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Circadian rhythm of heat production, heart rate, and skin and core temperature under unmasking conditions in men
Abstract
Seven healthy men were studied in a 34-h constant routine protocol to investigate whether the daily rhythm of heat production and heat loss has an endogenous circadian component. Under these unmasking conditions (constant bed rest, no sleep allowed, regular food and fluid intake), a significant circadian rhythm could be demonstrated for heat production, heart rate, and skin temperatures but not for the respiratory quotient. Heat production and heart rate were phase locked with a maximum at 1100-1200 h. Proximal skin temperatures (infraclavicular region, thigh, and forehead) followed the same circadian rhythm as rectal temperature, whereas distal skin temperatures (hands and feet) were opposite in phase. These physiological circadian rhythm parameters, as well as biochemical parameters (urinary sodium, potassium, urea, and urine flow), were phase advanced by 25-180 min with respect to the circadian rhythm in rectal temperature. Our findings under unmasking conditions show that the circadian variation in rectal temperature is a consequence of endogenous circadian rhythms in both heat production and heat loss.
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“The daily rhythm in core body and skin temperatures is due to the circadian variation in heat production and heat loss and, in particular, the nocturnal increase in heat loss from the extremities, which leads to an increase in distal skin temperatures [1,4,50].”
From Human thermal perception and time of day: A review (2021) · cites this paper as [50]
In the citing paper
“Both heat production and heat loss contribute to the circadian variation in heat content, leading to a circadian rhythm in core body temperature [22].”
From Temperature regulation in women: Effects of the menstrual cycle (2020) · cites this paper as [22]
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“Consistent with our findings in mice, such human studies have provided evidence for an endogenous circadian rhythm of HR, independent of the effects of activity [36–40].”
BackgroundA schizophrenic patient with an arrhythmic circadian rest-activity cycle
Wirz-Justice, A., Cajochen, C., & Nussbaum, P. (1997) · Psychiatry Research · doi:10.1016/s0165-1781(97)00117-0 · Cited by 78
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InfluentialGabel, V., Reichert, C., Maire, M., Schmidt, C., Schlangen, L. J. M., Kolodyazhniy, V., Garbazza, C., Cajochen, C., & Viola, A. (2017) · Scientific Reports · doi:10.1038/s41598-017-07060-8 · Cited by 78
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“Although heat production was not directly assessed in the present study, it has been suggested to be modulated by SNS activity (20, 29).”
BackgroundChanges in cardiovascular function during the sleep onset period in young adults
Carrington, M. J., Barbieri, R., Colrain, I. M., Crowley, K. E., Kim, Y.-M., & Trinder, J. C. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00702.2004 · Cited by 71
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BackgroundAccurate Temperature Measurements for Medical Research Using Body Sensor Networks
Boano, C. A., Lasagni, M., Römer, K., & Lange, T. (2011) · IEEE International Symposium on Object/Component/Service-Oriented Real-Time Distributed Computing Workshops (ISORCW) · doi:10.1109/isorcw.2011.28 · Cited by 70
“We want to confirm those results and verify if brain activity produces a decrease of skin temperature by monitoring the temple skin temperature of patients.”
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“These results are similar with those of Krauchi and Wirz-Justice (Krauchi and Wirz-Justice, 1994).”
ResultSleep Processes Exert a Predominant Influence on the 24-h Profile of Heart Rate Variability
Viola, A., Simon, C., Ehrhart, J., Gény, B., Piquard, F., Muzet, A. G., & BRANDENBERGER, G. (2002) · Journal of Biological Rhythms · doi:10.1177/0748730402238236 · Cited by 69
“The existence of a true circadian influence on HR, with low levels during the night and high levels in the morning hours, has been established in studies checking for confounding effects of sleep, posture, activity, and meal intake, which all contribute to the overall 24-h variations and mask the characteristics of an…”
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“In light of existing data from constant routine studies (Burgess et al., 1997; Kerkhof et al., 1998; Krauchi and Wirz-Justice, 1994), the effect is interpreted as reflecting a circadian system influence,”
BackgroundResultInfluentialNocturnal body core temperature falls in Parkinson's disease but not in multiple‐system atrophy
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Repeated assessment of the endogenous 24-hour profile of blood pressure under constant routine
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“The presence of a circadian rhythm of HR, which was also observed under constant routine by Kräuchi and Wirz-Justice (28), Burgess et al. (29), Kerkhof et al. (12), and Khalsa et al. (30), corroborated the potential of the constant-routine paradigm for exposing endogenous circadian rhythmicity in the cardiovascular s…”
BackgroundDiurnal variation in cutaneous vasodilator and vasoconstrictor systems during heat stress
Aoki, K., Stephens, D. P., & Johnson, J. M. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.2.r591 · Cited by 65
“This rhythm in internal temperature results from an endogenous circadian rhythm in heat production and heat dissipation (4, 13).”
