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Adolescent Changes in the Homeostatic and Circadian Regulation of Sleep
Open accessAbstract
Sleep deprivation among adolescents is epidemic. We argue that this sleep deprivation is due in part to pubertal changes in the homeostatic and circadian regulation of sleep. These changes promote a delayed sleep phase that is exacerbated by evening light exposure and incompatible with aspects of modern society, notably early school start times. In this review of human and animal literature, we demonstrate that delayed sleep phase during puberty is likely a common phenomenon in mammals, not specific to human adolescents, and we provide insight into the mechanisms underlying this phenomenon.
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“For pubertal mice, this tendency was exaggerated, with the animals being clearly more sensitive to evening light than adults [70, 198].”
From The neuroendocrine control of the circadian system: Adolescent chronotype (2012) · cites this paper as [70]
In the citing paper
“Reduced sensitivity to the homeostatic sleep drive that builds during extended wakefulness may also contribute to later bedtimes in adolescents (Hagenauer, Perryman, Lee, & Carskadon, 2009).”
From Sleep and circadian contributions to adolescent alcohol use disorder (2015) · cites this paper as Hagenauer et al., 2009
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Bioactive Compounds from and against Yeasts in the One Health Context: A Comprehensive Review
Tadioto, V., Giehl, A., Cadamuro, R. D., Guterres, I. Z., dos Santos, Â. A., Bressan, S. K., Werlang, L., Stambuk, B. U., Fongaro, G., Silva, I. T., et al. (2023) · Fermentation · doi:10.3390/fermentation9040363 · Cited by 22
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“More complex interactions between internal and external factors may also play a role, for example, changes in sensitivity of the internal pacemaker to light has been suggested as a possible mechanism for the phase delay in adolescence.(55) In conjunction with the chronobiological and pubertal maturation perspectives,…”
Hayes, B., & Bainton, J. (2020) · School Psychology International · doi:10.1177/0143034320961130 · Cited by 24
“These include differences in their circadian regulation and sleep phase, resulting in differences in the times of day and night that they feel sleepy and wakeful (Colrain & Baker, 2011; Hagenauer et al., 2009; Kelley et al., 2015; Short & Chee 2019; Skeldon et al., 2016).”
BackgroundGender moderates the relationship between media use and sleep quality
McManus, B., Underhill, A. T., Mrug, S., Anthony, T., & Stavrinos, D. (2020) · Journal of Sleep Research · doi:10.1111/jsr.13243 · Cited by 25
“Although the pubertal onset and associated circadian phase delay begin earlier in females (Roenneberg et al., 2004), peak delay occurs between the ages of 15 to 21 years for both males and females (Hagenauer et al., 2009).”
BackgroundToufexis, D. J., & Wilson, M. E. (2011) · Brain Research · doi:10.1016/j.brainres.2011.10.024 · Cited by 20
“Although, It has been shown that androgens are important at puberty for calibrating the regulation of circadian cycles related to changes in activity level in male rodents, and in adolescent boys (Hagenauer et al.; Hagenauer et al., 2009), and that the diurnal rhythm of CORT is absent following long-term castration in…”
Saidi, O., Rochette, E., Bovet, M., Merlin, É., & Duché, P. (2020) · Pediatric Obesity · doi:10.1111/ijpo.12613 · Cited by 20
“This was explained in part by a reduced and delayed peak of melatonin from the onset of puberty.(5) However, teenagers still require 9 to 10 hours of sleep per day,(6) and sleep remains fundamental for several physiological processes such as homeostatic regulation, recovery, and energy conservation, especially”
BackgroundTroxel, W., Rodriguez, A., Seelam, R., Dong, L., Perez, L. G., Tucker, J. S., Siconolfi, D. E., & D’Amico, E. J. (2022) · Addictive Behaviors · doi:10.1016/j.addbeh.2022.107417 · Cited by 21
Borisenkov, M. F., Popov, S. V., Смирнов, В. В., Dorogina, O. I., Pecherkina, A. A., & Symaniuk, E. E. (2022) · Chronobiology International · doi:10.1080/07420528.2022.2117050 · Cited by 19
“One of the possible reasons for the low effectiveness of these methods is that, according to several studies, the delay in the phase of the sleepwake rhythm in adolescents is mainly determined by the increase in the period of the endogenous rhythm (Carskadon et al. 1999; Hagenauer et al. 2009).”
BackgroundSleep behavior across the lifespan: How a model can expand our current understanding
Crowley, S. J. (2015) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.12.003 · Cited by 19
“Previous studies in adolescent humans [38,39] and in other young mammals [40] found a puberty-related delay of the circadian timing system.”
