Periocular skin warming was reported to have favorable effects on subjective and objective sleep quality. We hypothesized that enhancing body heat loss by periocular skin warming would reduce sleep onset and improve sleep quality. Eighteen healthy volunteers were asked to maintain wakefulness with their eyes closed for 60 min after applying either a warming or sham eye mask, followed by a 60-min sleep period. Compared to the sham, periocular warming increased the distal skin temperature and distal–proximal skin temperature gradient only during the 30-min thermal manipulation period. In the subsequent sleep period, periocular warming facilitated sleep onset, increased stage 2 sleep and electroencephalographic delta activity during the first half of the sleep period relative to the sham. These results suggest that periocular skin warming may accelerate and deepen sleep by enhancing physiological heat loss via the distal skin, mimicking physiological conditions preceding habitual sleep.
Habitual sleep onset is usually preceded by a decline in core body temperature (CBT)1. The decline in CBT is promoted by the enhancement of heat loss which results in an increase in the distal skin temperature related with distal skin vasodilation1,2,3,4. Kräuchi and colleagues have reported that heat loss could be indirectly measured by assessing the temperature gradient from the proximal (i.e., infraclavicular, thigh, and stomach) skin to the distal (i.e., foot and hand) skin, known as the distal–proximal skin temperature gradient (DPG), and that the DPG was a good predictor of sleepiness and correlated with sleep onset latency (SOL)3,5,6. Furthermore, they have documented that cold feet or hands due to vasoconstriction syndrome have been associated with sleep onset difficulties7,8,9,10, indicating that the body’s physiological state was not yet ready for sleep due to insufficient heat loss caused by the impaired distal vasodilation3,7,8,9,10. Thus, changes in skin temperature play an important role in sleep regulation.
Many human studies have investigated that the effects of whole or localized body temperature manipulation on sleep regulation, by applying a warm bath11,12,13,14, a high heat capacity mattress15, air conditioning16, bed socks17, or a thermosuit18,19. Some studies have demonstrated that whole body warming by a warm bath 1–2 h before bedtime reduced SOL and increased slow-wave sleep11,12,13,14. Furthermore, regarding the local warming of the body, a study has demonstrated that foot temperature manipulation with bed socks was associated with reduced SOL in young and elderly subjects17. These findings in which sleep was successfully induced after thermal manipulation, may be interpreted as a consequence of the heat loss associated with the elevation of the distal skin temperature.
We have previously developed a disposable heat- and steam generating sheet (HSG-sheet) which can safely and easily manipulate the local skin temperature (e.g., the periocular20,21,22,23,24, neck23, and abdominal25 skin region) at home. Our studies has reported that periocular skin warming before bedtime improved the subjective sleep quality22,23 and increased the electroencephalography (EEG) delta power23 during the first half of the sleep episode in adults with mild difficulty falling asleep. Recently, we have demonstrated that periocular skin warming increased the distal skin temperature in the hand and foot, which indicated enhancement of the physiological heat loss process24. However, it is unclear whether periocular skin warming modulate sleep through physiological heat loss.
In the present study, to clarify the effect of periocular skin warming on sleep, we used a previously developed eye mask with HSG sheets and measured the skin and core body temperature as well as EEG during the sleep period under controlled experimental conditions. This minimizes the confounding effects of posture, food intake, and ambient temperature, as described in a previous study24. We then evaluated the changes in the distal and proximal skin and core body temperatures, as well as in sleep after periocular warming.
Two of twenty health subjects were excluded due to the impairment of the device during the experimental period. Finally, the data of eighteen male subjects (aged 29–57 years, mean ± SD: 45.4 ± 7.7 years) were included in the analysis.
Body temperature, heart rate, and subjective sleepiness
The body temperature measures, heat rate, and subjective sleepiness score obtained just before the thermal manipulation period did not differ between the sham and warming conditions (Table 1). Figure 1 represents changes in the body temperature and heart rate throughout the experimental period. During the 30-min thermal manipulation period in which the periocular skin temperature was manipulated by a warming or sham eye mask, the foot skin temperature significantly increased under the warming condition compared with the sham condition (Fig. 2b), while the infraclavicular and rectum temperature did not differ between the two conditions (Fig. 2a,c). Similarly, the hand skin temperature during the thermal manipulation period significantly increased under the warming condition compared with the sham condition (p = 0.012). The DPG during the thermal manipulation period was significantly higher under the warming condition than under the sham condition (Fig. 2d), while no differences in the DPG were observed between the sham and warming conditions during the subsequent observation and sleep periods. The heart rate did not differ between the sham and warming conditions throughout the experimental period (Fig. 2e). Although the subjective sleepiness scores did not significantly differ between the sham and warming conditions, there was a trend for enforced subjective sleepiness under the warming condition compared with the sham condition during the observation period (p = 0.088; Fig. 2f).
