. (2004) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2003.08.004 · Cited by 209 · see citing works
Obesity and obstructive sleep apnea in children
Tauman, R., & Gozal, D. (2006) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2006.08.003 · Cited by 205 · see citing works
Sleep after Vaccination Boosts Immunological Memory
Lange, T., Dimitrov, S., Bollinger, T., Diekelmann, S., & Born, J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100015 · Cited by 201 · see citing works
Normal and abnormal sleep in the elderly
Cooke, J. R., & Ancoli‐Israel, S. (2010) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52006-7.00041-1 · Cited by 204 · see citing works
Someren, E. J. W. V. (2002) · Ageing Research Reviews · doi:10.1016/s1568-1637(02)00030-2 · Cited by 195 · see citing works
Sleep Quality and Body Mass Index in College Students: The Role of Sleep Disturbances
Vargas, P. A., Flores, M. A., & Robles, E. (2014) · Journal of American College Health · doi:10.1080/07448481.2014.933344 · Cited by 191 · see citing works
Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep
Backhaus, J., Born, J., Hoeckesfeld, R., Fokuhl, S., Hohagen, F., & Junghanns, K. (2007) · Learning & Memory · doi:10.1101/lm.470507 · Cited by 187 · see citing works
Chung, F. F., Liao, P., Yegneswaran, B., Shapiro, C. M., & Kang, W. (2013) · Anesthesiology · doi:10.1097/aln.0000000000000040 · Cited by 187 · see citing works
Form and function of sleep spindles across the lifespan
Clawson, B. C., Durkin, J., & Aton, S. J. (2016) · Neural Plasticity · doi:10.1155/2016/6936381 · Cited by 178 · see citing works
Raison, C. L., Borisov, A. S., Woolwine, B. J., Massung, B., Vogt, G., & Miller, A. H. (2010) · Molecular Psychiatry · doi:10.1038/mp.2008.58 · Cited by 183 · see citing works
Sleep, dreams, and memory consolidation: the role of the stress hormone cortisol
Payne, J. D., & Nadel, L. (2004) · Learning & Memory · doi:10.1101/lm.77104 · Cited by 184 · see citing works
Higher levels and blunted diurnal variation of cortisol in frail older women
Varadhan, R., Walston, J., Cappola, A. R., Carlson, M. C., Wand, G. S., & Fried, L. P. (2008) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/63.2.190 · Cited by 182 · see citing works
Scullin, M. K. (2013) · Psychology and Aging · doi:10.1037/a0028830 · Cited by 181 · see citing works
Zeng, Y., Guo, Z., Wu, M., Chen, F., & Chen, L. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-01960-1 · Cited by 184 · see citing works
Gonnissen, H. K. J., Hursel, R., Rutters, F., Martens, E. A. P., & Westerterp-Plantenga, M. S. (2013) · British Journal of Nutrition · doi:10.1017/s0007114512001894 · Cited by 170 · see citing works
Backhaus, J., Hoeckesfeld, R., Born, J., Hohagen, F., & Junghanns, K. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.010 · Cited by 168 · see citing works
Leproult, R., Van Onderbergen, A., L’Hermite‐Balériaux, M., Van Cauter, E., & Copinschi, G. (2005) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2005.02341.x · Cited by 167 · see citing works
Factors underlying cognitive decline in old age and Alzheimer’s disease: the role of the hippocampus
Jaroudi, W., Garami, J. K., Garrido, S., Hornberger, M., Kéri, S., & Moustafa, A. A. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2016-0086 · Cited by 166 · see citing works
Treating insomnia: Current and investigational pharmacological approaches
Ebert, B., Wafford, K. A., & Deacon, S. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.04.014 · Cited by 166 · see citing works
Obál, F., & Krueger, J. M. (2004) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2004.03.005 · Cited by 166 · see citing works
Age-Related Increase in Awakenings: Impaired Consolidation of NonREM Sleep at All Circadian Phases
Dijk, D., Duffy, J. F., & Czeisler, C. A. (2001) · SLEEP · doi:10.1093/sleep/24.5.565 · Cited by 159 · see citing works
Bedside‐to‐Bench Conference: Research Agenda for Idiopathic Fatigue and Aging
Alexander, N. B., Taffet, G. E., Horne, F. M., Eldadah, B. A., Ferrucci, L., Nayfield, S., & Studenski, S. A. (2010) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2010.02811.x · Cited by 153 · see citing works
Lorton, D., Lubahn, C. L., Estus, C., Millar, B. A., Carter, J. L., Wood, C. A., & Bellinger, D. L. (2006) · NeuroImmunoModulation · doi:10.1159/000104864 · Cited by 147 · see citing works
Illuminating the Effects of Dynamic Lighting on Student Learning
Mott, M. S., Robinson, D. H., Walden, A., Burnette, J. L., & Rutherford, A. S. (2012) · SAGE Open · doi:10.1177/2158244012445585 · Cited by 145 · see citing works