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Evidence Base Update on Assessing Sleep in Youth
Meter, A. V., & Anderson, E. A. (2020) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2020.1802735 · Cited by 21
Sleep and slow-wave activity in depressed adolescent boys: a preliminary study
Santangeli, O., Porkka‐Heiskanen, T., Virkkala, J., Castaneda, A. E., MARTTUNEN, M. J., Paunio, T., & Urrila, A. S. (2017) · Sleep Medicine · doi:10.1016/j.sleep.2017.06.029 · Cited by 20
“The changes in sleep occur during adolescence go hand in hand with major maturation of the psychosocial and physical processes, including a massive reorganization of the brain neuronal networks (synaptic pruning) [27].”
BackgroundLei, Y., Wang, D., Bai, Y., Nougaisse, J., Weintraub, N. L., Guo, M., & Lu, X. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01778-2 · Cited by 20
“In C57BL/6 mice, pubertal onset starts at P28 in female mice and P30 in male mice [70, 73, 74].”
BackgroundVandendriessche, A., Verloigne, M., Boets, L., Joriskes, J., DeSmet, A., Dhondt, K., & Deforche, B. I. (2022) · BMC Public Health · doi:10.1186/s12889-022-14278-3 · Cited by 18
“From a physiological perspective, adolescents often experience a delayed sleep phase due to hormonal fluctuations and a changed circadian rhythm which is associated with a significant decrease in melatonin production [33].”
BackgroundDíaz‐Morales, J. F., Escribano, C., Puig‐Navarro, Y., & Jankowski, K. S. (2022) · Journal of Youth and Adolescence · doi:10.1007/s10964-022-01708-z · Cited by 19
“Hagenauer et al. (2009) concluded that biological factors can account for the shift towards eveningness during adolescence given that (1) bedtime delay was observed earlier in girls than in boys coinciding with their earlier pubertal development, (2) the shift towards eveningness has been observed…”
Background(2012) · Frontiers research topics · doi:10.3389/978-2-88919-025-6 · Cited by 18
Koterov, A. N., Ushenkova, L. N., Зубенкова, Э., Vainson, A. A., Vaynson, A., Бирюков, А. П., & Biryukov, A. P. (2018) · Medical Radiology and radiation safety · doi:10.12737/article_5a82e4a3908213.56647014 · Cited by 21
Epidemiology of Bedtime, Arising Time, and Time in Bed: Analysis of Age, Gender, and Ethnicity
Thomas, S. J., Lichstein, K. L., Taylor, D. J., Riedel, B. W., & Bush, A. J. (2013) · Behavioral Sleep Medicine · doi:10.1080/15402002.2013.778202 · Cited by 18
“In general, these data reflect a delayed sleep phase for young adults as compared to older adults, which were consistent with circadian and behavioral research (Hagenauer et al., 2009).”
ResultHamilton, J. L., Ladouceur, C. D., Silk, J. S., Franzen, P. L., & Bylsma, L. M. (2019) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsz079 · Cited by 18
“Increased psychosocial demands, such as academic pressure, extracurricular activities, and latenight socializing, all combine to push sleep toward both biological and behaviorally induced later bedtimes and sleep midpoints (Carskadon, 2011; Hagenauer et al., 2009; Wong, Hasler, Kamarck, Muldoon, & Manuck, 2015).”
BackgroundSantos, J. S., Pereira, S. I. R., & Louzada, F. M. (2021) · Sleep Medicine · doi:10.1016/j.sleep.2021.04.016 · Cited by 18
Effect of Two Interventions on Sleep Quality for Adolescent and Young Adult Cancer Survivors
Li, L., Wang, L., Sun, Q., Xiao, P., Duan, Y., Liu, X., Zhou, J., Xie, J., & Cheng, A. S. K. (2021) · Cancer Nursing · doi:10.1097/ncc.0000000000000932 · Cited by 16
“More than 45% of AYA cancer patients suffer from sleep deprivation in part because of changes in the circadian rhythm regulation of sleep during puberty, which can delay the sleep phase.(11,12) Additionally, AYA cancer patients experience a variety of disease or treatment symptoms(13) and may experience psychological…”
BackgroundSleep and Adolescent Depression
Fontanellaz-Castiglione, C. E. G., & Tarokh, L. (2023) · Clinical and Translational Neuroscience · doi:10.3390/ctn8010003 · Cited by 22
Papaconstantinou, E. A., Shearer, H. M., Fynn-Sackey, N., Smith, K., Taylor-Vaisey, A. L., & Côté, P. (2018) · International Journal of Mental Health and Addiction · doi:10.1007/s11469-018-0006-6 · Cited by 19
Putilov, A. A., & Verevkin, E. G. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01529 · Cited by 20
“…the hypothalamus and its major function is to entrain the circadian period and to reset the circadian phase of all other structures and processes of an organism in response to changes in the environmental 24-h light–dark cycle (Moore and Eichler, 1972; Ibuka and Kawamura, 1975; Ralph et al., 1990).”