SOL was significantly shortened in the warming condition compared to the sham condition (p = 0.029; Table 2 and Fig. 3). Other sleep parameters did not differ between the sham and warming conditions. To observe the temporal features of the effects, the 60-min sleep period was divided into two: the first half and the second half (Table 3). During the first half of the sleep period, stage 2 sleep was significantly increased under the warming condition compared to the sham condition (p = 0.029; Table 3).
Spectral analysis of EEG
Figure 4 represents the time course of the EEG frequency activities (delta, theta, alpha, and beta activities). The EEG frequency activities during the 60-min sleep did not differ between the sham and warming conditions. Then, the EEG frequency activities were divided into the first and second halves of the 60-min sleep period (Table 4). Delta activity during the first half of the sleep period was significantly increased in the warming condition compared to the sham condition (p = 0.039), while the other frequency activities did not differ between the sham and warming conditions.
Correlations between SOL and body temperatures
There were no significant correlations with SOL and changes in foot skin temperature, CBT, or DPG in the sham and warming conditions. DPG prior to the sleep period was significantly and negatively correlated with SOL in the warming condition (r = − 0.51, p = 0.029; Fig. 5). Similarly, the foot skin temperature prior to the sleep period significantly and negatively correlated with SOL (r = − 0.50, p = 0.034). In the sham condition, however, there were no significant correlations for DPG (r = 0.04, p = 0.848; Fig. 5) and foot skin temperature (r = 0.01, p = 0.97) prior to the sleep period with SOL.
The present study was conducted using a semi-constant routine protocol in which posture, movement, food intake, and ambient temperature were controlled to clarify the effect of periocular skin warming on sleep. Periocular skin warming was revealed to increase the distal skin temperature and DPG, then enhance the subjective sleepiness, which subsequently shortened the SOL and increased stage 2 sleep for the first half of the sleep period. Using EEG spectral analysis, we also found that delta activity during the first half of the sleep period increased after periocular skin warming.
Based on previous studies demonstrating that thermal manipulation promoted sleep induction11,17,18, we hypothesized that periocular skin warming may have shortened SOL by accelerating heat loss, which is typically represented by an elevation in the distal skin temperature.
Periocular skin warming increased the distal skin temperature and DPG without affecting the proximal and core body temperatures, as previously reported24. The increases in the distal skin temperature and DPG, which were reportedly characteristic peripheral manifestations associated with sleep promoting process of the brain1,2,3,4, were observed only during the thermal manipulation period, not but during the observation and sleep periods.
Our results are comparable with our previous findings that periocular warming before bedtime improved subjective sleep initiation and enhanced delta power in the first 90-min period of the nocturnal sleep23. The results obtained through qualitive and quantitative EEG analyses in the present study clearly indicated that periocular skin warming accelerated and deepened non-rapid eye movement (NREM) sleep. Likewise, prior human studies found that homeostatic build-up of sleep pressure26 or pharmacological intervention27 led to the enhancement of sleep. Van Someren and colleagues have demonstrated that continuous skin temperature manipulation using a thermo-suit enhanced and deepened sleep28, and suggested that the effects may be due to modulation of brain areas involved in sleep regulation29.
In the present study, distal skin temperature elevation or heat loss enhanced by periocular skin warming during the thermal manipulation period disappeared during the subsequent periods, when sleep was robustly enhanced and deepened. Our findings can be interpreted as follows; periocular skin warming may have triggered brain mechanisms responsible for NREM sleep control, suggesting a novel interaction between thermal manipulation and sleep.
The effects of periocular skin warming on sleep enhancement might be interpreted by methods other than thermo regulation. Our prior study indicated that the sleep inducing effects of periocular skin warming were strongly related to psychological comfortableness24. Many prior studies have reported that less subjective anxiety at bedtime has been associated with reduced sleep latency and elevated deep sleep30. Our prior study documented that steam inhalation before bedtime first induced psychological relaxation and then increased delta power value31. The present results might be considered as a consequence of the psychological and physiological effects documented in such prior studies.