BackgroundHöhn, C., Schmid, S. R., Plamberger, C. P., Bothe, K., Angerer, M., Gruber, G., Pletzer, B., & Hoedlmoser, K. (2021) · Clocks & Sleep · doi:10.3390/clockssleep3010005 · Cited by 61
“After 3 h of short-wavelength light exposure CBT remained higher during the first half of the night.”
MethodInfluentialDifferent effects of heat exposure upon exercise performance in the morning and afternoon
Racinais, S. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2010.01212.x · Cited by 64
“…the hypothermic effect of melatonin may be partly due to an increased convective heat loss as suggested by the increase in temperature of the feet (Kräuchi & Wirz-Justice, 1994) and hands (Van den Heuvel et al., 1999) in humans or of the metatarsals in chickens (Rozenboim et al., 1998).”
BackgroundCardiovascular Chronobiology and Chronopharmacology
Lemmer, B. (2001) · Humana Press eBooks · doi:10.1007/978-1-59259-004-9_12 · Cited by 62
Diurnal variations of tonic electrodermal activity
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Effects of sleep on the cardiovascular and thermoregulatory systems: a possible role for hypocretins
Schwimmer, H., Stauss, H. M., Abboud, F. M., Nishino, S., Mignot, E. J.-M., & Zeitzer, J. M. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00516.2010 · Cited by 60
“(26) and using a greater number of animals it might have been significant.”
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Mora‐Rodríguez, R., Coso, J. D., Hamouti, N., Estévez, E., & ORTEGA, J. F. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1436-4 · Cited by 61
Peripheral Skin Temperature and Circadian Biological Clock in Shift Nurses after a Day off
Bracci, M., Ciarapica, V., Copertaro, A., Barbaresi, M., Manzella, N., Tomasetti, M., Gaetani, S., Monaco, F., Amati, M., Valentino, M., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17050623 · Cited by 63
“In contrast, the peripheral temperature decreases in the daytime raising the core temperature [19,22–25].”
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“This was confirmed by the shape of rectal temperature, very close to a sinusoid (Waterhouse et al., 2005; Waterhouse et al., 2000), and by the forehead skin temperature, which follows the rhythm of rectal temperature (Kräuchi & Wirz-Justice, 1994; Park & Waterhouse, 2013).”
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“Sleep propensity is accompanied by an increased skin blood flow and less cold-induced vasoconstriction, particularly in the distal skin areas that are most strongly involved in the regulation of heat loss because of their richness in arteriovenous anastomoses, thus increasing the skin temperature [22,23].”
BackgroundCircadian disruption and cancer- and treatment-related symptoms
Amidi, A., & Wu, L. M. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1009064 · Cited by 66
“hands, feet) is inversely associated with core body temperature (130).”
BackgroundEnergy metabolism differs between sleep stages and begins to increase prior to awakening
Kayaba, M., Park, I., Iwayama, K., Seya, Y., Ogata, H., Yajima, K., Satoh, M., & Tokuyama, K. (2017) · Metabolism · doi:10.1016/j.metabol.2016.12.016 · Cited by 58
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“Heart rate may provide an additional predictive signal as cardiovascular regulation also expresses a circadian oscillation [18], and increased mean heart rate [19] and reduced variability [20,21] have been associated with increasing severity of psychotic symptoms.”
BackgroundChronopharmacology of Cardiovascular Diseases
Lemmer, B., & Portaluppi, F. (1997) · Handbook of experimental pharmacology · doi:10.1007/978-3-662-09355-9_10 · Cited by 58
Diurnal rhythms of wrist temperature are associated with future disease risk in the UK Biobank
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“Roughly 3.5 °C of these peak-to-through oscillations are driven by the circadian clock 21 , the remainder of about 1.5 – 2 °C is likely driven by behavioral and environmental components.”