BackgroundSleep Timing During Adolescence: A Latent Transition Analysis Approach
Magee, C., & Blunden, S. (2018) · Behavioural Sleep Medicine · doi:10.1080/15402002.2018.1546180 · Cited by 16
“These changes underpin the shift toward later sleep timing and a growing evening chronotype preference (Crowley et al., 2018; Hagenauer et al., 2009).”
BackgroundHajali, V., Sheibani, V., Esmaeili‐Mahani, S., Hajializadeh, Z., Shabani, M., Pasban-Aliabadi, H., Saadati, H., & Esmaeilpour, K. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.03.010 · Cited by 17
“Both subjective and objective sleepdisturbances inwomen associatewith remarkable changes in the gonadal hormone profile such as at adolescence, pregnancy or menopause [21,22].”
The Relationship Between Estrogen and the Decline in Delta Power During Adolescence
McHill, A. W., Klerman, E. B., Slater, B., Kangarloo, T., Mankowski, P. W., & Shaw, N. D. (2017) · SLEEP · doi:10.1093/sleep/zsx008 · Cited by 17
A Comparative Study of Sleep and Mood Between Young Elite Athletes and Age-Matched Controls
Harris, A., Gundersen, H. S., Andreassen, P. M., Thun, E., Bjorvatn, B., & Pallesen, S. (2017) · Journal of Physical Activity and Health · doi:10.1123/jpah.2016-0513 · Cited by 17
Napping Behavior in Adolescents: Consensus, Dissents, and Recommendations
Santos, J. S., Beijamini, F., & Louzada, F. M. (2021) · Sleep and Vigilance · doi:10.1007/s41782-021-00155-3 · Cited by 16
Vollmer, C., Hammer, J., Keller, C., Maxand, A. K., Díaz‐Morales, J. F., & Randler, C. (2014) · International Journal Of Biology Education · doi:10.20876/ijobed.66052 · Cited by 16
“With the onset of puberty, physiological and psychological changes delay sleep timing, also known as chronotype (Carskadon 1990, Crowley et al., 2007, Hagenauer et al., 2009, Randler et al., 2009).”
Sleep in child and adolescent psychiatry: overlooked and underappreciated
Tarokh, L., Hamann, C., & SCHIMMELMANN, B. G. (2014) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-014-0554-7 · Cited by 15
Differential Sensitivity to Ethanol‐Induced Circadian Rhythm Disruption in Adolescent and Adult Mice
Ruby, C. L., Palmer, K. N., Zhang, J., Risinger, M. O., Butkowski, M. A., & Swartzwelder, H. S. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13275 · Cited by 16
“In humans, circadian activity and sleep patterns change throughout life and are generally delayed during adolescence (Hagenauer et al., 2009).”
InfluentialEffects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
Hehr, A., Marusak, H. A., Huntley, E. D., & Rabinak, C. A. (2019) · Chronic Stress · doi:10.1177/2470547019856332 · Cited by 17
Gasperetti, C. E., Dolsen, E. A., & Harvey, A. G. (2020) · Sleep Medicine · doi:10.1016/j.sleep.2020.11.014 · Cited by 16
“The onset and progression of puberty is associated with a shift towards an evening circadian preference, characterized by a desire to go to bed later and wake later (Gradisar et al., 2011; Hagenauer et al., 2009).”
BackgroundEvanger, L. N., Bjorvatn, B., Pallesen, S., Hysing, M., Sivertsen, B., & Saxvig, I. W. (2023) · Journal of Sleep Research · doi:10.1111/jsr.13840 · Cited by 18
“This delay in circadian timing appears to be biologically based, possibly underpinned by a elongation of the endogenous circadian period and/or altered light sensitivity that may shift the circadian phase (Crowley et al., 2007; Hagenauer et al., 2009; Hummer & Lee, 2016).”
BackgroundAre achievement goals different among morning and evening-type adolescents?