DPG prior to the sleep period showed significant correlation with SOL in the warming condition, while it was not correlated with SOL in the sham condition. There were no significant correlations between SOL and change in body temperature or DPG. Previously, changes in DPG have been demonstrated to significantly correlate with SOL in the administration of ramelteon32. We postulated that the 30-min observation period might have influenced the detection of association between sleep and changes in thermoregulatory measures.
Regarding the relationship between skin warming and sleep, the location on the skin, temperature, and timing of skin warming are likely to play an important role in sleep. A few studies have reported that the warming the foot skin accelerated sleep onset17,33, whereas others have showed no significant difference in SOL34,35. Additionally, Van Someren and colleague have demonstrated that proximal skin warming was more effective than distal skin warming18,19. However, it is not clear which location on the human skin is most effective to promote sleep. Previous22,23 studies and present study have showed that appropriate periocular skin warming has favorable effects on sleep. We postulate that the periocular skin region might be regarded as one closest regions of the eyes which is directly connected to the brain.
The present result that effects of periocular warming had favorable effects in inducing sleep may conversely indicate a possibility that appropriate periocular cooling could impede sleepiness and help in maintaining wakefulness because prior studies have suggested some thermoregulatory interventions to ameliorate pathologic hypersomnolence36,37,38.
This study had several limitations. First, the experimental studies were conducted in healthy male subjects aged 29–57 years. Difference in age has been reported to negatively affect thermoreception and temperature regulation37. Previously, Van Someren and colleague have demonstrated age-related changes in the thermoregulatory response during skin temperature manipulation17. Furthermore, this study did not include female subjects. Therefore, further study is required to clarify the effects of periocular warming on age- or sex-related thermoregulatory functions. Second, although our previous report suggested an improvement in subjective sleep initiation by periocular skin warming23, the present results alone may not sufficiently reveal the effects of periocular warming on nocturnal sleep because this study examined the effects of periocular warming only during the ascending portion of circadian core body temperature fluctuation, in the daytime. It is necessary to verify whether periocular skin warming has favorable effects on sleep during the night, when circadian core body temperature fluctuation shows descending trend. Further studies under nocturnal sleep conditions are required to confirm the direct relationship between periocular warming and nocturnal sleep. Third, there were no significant differences in the subjective sleepiness score between the sham and warming conditions in the present study. It has been reported that objective measures could be more sensitive to sleepiness than subjective measures39. Further studies including a sensitive objective measure may be required. Fourth, the measurements of distal skin temperature were performed for the dorsum sides of the feet and hands, according to a previous study32. It may be necessary to evaluate more suitable sites of the distal skin region that are involved in heat loss such as the plantar side. Hence, the association with the dorsum and plantar sides of the feet and hands should be investigated in a further study. Fifth, this study was conducted using a warming eye mask, which maintained the periocular skin temperature at 38–40°C for approximately 20 min. However, the duration of warming in the previous study was approximately 10 minutes23. Therefore, further investigation on applying the warming eye mask for varying durations will be necessary to clarify the relationship of warming duration and sleep.
In conclusion, periocular skin warming increased the distal skin temperature that is similar to physiological heat loss related with changes in body temperature before bedtime, leading to the acceleration of sleep onset and increase in delta power during the first half of sleep. These results suggest that skin warming manipulation in the periocular region may have favorable effects in promoting sleep onset by enhancing physiological heat loss.
Twenty healthy volunteers recruited through a clinical research organization participated in this study. All subjects were free of any medical conditions and did not engaged in shift work. The detailed eligibility criteria and the sources of and methods of selection of subjects are described elsewhere24. All study procedures were approved by the Ethics Committee of Kao Corporation, and all subjects provided written informed consent after they received a detailed explanation of the experiment according to the Declaration of Helsinki. The study protocol was registered at the University Hospital Medical Information Network Clinical Trials Registry (UMIN-CTR registry ID: UMIN000029140) on September 14, 2017.
We designed this study in a randomized placebo-controlled crossover manner. Subjects visited a laboratory for two experimental sessions that were 1 week apart. They were asked to keep their habitual sleep–wake schedule for 1 week prior to each session and to refrain from alcohol and caffeinated beverages for 24 h before each session. Subjects were randomly allocated to either a warming session or a sham session during the twice experimental sessions by an assistant staff in the clinical research organization. The study was conducted from October 16 to November 17 in 2017. The detailed experimental design is described elsewhere24.