InfluentialCircadian Variations in the Kinematics of Handwriting and Grip Strength
Jasper, I., Häußler, A., Baur, B., Marquardt, C., & Hermsdörfer, J. (2009) · Chronobiology International · doi:10.1080/07420520902896590 · Cited by 57
“The well-documented circadian rhythm in body temperature shows its maximum in the early evening and its minimum in the early morning in diurnally active individuals (Kräuchi & Wirz-Justice, 1994).”
BackgroundEffect of Sex, Menstrual Cycle Phase, and Oral Contraceptive Use on Circadian Temperature Rhythms
Kattapong, K. R., Fogg, L. F., & Eastman, C. I. (1995) · Chronobiology International · doi:10.3109/07420529509057274 · Cited by 57
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“It has been described repeatedly with maximal values in the early evening (Gubin et al., 2006a, 2006b; Krauchi & Wirz-Justice, 1994; Waterhouse et al., 2001; Weinert & Waterhouse, 2007).”
BackgroundResultMousel, M. R., Stroup, W. W., & Nielsen, M. K. (2001) · Journal of Animal Science · doi:10.2527/2001.794861x · Cited by 53
“A human study by Krauchi and Wirz-Justice (1994) found that the circadian rhythm of heat production precedes rectal temperature rhythm, thus indicating a phase delay of heat loss with respect to core temperature.”
BackgroundSchizophrenia: the role of sleep and circadian rhythms in regulating dopamine and psychosis
Yates, N. J. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2016-0030 · Cited by 55
“Body temperature is under circadian regulation (Krauchi and Wirz-Justice, 1994) and is responsive to a variety of environmental and biological factors.”
BackgroundSkin temperature, sleep, and vigilance
Lindert, B. H. W. T., & Someren, E. J. W. V. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63912-7.00021-7 · Cited by 53
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Acute finger temperature changes preceding sleep onsets over a 45‐h period
Lack, L. C., & Gradisar, M. (2002) · Journal of Sleep Research · doi:10.1046/j.1365-2869.2002.00312.x · Cited by 51
Drowsiness measures for commercial motor vehicle operations
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Dynamics of Non-visual Responses in Humans: As Fast as Lightning?
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BackgroundAssessing Chronotypes by Ambulatory Circadian Monitoring
Martínez-Nicolás, A., Martínez-Madrid, M. J., Pagán, P., Bonmatí‐Carrión, M., Madrid, J. A., & Rol, M. A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01396 · Cited by 53
Human thermal comfort under dynamic conditions: An experimental study
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“The DPG shows a circadian rhythm such that prior to habitual sleep time the DPG narrows, whereas prior to habitual wake time the DPG widens (Smolander et al., 1993; Kräuchi and Wirz-Justice, 1994; Kräuchi et al., 1997).”
BackgroundPotentially beneficial cardiovascular effects of melatonin administration in women
Cagnacci, A., Arangino, S., Angiolucci, M., et al. (1997) · Journal of Pineal Research · doi:10.1111/j.1600-079x.1997.tb00297.x · Cited by 50
Thermoregulation During Mild Exercise at Different Circadian Times
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Daily oscillations of skin temperature in military personnel using thermography
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Correlation of heart rate variability and circadian markers in humans
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“A circadian rhythm of the mean RR interval series has been shown in many studies, with high levels at night and low levels during the day [2, 58, 10-13].”
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Influences of Melatonin on Human Orcadian Rhythms
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“Studies have shown that decreased core (rectal) temperature and increased distal (foot) temperature are d. associated with shortened sleep-onset latency (Krauchi and Wirz-Justice, 1994; van den Heuvel et al., 1998) and increased NREM sleep (Burgess et al., 2001).”
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“It is well documented that under controlled laboratory resting conditions (e.g. the constant routine protocol), skin-temperature rhythms of diverse skin regions can exhibit a wide spectrum of circadian phase positions (Aschoff et al., 1974; Kräuchi & Wirz-Justice, 1994; Kräuchi et al., 2006).”
BackgroundInfluentialSelf-citationThe influence of a moderate temperature drift on thermal physiology and perception
Ivanova, Y. M., Pallubinsky, H., Kramer, R., & van Marken Lichtenbelt, W. (2021) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113257 · Cited by 45
“However, a gradual increase in core body temperature was observed during the day, which is indicative of normal circadian rhythmicity [38].”