Escribano, C., & Díaz‐Morales, J. F. (2015) · Personality and Individual Differences · doi:10.1016/j.paid.2015.08.032 · Cited by 16
Noorwali, E. A., Hardie, L. J., & Cade, J. E. (2018) · Sleep Science and Practice · doi:10.1186/s41606-018-0032-0 · Cited by 17
The teen sleep loss epidemic: what can be done?
Bryant, N. B., & Gómez, R. L. (2015) · Translational Issues in Psychological Science · doi:10.1037/tps0000020 · Cited by 15
“Hale and Guan (2014) reported that 90% of studies published on the topic of technology use in 5- to 17-year-olds noted disrupted sleep, with shortened sleep and later bedtimes showing the most consistent effects.”
BackgroundFry, C. M. (2021) · Journal of Children and Media · doi:10.1080/17482798.2020.1858907 · Cited by 15
Lambert, L., Joshanloo, M., Marquez, J., Cody, B. L., Arora, T., Warren, M. A., Aguilar, L., Samways, M., & Teasel, S. (2022) · International Journal of Applied Positive Psychology · doi:10.1007/s41042-022-00066-2 · Cited by 14
“Adolescents commonly experience delayed circadian rhythmicity resulting in a preference for eveningness (Hagenauer et al., 2009; Hummer & Lee, 2016); consequently, later sleep timings are common in this age group.”
BackgroundBarley, B. K., Gao, C., Luster, T. G., Porro, A., Parizi‐Robinson, M., Quigley, D., Zinke, P., & Scullin, M. K. (2023) · Chronobiology International · doi:10.1080/07420528.2023.2203251 · Cited by 19
“…timing is sometimes viewed as “fixed,” there is also evidence that it can change over time, such as the phase-delays that occur across adolescence and the phase-advances that occur in older adulthood (e.g., Didikoglu et al. 2019; Hagenauer et al. 2009; Roenneberg et al. 2007; Scullin 2017).”
BackgroundA Pilot Study on Adolescents With Depression and Insomnia: Qualitative Findings From Focus Groups
Conroy, D. A., Czopp, A., Dore‐Stites, D., Dopp, R. R., Armitage, R., Hoban, T. F., & Arnedt, J. T. (2015) · Behavioral Sleep Medicine · doi:10.1080/15402002.2015.1065412 · Cited by 18
Shochat, T., Barker, D., Sharkey, K. M., Reen, E. V., Roane, B. M., & Carskadon, M. A. (2017) · Journal of Sleep Research · doi:10.1111/jsr.12550 · Cited by 15
“…to maintain early sleep schedules, which often conflict with their developmental tendency towards later bedtimes (Carskadon et al., 1998; Hagenauer et al., 2009; Short et al., 2013), resulting in shorter sleep duration during the school week and delayed sleep timing and longer sleep…”
InfluentialHaynes, P. L., Silva, G. E., Howe, G. W., Thomson, C. A., Butler, E. A., Quan, S. F., Sherrill, D. L., Scanlon, M. M., Rojo‐Wissar, D. M., Gengler, D. N., et al. (2017) · BMC Public Health · doi:10.1186/s12889-017-4818-2 · Cited by 14
“All participants are between the ages of 25-60 years, as age above or below this range may have substantial impact on sleep [48, 49] and social rhythms [50].”
BackgroundWhy sleep matters in chronic pain: evidence across the lifespan
Kelleher, E. M., Wall, A. J. W., Seymour, B., & Irani, A. (2026) · EBioMedicine · doi:10.1016/j.ebiom.2026.106158 · Cited by 18
“74 Against this backdrop of biological sleep disruption, chronic pain prevalence also rises, affecting 20–25% of teens.”
Wolf‐Meyer, M. (2014) · Science as Culture · doi:10.1080/09505431.2014.945411 · Cited by 14
Schlecht, S. H., Martin, C. T., Ochocki, D. N., Nolan, B. T., Wojtys, E. M., & Ashton‐Miller, J. A. (2019) · Journal of Orthopaedic Research® · doi:10.1002/jor.24328 · Cited by 14
Gasperetti, C. E., Dong, L., & Harvey, A. G. (2021) · Sleep Health · doi:10.1016/j.sleh.2021.10.007 · Cited by 14
Sleep Quality’s Effect on Vigilance and Perceptual Ability in Adolescent and Adult Athletes
Stavrou, V. T., Astara, K., Tourlakopoulos, K. N., Daniil, Z. D., Gourgoulianis, K. I., Kalabakas, K., Karagiannis, D., & Βasdekis, G. (2021) · Journal of Sports Medicine · doi:10.1155/2021/5585573 · Cited by 14
“Due to this social misconception, adolescents are faced with delayed sleep phase, worsening their quality and quantity [38].”