Figure 6 illustrates the schematic explanation in the experimental session. In each session, subjects were admitted to the laboratory by 10:30 and wore light experimental clothing. Then subjects stayed there until 11:30 while being allowed to read books or listen to music; however, they were prohibited from using cellular phones or watching digital monitors. At 11:30, a designated lunch (500 ~ 600 kcal) was provided to subjects, and the lunch was finished by 12:00. Then, the electrodes and thermistor probes were attached to subjects to obtain polysomnographic and body temperature recordings as described below. Subjects were instructed to keep a semi-recumbent posture on a bed with the head raised at approximately 35 degrees during the experimental period (13:00–15:30). The experimental period was divided into two periods; subjects were asked to remain awake during the first 90-min period (13:00–14:30) and try to sleep during the subsequent 60-min period (14:30–15:30). The 90-min wakefulness period consisted of three consecutive blocks, each with a duration of 30 min. In the first block (Adaptation period), subjects were required to maintain a semi-recumbent posture on a bed with their eyes open from 13:00 to 13:30. At 13:30, subjects were instructed to maintain wakefulness with their eyes closed until 14:30 and the periocular skin temperature was manipulated from 13:30 to 14:00 by placing a warming or sham eye mask on subjects’ periocular region during the block (Thermal manipulation period). In our prior study, the warming eye mask with active HSG sheets was confirmed to increase the periocular skin temperature gradually to 38°C within 5 min and maintain the skin temperature at 38–40°C for approximately 20 min, whereas the sham eye mask with inactive HSG sheets did not changed the skin temperature24. Changes in periocular skin temperature through the use of the warming and sham eye masks have been described in detail elsewhere24. Between 14:00 and 14:30, subjects were asked to maintain the same state as before, and the subjects’ physiological changes were observed in the final block (Observation period). Throughout these blocks, the subjects’ states were monitored visually and via EEG recordings by research assistants to enforce wakefulness, as described in detail elsewhere24. At 14:30, subjects were given a 60 min sleep period. Throughout these experimental periods, an ambient room temperature was maintained at 21–22°C and the light condition was maintained at dim light (~ 100 lx).
Core body and skin temperatures were recorded using a portable device (LT-200, Gram Corp, Saitama, Japan) with a sampling rate of 1 Hz. The core body temperature was obtained using a thermistor that was self-inserted approximately 10 cm into the rectum. The skin temperature was measured at the following locations: the left and right sides of the feet (the middle of the dorsum side), hands (the middle of the dorsum side), infraclavicular regions, and left upper eyelids. The mean value of the left and right infraclavicular skin temperature was defined as the proximal skin temperature. The foot skin temperature of the left and right regions was averaged and was defined as the distal skin temperature. The distal–proximal skin temperature gradient (DPG) was calculated by subtracting the proximal skin temperature from the distal skin temperature. The detailed temperature recordings are described elsewhere24.
Polysomnographic (PSG) recordings were performed with the Biosignal Amplifier system (Polymate AP216, Miyuki Giken Corp., Tokyo, Japan) using four EEG channels (Fz, Cz, Pz, and O1, referenced against linked mastoid A1 and A2), two Electrooculogram (EOG)s channels (right and left outer canthus), a submental electromyogram (EMG), and electrocardiogram (ECG) channels. All data were sampled at 500 Hz. The heart rate was calculated from the R-R interval (RRI) detected on the ECG signal. The detailed polysomnographic recordings are described elsewhere24.
Subjective sleepiness was evaluated using the Karolinska sleepiness scale40. Subjects were instructed to verbally reported their sleepiness at 0, 30, and 60 min after the eye mask placement. The subjects were pre-trained on how to verbally respond twice before application of the eye mask.
Data on the core body temperature, skin temperature, DPG, and heart rate were respectively averaged over the 30-min thermal manipulation and observation periods, and the first and second halves of the 60-min sleep period. In order to examine the effects of thermal manipulation, the averaged core body temperature, skin temperature, DPG, and heart rate obtained during each period were subtracted by the respective baseline data taken just before the thermal manipulation period.
In accordance with the standard criteria41, the EEG recordings were divided into 30-s epochs, and classified into the following sleep stages using an automated stager (NightOwl Professional, NoruPro Light Systems, Inc., Tokyo, Japan)42: awake, rapid-eye-movement (REM), non-REM (NREM) sleep stage1, NREM stage2, and NREM stage3. The automatically staged data were verified by an investigator blinded to the conditions. SOL was defined as the time interval between 14:30 and the first onset of 3 continuous epochs of sleep defined by EEG.