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A sedentary day: effects on subsequent sleep and body temperatures in trained athletes
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“The daily rhythm in core body and skin temperatures is due to the circadian variation in heat production and heat loss and, in particular, the nocturnal increase in heat loss from the extremities, which leads to an increase in distal skin temperatures [1,4,50].”
BackgroundControl of the Cutaneous Circulation by the Central Nervous System
Blessing, W. W., McAllen, R. M., & McKinley, M. J. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150034 · Cited by 54
Bulluck, H., Nicholas, J. M., Crimi, G., White, S. K., Ludman, A. J., Pica, S., Raineri, C., Cabrera-Fuentes, H. A., Yellon, D. M., Rodríguez-Palomares, J. F., et al. (2016) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.12.030 · Cited by 46
Mahadi, M. K., Lall, V. K., Deuchars, S. A., & Deuchars, J. (2019) · Brain stimulation · doi:10.1016/j.brs.2019.05.002 · Cited by 43
“Such circadian patterns of SND as well as BP are found in humans (40, 41).”
BackgroundThe Impact of Time of Day on Energy Expenditure: Implications for Long-Term Energy Balance
Shaw, E., Leung, G. K. W., Jong, J., Coates, A. M., Davis, R., Blair, M., Huggins, C. E., Dorrian, J., Banks, S., Kellow, N. J., et al. (2019) · Nutrients · doi:10.3390/nu11102383 · Cited by 45
“As such, the patterns observed in these two studies [38,39] can only imply circadian rhythmicity in TEE (a combination of RMR and TEF).”
BackgroundInfluentialCircadian regulation of appetite and time restricted feeding
Page, A. J., Christie, S., Symonds, E. L., & Li, H. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112873 · Cited by 44
Circadian variation in base rate measures of cardiac autonomic activity
van Eekelen, A. P. J., Houtveen, J. H., & KERKHOF, G. A. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-004-1158-6 · Cited by 43
“Cognitive performance (Monk et al. 1997), activity of the hypothalamic–pituitary–adrenocortical axis (Buijs et al. 1999), heart rate (Kräuchi and Wirz-Justice 1994), and core body temperature (CBT; Watts 1991) represent parameters that are strongly modulated by an endogenous clock mechanism.”
BackgroundRomeijn, N., Verweij, I. M., Koeleman, A., Mooij, A., Steimke, R., Virkkala, J., van der Werf, Y., & Van Someren, E. J. W. (2012) · Sleep · doi:10.5665/sleep.2242 · Cited by 41
A Review of Environmental Barriers to Obtaining Adequate Sleep in the Military Operational Context
Mantua, J., Bessey, A. F., Sowden, W. J., Chabuz, R., Brager, A. J., Capaldi, V. F., & Simonelli, G. (2019) · Military Medicine · doi:10.1093/milmed/usz029 · Cited by 43
“The optimal temperature of the sleep microclimate is roughly 82 degrees,(35) and a microclimate higher or lower than 82 degrees will increase the risk for sleep disturbances.(33,34) Humidity can also disrupt sleep: the optimal comfort level of humidity is 40–60% for sleeping environment, and several studies have docum…”
BackgroundMeasuring Circadian Temperature Rhythm
HANNEMAN, S. K. G. (2001) · Biological Research For Nursing · doi:10.1177/109980040100200403 · Cited by 42
“Most investigators sample temperature more frequently than 6-minute intervals (Boivin and others 1994; Härmä and others 1994; Kräuchi and Wirz-Justice 1994; Campbell and Murphy 1998; Strijkstra and others 1999; Hanneman 2000; Bailey and Heitkemper 2001; Hanneman and others forthcoming) and collapse…”
BackgroundInfluentialHamouti, N., Fernández‐Elías, V. E., Ortega, J. F., & Mora‐Rodriguez, R. (2014) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.12028 · Cited by 41
“Experimental trials were conducted in the morning to avoid an effect of circadian variation on physiological variables (Krauchi & Wirz-Justice, 1994).”
BackgroundEffect of time-of-day on human dynamic thermal perception
Vellei, M., Pigliautile, I., & Pisello, A. L. (2023) · Scientific Reports · doi:10.1038/s41598-023-29615-8 · Cited by 44
Parker, K. P., Bailey, J. L., Rye, D. B., Bliwise, D. L., & Someren, E. J. W. V. (2007) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2007.00568.x · Cited by 40
“Under normal circumstances, core BT demonstrates a predictable sinusoidal rhythmic variability (circadian rhythm) over a 24-h period with a peak around 21:00 hours and a minimum around 05:00 hours (Krauchi and Wirz-Justice, 1994).”