Backgroundde Melo, P. R., Gonçalves, B. S. B., Menezes, A. A. L., & de Azevedo, C. V. M. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.12.023 · Cited by 15
Circadian Rhythms, Sleep, and the Autonomic Nervous System
Garbarino, S., Lanteri, P., Feeling, N. R., Jarczok, M. N., Quintana, D. S., Koenig, J., & Sannita, W. G. (2019) · Journal of Psychophysiology · doi:10.1027/0269-8803/a000236 · Cited by 15
The diagnosis and management of common sleep disorders in adolescents
Reiter, J. M., & Rosen, D. (2014) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000113 · Cited by 14
“When DSPS is present, treatment includes improving sleep hygiene with special attention to minimizing bright light exposure during the last few hours of the evening (including that from computer and television screens), and maximizing bright light exposure in the morning, through either outdoor activities or exposure…”
BackgroundThe effects of sleep and light at night on melatonin in adolescents
Hersh, C., Sisti, J., Richiutti, V., & Schernhammer, E. (2015) · Hormones · doi:10.14310/horm.2002.1573 · Cited by 13
Impact of Sex on Sleep Disorders Across the Lifespan
Tobias, L. A., Thapa, S., & Won, C. H. J. (2021) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2021.04.005 · Cited by 15
Involvement in bullying and sleep disorders in Chinese early adolescents
Ding, H., Cao, L., Xu, B., Li, Y., Xie, J., Wang, J., Su, P., & Wang, G. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1115561 · Cited by 13
“Early adolescence (10–14 years) is a key development stage, involving crucial neurobiological, hormonal, and sociocontextual changes that influence sleep–wake regulation (28, 29).”
BackgroundKim, S., & Casement, M. D. (2024) · Chronobiology International · doi:10.1080/07420528.2024.2341156 · Cited by 14
“Research incorporating self-reported sleep patterns and biological markers, such as salivary melatonin levels, has demonstrated that puberty is associated with a delayed circadian phase (Hagenauer et al. 2009; Roenneberg et al. 2004).”
BackgroundMethodSleep and Neuroaffective Development from Early to Late Adolescence
Baker, A. E., & McMakin, D. L. (2024) · Annual Review of Developmental Psychology · doi:10.1146/annurev-devpsych-010923-093914 · Cited by 13
SLEEP-WAKE RHYTHMS AND COGNITION
Maire, M., Reichert, C., & Schmidt, C. (2013) · ORBi (University of Liège) · Cited by 13
Change in Individual Chronotype Over a Lifetime: A Retrospective Study
Lee, J. H., Kim, I. S., Kim, S. J., Wang, W., & Duffy, J. F. (2011) · Sleep Medicine Research · doi:10.17241/smr.2011.2.2.48 · Cited by 12
Morningness–eveningness and sleep habits at school: a comparative study between Mexico and Spain
Arrona‐Palacios, A., & Díaz‐Morales, J. F. (2016) · Biological Rhythm Research · doi:10.1080/09291016.2016.1245459 · Cited by 13
“During puberty, a preference for evening hours appears, consequence of the maturation processes typical of puberty (Hagenauer et al. 2009) and also moderated by the many changes in the adolescent’s relational and social spheres, such as school demands, new social opportunities, and diminution of…”
BackgroundTime for testosterone: the suprachiasmatic nucleus gets sexy
Hagenauer, M. H., & Lee, T. M. (2011) · Endocrinology · doi:10.1210/en.2011-0198 · Cited by 12
Albert, N., da Silva, C. A., Dı́ez-Noguera, A., & Cambras, T. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.06.025 · Cited by 12
Consequences of adolescent's evening preference on psychological functioning: a review
Díaz‐Morales, J. F., & Escribano, C. (2014) · Library Open Repository (Universidad Complutense Madrid) · Cited by 12
Sleeping Beauty? Developmental Timing, Sleep, and the Circadian Clock in Caenorhabditis elegans
Olmedo, M., Merrow, M. W., & Geibel, M. (2017) · Advances in genetics · doi:10.1016/bs.adgen.2017.05.001 · Cited by 12
Putilov, A. A. (2022) · Sleep And Breathing · doi:10.1007/s11325-022-02648-5 · Cited by 12
van der Laan, S. E. I., Lenters, V. C., Finkenauer, C., van Harmelen, A., van der Ent, C. K., & Nijhof, S. L. (2022) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2022.06.006 · Cited by 12
Díaz‐Morales, J. F., & Escribano, C. (2014) · Anales de Psicología · doi:10.6018/analesps.30.3.167941 · Cited by 23
Sleep Patterns of Middle & High School Students in Seoul and Their Perceptions of Their Own Sleep
Kim, J. H., Moon, H.-S., & Lee, H. W. (2014) · Journal of Korean Sleep Research Society · doi:10.13078/jksrs.14005 · Cited by 12
“사춘 기와 함께 일주기 리듬이 지연되는 생물학적인 요인으로 인 해 자연스럽게 어렸을 때에 비해 고학년이 되면서 더 늦게 자 고 늦게 일어나는 경향을 가지게 된다.(1-4) 또한, 학년이 올라 가면서 등교 시간의 변화, 학업 등을 포함한 사회적인 요인으 로 인하여 수면과 각성 주기의 변화를 더욱 심화시켜 수면 위 상의 지연과 함께 수면 부족을 유발하게 된다.”