Spectra analysis of EEG (Cz-A1) data was performed using a fast Fourier transform with a Hamming window. The power values for 5-s periods were obtained in the following four bands: delta (1.0–4.0 Hz), theta (4.0–7.0 Hz), alpha (8.0–12.0 Hz), and beta (13.0–20.0 Hz). The power activity in each band was normalized to the mean power value in each band across the sleep phase. Each power activity was averaged into the first half second halves of the sleep period. These analyses were performed with the software package MATLAB (The Math Works Inc., USA) and its signal processing toolbox.
All values are expressed as the mean ± standard error of the mean (SEM). All statistical analyses for comparisons between the sham and warming conditions were performed with the Wilcoxon signed-rank test. Correlations between possible two factors were analyzed using the Pearson’s product-moment correlation coefficient. Probability values of less than 0.05 were accepted as statistically significant. All statistical analyses were performed using IBM SPSS Statistics version 25 (IBM Corp., Chicago, IL, USA).
The datasets analyzed during the current study are available from the corresponding author on reasonable request.
Kräuchi, K. The thermophysiological cascade leading to sleep initiation in relation to phase of entrainment. Sleep Med. Rev. 11, 439–451 (2007).
Gradisar, M. & Lack, L. Relationships between the circadian rhythms of finger temperature, core temperature, sleep Latency, and subjective sleepiness. J. Biol. Rhythms 19, 157–163 (2004).
Kräuchi, K., Cajochen, C., Werth, E. & Wirz-Justice, A. Functional link between distal vasodilation and sleep-onset latency?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R741–R748 (2000).
Rogers, N. L., Bowes, J., Lushington, K. & Dawson, D. Thermoregulatory changes around the time of sleep onset. Physiol. Behav. 90, 643–647 (2007).
Kräuchi, K., Cajochen, C., Werth, E. & Wirz-justice, A. Warm feet promote the rapid onset of sleep. Nature 401, 36–37 (1999).
Kräuchi, K., Cajochen, C. & Wirz-Justice, A. A relationship between heat loss and sleepiness : effects of postural change and melatonin administration. J. Appl. Physiol. 83, 134–139 (1997).
Pache, M. et al. Cold feet and prolonged sleep-onset latency in vasospastic syndrome. Lancet 358, 125–126 (2001).
Vollenweider, S., Wirz-Justice, A., Flammer, J., Orgül, S. & Kräuchi, K. Chronobiological characterization of women with primary vasospastic syndrome: body heat loss capacity in relation to sleep initiation and phase of entrainment. AJP Regul. Integr. Comp. Physiol. 294, R630–R638 (2007).
Kräuchi, K. et al. Cold extremities and difficulties initiating sleep: evidence of co-morbidity from a random sample of a Swiss urban population. J. Sleep Res. 17, 420–426 (2008).
Gompper, B., Bromundt, V., Orgül, S., Flammer, J. & Kräuchi, K. Phase relationship between skin temperature and sleep-wake rhythms in women with vascular dysregulation and controls under real-life conditions. Chronobiol. Int. 27, 1778–1796 (2010).
Haghayegh, S., Khoshnevis, S., Smolensky, M. H., Diller, K. R. & Castriotta, R. J. Before-bedtime passive body heating by warm shower or bath to improve sleep: a systematic review and meta-analysis. Sleep Med. Rev. 46, 124–135 (2019).
Bunnell, D. E., Agnew, J. A., Horvath, S. M., Jopson, L. & Wills, M. Passive body heating and sleep: influence of proximity to sleep. Sleep 11, 210–219 (1988).
Dorsey, C. M. et al. Effects of passive body heating on the sleep of older female insomniacs. J. Geriatr. Psychiatry Neurol. 9, 83–90 (1996).
Mishima, Y., Hozumi, S., Shimizu, T., Hishikawa, Y. & Mishima, K. Passive body heating ameliorates sleep disturbances in patients with vascular dementia without circadian phase-shifting. Am. J. Geriatr. Psychiatry 13, 369–376 (2005).
Kräuchi, K. et al. Sleep on a high heat capacity mattress increases conductive body heat loss and slow wave sleep. Physiol. Behav. 185, 23–30 (2018).
Togo, F. et al. Influence on human sleep patterns of lowering and delaying the minimum core body temperature by slow changes in the thermal environment. Sleep 30, 797–802 (2007).
Raymann, R. J. E. M., Swaab, D. F. & Van Someren, E. J. W. Skin temperature and sleep-onset latency: changes with age and insomnia. Physiol. Behav. 90, 257–266 (2007).