BackgroundGaspar, L. S., Hesse, J., Yalçın, M., Santos, B., Carvalhas-Almeida, C., Ferreira, M., Moita, J. J., Relógio, A., Cavadas, C., & Álvaro, A. R. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103248 · Cited by 40
“A later time point would be particularly relevant to visualize the melatonin peak, described to occur between 2 and 7 h [61,63,67,69], and the lower levels of corebody temperature reported after the mid-point of sleep [67,87], in healthy subjects.”
Circadian rhythms and cognition
Waterhouse, J. M. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53702-7.00008-7 · Cited by 41
Circadian aspects of body temperature regulation in exercise
Reilly, T., & Waterhouse, J. M. (2009) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2009.01.005 · Cited by 44
Human thermoregulation; A synergy between physiology and mathematical modeling
Kingma, B. (2012) · Research Publications (Maastricht University) · doi:10.26481/dis.20120227bk · Cited by 41
Human body temperature and new approaches to constructing temperature-sensitive bacterial vaccines
White, M. D., Bosio, C. M., Duplantis, B. N., & Nano, F. E. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0734-2 · Cited by 39
“For surface skin temperatures, this circadian variation follows a similar sinusoidal pattern as TC but generally has bigger amplitudes [15].”
Daily rhythm of skin temperature of women evaluated by infrared thermal imaging
Costa, C. M. A., Moreira, D. G., Sillero-Quintana, M., Brito, C. J., de Azambuja Pussieldi, G., de Andrade Fernandes, A., Cano, S. P., & Bouzas Marins, J. C. (2018) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2017.12.002 · Cited by 39
“The peak Tc at approximately 17 h has been previously observed through Tsk in proximal regions and Trectal (Krauchi and Wirz-Justice, 1994), as well as by Toral (Edwards et al.”
BackgroundInfluentialAcute effects of different light spectra on simulated night-shift work without circadian alignment
Canazei, M., Pohl, W., Bliem, H. R., & Weiss, E. M. (2016) · Chronobiology International · doi:10.1080/07420528.2016.1222414 · Cited by 42
Predominance of Distal Skin Temperature Changes at Sleep Onset across Menstrual and Circadian Phases
Shechter, A., Boudreau, P., Varin, F., & Boivin, D. B. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411404677 · Cited by 38
Lorenz, N., Spada, J., Sander, C., Riedel-Heller, S. G., & Hegerl, U. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.06.022 · Cited by 38
Circadian rhythms and psychiatric illness
Asarnow, L. D., Soehner, A. M., & Harvey, A. G. (2013) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e328365a2fa · Cited by 38
“Core body temperature can be measured by a variety of methods, such as intravascular, tympanic, bladder, rectal, and esophageal [19].”
Background
Metadata
- Authors
- Krauchi, K., & Wirz-Justice, A.
- Affiliations
- Chronobiology Laboratory, Psychiatric University Clinic, Basel,Switzerland.
- Venue
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
- Publisher
- American Physiological Society
- Published
- 1994-09-01
- Volume
- 267
- Issue
- 3
- Pages
- R819-R829
- ISSN
- 0363-6119 (ISSN-L)
- 1522-1490
- OpenAlex
- W1883140844
- Cited by
- 558
- References
- 0
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 16 · 2023: 25 · 2022: 21 · 2021: 37 · 2020: 32 · 2019: 28 · 2018: 23 · 2017: 24 · 2016: 26 · 2015: 21 · 2014: 12 · 2013: 24 · 2012: 20
- FWCI
- 3.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Physiology (medical) › Thermoregulation and physiological responses
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- circadian rhythm, thermogenesis, heat loss, heart rate, skin temperature, core body temperature, rectal temperature, constant routine, phase locking, phase advance, urinary sodium, urinary potassium, urea, urine flow, respiratory quotient, endogenous circadian rhythm
- MeSH terms
- Adult, Body Temperature, Body Temperature Regulation, Calorimetry, Indirect, Circadian Rhythm, Heart Rate, Humans, Male, Pulmonary Gas Exchange, Skin Temperature, Urine
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