InfluentialRelevance of Sleep and Circadian Rhythms to Adolescent Substance Use
Claudatos, S. A., Baker, F. C., & Hasler, B. P. (2019) · Current Addiction Reports · doi:10.1007/s40429-019-00277-9 · Cited by 14
Adolescent alcohol exposure increases orexin-A/hypocretin-1 in the anterior hypothalamus
Amodeo, L. R., Liu, W., Wills, D. N., Vetreno, R. P., Crews, F. T., & Ehlers, C. L. (2020) · Alcohol · doi:10.1016/j.alcohol.2020.06.003 · Cited by 11
“Recent findings have confirmed that adolescents and young adults with drug and alcohol problems also have sleep difficulties (Bartel, Gradisar, & Williamson, 2015; Cohen-Zion et al., 2009; Criado & Ehlers, 2010; Ehlers, Gilder, Criado, & Caetano, 2010; Ehlers, Wills, & Gilder, 2018; Hagenauer et al., 2009; Meltzer & M…”
BackgroundGarbers, S., Suruki, C., Falletta, K. A., Gold, M. A., & Bruzzese, J. (2021) · Complementary Therapies in Medicine · doi:10.1016/j.ctim.2021.102714 · Cited by 11
Impact of parental injury on adolescent sleep
Ahmed, S., Gorman, G. H., Susi, A., Robertson, B., Collen, J. F., & Hisle-Gorman, E. J. (2020) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.8514 · Cited by 11
“Adolescents are particularly vulnerable to insomnia, as teens experience changes in their circadian rhythmas theyprogress throughpuberty.(26) Parental injury may exacerbate these vulnerabilities if it leads to increased caregiving responsibilities for the adolescent, more family conflict, or increases parental injury-…”
Circadian Rhythms, Sleep, and Aging
Garbarino, S., Lanteri, P., Prada, V., Falkenstein, M., & Sannita, W. G. (2020) · Journal of Psychophysiology · doi:10.1027/0269-8803/a000267 · Cited by 11
Quera-Salva, M.-A., Kilic-Huck, Ü., & Vecchierini, M.-F. (2021) · Revue Neurologique · doi:10.1016/j.neurol.2020.07.021 · Cited by 11
McCrae, C. S., Taylor, D. J., Smith, M. T., & Perlis, M. L. (2010) · Behavioral Sleep Medicine · doi:10.1080/15402001003622792 · Cited by 11
“See Hagenauer, Perryman, Lee, and Carskadon (2009) ; and Wolfson and Carskadon (2003) .”
BackgroundMaking Memories: Why Time Matters
Kelley, P., Evans, M. D. R., & Kelley, J. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00400 · Cited by 10
“Starting with the pioneering of Carskadon (Carskadon et al., 1993; Carskadon and Dement, 2005; Millman, 2005; Hagenauer et al., 2009; Carskadon, 2011), US school times were demonstrated to be desynchronized from adolescent biological timing.”
BackgroundChan, C. S., Tang, M. C., Leung, J. C. Y., Poon, C. Y. S., & Lau, E. Y. Y. (2024) · SLEEP · doi:10.1093/sleep/zsae171 · Cited by 10
Melatonin secretion across puberty: A systematic review and meta-analysis
Andersen, C. C., Kjær, E. K. R., Vase, C. B., Mathiasen, R., Debes, N. M., Jørgensen, N. R., & Jennum, P. (2025) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2025.107281 · Cited by 10
Meneo, D., Gavriloff, D., Cerolini, S., Baldi, E., Schlarb, A. A., Nobili, L., & Baglioni, C. (2025) · Journal of Sleep Research · doi:10.1111/jsr.70078 · Cited by 14
“Girls begin to show a delay in the timing of sleep earlier than boys, paralleling their younger pubertal onset (Hagenauer et al. 2009; Roenneberg et al. 2004).”