Lananna, B. V., & Musiek, E. S. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104832 · Cited by 145 · see citing works
Parcell, D. L., Ponsford, J. L., Redman, J. R., & Rajaratnam, S. M. W. (2008) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2007.09.057 · Cited by 142 · see citing works
Physiological Features of Aging Persons
Aalami, O. (2003) · Archives of Surgery · doi:10.1001/archsurg.138.10.1068 · Cited by 143 · see citing works
Blackman, J., Swirski, M., Clynes, J., Harding, S., Leng, Y., & Coulthard, E. (2021) · Journal of Sleep Research · doi:10.1111/jsr.13229 · Cited by 141 · see citing works
Sleep Disorders in the Elderly
Yaremchuk, K. (2018) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2018.01.008 · Cited by 141 · see citing works
Defining osteoblast and adipocyte lineages in the bone marrow
Pierce, J. L., Begun, D. L., Westendorf, J. J., & McGee‐Lawrence, M. E. (2018) · Bone · doi:10.1016/j.bone.2018.05.019 · Cited by 134 · see citing works
Melatonin in Patients with Reduced REM Sleep Duration: Two Randomized Controlled Trials
Kunz, D., Mahlberg, R., Müller, C., Tilmann, A., & Bes, F. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021057 · Cited by 133 · see citing works
Leineweber, C., Kecklund, G., Janszky, I., Åkerstedt, T., & Orth‐Gomér, K. (2003) · Journal of Psychosomatic Research · doi:10.1016/s0022-3999(02)00475-0 · Cited by 131 · see citing works
Psychosocial and endocrine features of chronic first-episode major depression in 8–16 year olds
Goodyer, I. M., Park, R. J., & Herbert, J. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01120-9 · Cited by 130 · see citing works
Daytime naps improve procedural motor memory
Backhaus, J., & Junghanns, K. (2006) · Sleep Medicine · doi:10.1016/j.sleep.2006.04.002 · Cited by 128 · see citing works
Sleep Habits and Insomnia in a Sample of Elderly Persons in China
Liu, X., & Liu, L. (2005) · SLEEP · doi:10.1093/sleep/28.12.1579 · Cited by 128 · see citing works
Molecular Endocrinology and Physiology of the Aging Central Nervous System
Smith, R. G., Betancourt, L., & Sun, Y. (2005) · Endocrine Reviews · doi:10.1210/er.2002-0017 · Cited by 127 · see citing works
Steinmeyer, C., Schielzeth, H., Mueller, J. C., & Kempenaers, B. (2010) · Animal Behaviour · doi:10.1016/j.anbehav.2010.08.005 · Cited by 123 · see citing works
Happy as a lark: Morning-type younger and older adults are higher in positive affect.
Biss, R. K., & Hasher, L. (2012) · Emotion · doi:10.1037/a0027071 · Cited by 122 · see citing works
Caufriez, A., Leproult, R., L’Hermite‐Balériaux, M., Kerkhofs, M., & Copinschi, G. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2558 · Cited by 122 · see citing works
Slow Wave Sleep Is a Promising Intervention Target for Alzheimer’s Disease
Lee, Y. F., Gerashchenko, D., Timofeev, I., Bacskai, B. J., & Kastanenka, K. V. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00705 · Cited by 119 · see citing works
Benedict, C., Brytting, M., Markström, A., Broman, J.-E., & Schiöth, H. B. (2012) · BMC Immunology · doi:10.1186/1471-2172-13-1 · Cited by 119 · see citing works
Sleep disorders and their impacts on healthy, dependent, and frail older adults
Cock, V. C. D., Arbus, C., Soto, M., Villars, H., Tiberge, M., Montemayor, T., Hein, C., Veccherini, M. F., Onen, S. ‐., Ghorayeb, I., et al. (2009) · The journal of nutrition health & aging · doi:10.1007/s12603-009-0030-0 · Cited by 117 · see citing works
- Authors
- Van Cauter, E.
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2000-08-16
- Volume
- 284
- Issue
- 7
- Pages
- 861
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- OpenAlex
- W2035490031
- Semantic Scholar
- 7e085c801202adf0cc333fa840264be285802ae2
- Cited by
- 773
- References
- 52
- Citations by year
- 2026: 25 · 2025: 31 · 2024: 35 · 2023: 28 · 2022: 28 · 2021: 51 · 2020: 40 · 2019: 35 · 2018: 36 · 2017: 22 · 2016: 35 · 2015: 33 · 2014: 31 · 2013: 33 · 2012: 38
- FWCI
- 10.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- Funders
- National Institute on Aging (P01AG011412, AG-11412)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-41814, R01DK041814)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- age-related sleep changes, slow-wave sleep, REM sleep, growth hormone secretion, cortisol, sleep stages, sleep fragmentation, aging, men, sleep quality, circadian rhythm, NREM sleep, healthy men, polygraphic sleep recording, plasma hormone levels
- MeSH terms
- Adolescent, Adult, Age Factors, Aged, Aged, 80 and over, Aging, Analysis of Variance, Humans, Hydrocortisone, Male, Middle Aged, Sleep, Sleep, REM, Body Mass Index, Polysomnography, Human Growth Hormone
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