Wright, L., & Kutcher, S. (2016) · Colloquium Series on The Developing Brain · doi:10.4199/c00133ed1v01y201602dbr012 · Cited by 12
Vidal, H., & Shochat, T. (2017) · Sleep Health · doi:10.1016/j.sleh.2017.08.002 · Cited by 10
“evidence suggests that delayed bedtime is the outcome of a delay in the circadian sleep–wake cycle, dictated by the biological clock, and by slower daily accumulation of sleep pressure, reflecting the homeostatic sleep factor.(4,5,14) On the other hand, early school start times, as well as extracurricular activities (…”
The impact of training shifts in dancers’ chronotype and sleep patterns
Coirolo, N., Silva, A., & Tassino, B. (2020) · Sleep Science · doi:10.5935/1984-0063.20200010 · Cited by 10
Sleep, energy disturbances and pre-competitive stress in female traveller athletes.
Silva, R., & Paiva, T. (2019) · PubMed Central · doi:10.5935/1984-0063.20190093 · Cited by 10
“In addition to sport and competition demands, and participants’ mean age, our gymnasts may be close to an early onset sleep, which was defined by Hagenauer et al. 33 at around 19.5 years old.”
BackgroundInfluentialJamieson, D., Schwenn, P., Beaudequin, D. A., Shan, Z., McLoughlin, L. T., Lagopoulos, J., & Hermens, D. F. (2020) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10077 · Cited by 11
“Previous studies have shown the observed circadian rhythm late shift seems to be aligned with the onset of puberty, rather than with the attainment of chronological age (Crowley et al., 2007; Hagenauer et al., 2009).”
BackgroundInfluentialFigueiredo, S. (2023) · Psychology in the Schools · doi:10.1002/pits.23029 · Cited by 12
Wilson, S. M. B., Sparks, K. V., Cline, A., Draper, S. B., Jones, M. I., & Parker, J. K. (2024) · Behavioral Sleep Medicine · doi:10.1080/15402002.2024.2374257 · Cited by 9
“Although this restriction was applied in response to the differences in biological sleep regulation during childhood and adolescence (Hagenauer et al., 2009), it is noteworthy that recent research has employed behavioral sleep interventions within athletes in this age group, and contain BCTs that…”
Winpenny, E. M., Rowthorn, H., Hollidge, S. E., Westgate, K. L., Goodyer, I. M., Brage, S., & van Sluijs, E. M. F. (2023) · International Journal of Behavioral Nutrition and Physical Activity · doi:10.1186/s12966-023-01420-6 · Cited by 10
“A developmental shift in circadian preference (‘chronotype’) to a later sleep and wake time is thought to take place during adolescence [7], which can lead to ‘social jetlag’ [8], whereby societal demands (e.”
BackgroundChronotype and Its Relationship with Sleep Quality among Professional Students at Indian University
Khan, M. H., Sharma, S. R., & Saleem, M. (2023) · Indian Journal of Physical Therapy and Research · doi:10.4103/ijptr.ijptr_132_23 · Cited by 10
Satellite cells in the growth and maintenance of muscle
Bachman, J. F., & Chakkalakal, J. V. (2024) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2024.01.020 · Cited by 9
The short and long of adolescent sleep: the unique impact of day length
Bartel, K., van Maanen, A., Cassoff, J., Friborg, O., Meijer, A. M., Oort, F. J., Williamson, P., Gruber, R., Knaüper, B., & Gradisar, M. (2017) · Sleep Medicine · doi:10.1016/j.sleep.2017.06.018 · Cited by 8
“2 Adolescents living in areas with a shorter day length may be particularly vulnerable to the effects of evening light, as sensitivity to evening light has also been shown to increase for people who receive less light during the day [25e27] and the period of adolescence may be a time for increased sensitivity to eveni…”
BackgroundSteidten, T., Baumbach, P., May, R., Gabriel, B., Herbsleb, M., Markov, A., Granacher, U., Kellmann, M., Bloch, W., Gabriel, H. H. W., et al. (2021) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2021.689805 · Cited by 13
“during adolescence and concomitant hormonal and neuronal changes that lead to disturbed sleep-wake rhythm affect sleep duration and sleep quality (Campbell et al., 2007; Hagenauer et al., 2009; Darchia and Cervena, 2014).”
BackgroundSelf-Reported Sleep Problems in Adolescent Survivors of Childhood Cancer
Desaulniers, G., Riley, L. P., Vangle, K., Gilleland, J., Higgins, M. K., & Wasilewski‐Masker, K. J. (2015) · Clinical journal of oncology nursing · doi:10.1188/15.cjon.81-88 · Cited by 9
Gutierrez‐Colina, A. M., Quast, L. F., Eaton, C. K., LaMotte, J. E., Stolz, M. G., Mee, L. L., George, R. P., Lee, J. L., Reed, B., Rich, K. L., et al. (2019) · Pediatric Transplantation · doi:10.1111/petr.13577 · Cited by 9
Sleep Duration and Quality in Adolescents: Associations With Suicidal Ideation
Lemke, T., Hökby, S., Carli, V., & Hadlaczky, G. (2025) · Journal of Adolescence · doi:10.1002/jad.12473 · Cited by 8
Yuri, G., Chamorro, R., Tobar, N., & Cifuentes, M. (2025) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2025.102142 · Cited by 11
Convergent thyroid-ATPase interactions regulate collective behavior in Danionella
Zada, D., Kadobianskyi, M., Judkewitz, B., & Lovett-Barron, M. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116730 · Cited by 8
“75 Our findings support the idea of phase shifts in circadian rhythms between juvenile and adult fish, 76 suggesting that genetic and social disruptions can lead to circadian dysregulation and immature social behavior.”
Jamieson, D., Shan, Z., Sacks, D. D., Boyes, A., Lagopoulos, J., & Hermens, D. F. (2022) · The Journal of Early Adolescence · doi:10.1177/02724316221104222 · Cited by 9
“As this circadian rhythm phase delay is believed to be linked to pubertal onset it seems likely that it will impact females at a younger age (Carskadon, 2011; Hagenauer et al., 2009).”
BackgroundMethodSleep and physical activity: results from a long-term actigraphy study in adolescents
Fontanellaz-Castiglione, C. E. G., Timmers, T. T., Lerch, S., Hamann, C., Kaess, M., & Tarokh, L. (2022) · BMC Public Health · doi:10.1186/s12889-022-13657-0 · Cited by 12
“to the circadian timing system [2, 3] which favors later bedtimes in adolescence and is further exacerbated by environmental and psychosocial factors, such as homework, after-school activities, autonomy from parents, socialization and the use of technology (e.”
BackgroundAssociated factors of habitual midday napping among Chinese adolescents
Cui, N., Li, J., Li, J., Cui, N., & Wang, G. (2020) · Sleep and Biological Rhythms · doi:10.1007/s41105-020-00292-8 · Cited by 8
Day-of-week mood patterns in adolescents considering chronotype, sleep length and sex
Díaz‐Morales, J. F., & Parra-Robledo, Z. (2021) · Personality and Individual Differences · doi:10.1016/j.paid.2021.110951 · Cited by 8
Metadata
- Authors
- Hagenauer, M. H., Perryman, J. I., Lee, T. M., & Carskadon, M. A.
- Affiliations
- University of Michigan (US)
- Brown University (US)
- Venue
- Developmental Neuroscience
- Publisher
- S. Karger AG
- Published
- 2009
- Volume
- 31
- Issue
- 4
- Pages
- 276-284
- ISSN
- 0378-5866 (ISSN-L)
- 1421-9859
- PMC
- PMC2820578
- OpenAlex
- W2032467619
- Cited by
- 593
- References
- 67
- Citations by year
- 2026: 42 · 2025: 40 · 2024: 32 · 2023: 34 · 2022: 55 · 2021: 49 · 2020: 53 · 2019: 31 · 2018: 59 · 2017: 44 · 2016: 21 · 2015: 31 · 2014: 28 · 2013: 22 · 2012: 17
- FWCI
- 1.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Developmental Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- National Science Foundation
- National Institutes of Health (5k05mh001358-03, 5r01nr004279-04)
- National Institute of Mental Health (R01MH045945, MH52415, MH01358, R01MH052415, R01MH076969, MH076969)
- National Institute of Nursing Research (NR04279)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007048)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Keywords
- adolescent sleep, sleep deprivation, pubertal development, sleep homeostasis, circadian rhythm, delayed sleep phase, evening light exposure, school start time, mammals
- MeSH terms
- Adolescent, Adolescent Behavior, Animals, Biological Clocks, Circadian Rhythm, Female, Homeostasis, Humans, Light, Male, Puberty, Sleep, Sleep Deprivation, Photoperiod, Gonadal Hormones
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