Raymann, R. J. E. M., Swaab, D. F. & Van Someren, E. J. W. Cutaneous warming promotes sleep onset. AJP Regul. Integr. Comp. Physiol. 288, R1589–R1597 (2005).
Raymann, R. J. E. M. & Van Someren, E. J. W. Diminished capability to recognize the optimal temperature for sleep initiation may contribute to poor sleep in elderly people. Sleep 31, 1301–1309 (2008).
Takamoto, K. et al. Thermotherapy to the facial region in and around the eyelids altered prefrontal hemodynamic responses and autonomic nervous activity during mental arithmetic. Psychophysiology 50, 35–47 (2013).
Arita, R. et al. Effects of a warm compress containing menthol on the tear film in healthy subjects and dry eye patients. Sci. Rep 7, 45848 (2017).
Sakamoto, I. et al. Effects of bedtime periocular warming on sleep status in adult female subjects: a pilot study. Evid. Based Complement. Alternat. Med. 2017, 6419439 (2017).
Igaki, M. et al. Effects of bedtime periocular and posterior cervical cutaneous warming on sleep status in adult male subjects: a preliminary study. Sleep Biol. Rhythms 16, 77–84 (2018).
Ichiba, T., Suzuki, M., Aritake-okada, S. & Uchiyama, M. Periocular skin warming elevates the distal skin temperature without affecting the proximal or core body temperature. Sci. Rep. 1–8 (2019).
Nagashima, Y. et al. Application of a heat- and steam-generating sheet increases peripheral blood flow and induces parasympathetic predominance. Evid. Based Complement. Alternat. Med. 2011, 965095 (2011).
Borbély, A. A., Baumann, F. B., Brandeis, D., Strauch, I. & Lehmann, D. Sleep deprivation Effect on sleep stages and EEG power density in man.pdf. Electroencephalogr. Clin. Neurophysiol. 51, 483–493 (1981).
Ma, J. et al. EEG power spectra response to a 4-h phase advance and gaboxadol treatment in 822 men and women. J. Clin. Sleep Med. 7, 493–501 (2011).
Raymann, R. J. E. M., Swaab, D. F. & Van Someren, E. J. W. Skin deep: enhanced sleep depth by cutaneous temperature manipulation. Brain 131, 500–513 (2008).
Van Someren, E. J. W. More than a marker: interaction between the circadian regulation of temperature and sleep, age-related changes, and treatment possibilities. Chronobiol. Int. 17, 313–354 (2000).
Kecklund, G. & Åkerstedt, T. Apprehension of the subsequent working day is associated with a low amount of slow wave sleep. Biol. Psychol. 66, 169–176 (2004).
Ichiba, T., Kakiuchi, K., Suzuki, M. & Uchiyama, M. Warm steam inhalation before bedtime improved sleep quality in adult men. Evid. Based Complement. Alternat. Med. 2019, 2453483 (2019).
Markwald, R. R., Lee-Chiong, T., Burke, T. M., Snider, J. A. & Wright Jr., K., P. Effects of the melatonin MT-1/MT-2 agonist ramelteon on daytime body temperature and Sleep. Sleep. 33, 825–831 (2010).
Ko, Y. & Lee, J. Effects of feet warming using bed socks on sleep quality and thermoregulatory responses in a cool environment. J. Physiol. Anthropol. 37. 13 (2018).
Liao, W. C., Chiu, M. J. & Landis, C. A. A warm footbath before bedtime and sleep in older Taiwanese with sleep disturbance. Res. Nurs. Heal. 31, 514–528 (2008).
Ebben, M. R. & Spielman, A. J. The effects of distal limb warming on sleep latency. Int. J. Behav. Med. 13, 221–228 (2006).
Fronczek, R., Overeem, S., Lammers, G. J., Van Dijk, J. G. & Van Someren, E. J. W. Altered skin-temperature regulation in narcolepsy relates to sleep propensity. Sleep 29, 1444–1449 (2006).
Fronczek, R. et al. Manipulation of core body and skin temperature improves vigilance and maintenance of wakefulness in narcolepsy. Sleep 31, 233–240 (2008).
Fronczek, R. et al. Manipulation of skin temperature improves nocturnal sleep in narcolepsy. J. Neurol. Neurosurg. Psychiatry 79, 1354–1357 (2008).
Van Dongen, H. P. A., Baynard, M. D., Maislin, G. & Dinges, D. F. Systematic interindividual differences in neurobehavioral impairment from sleep loss : evidence of trait-like differential vulnerability. Sleep 27, 423–433 (2004).
Kaida, K. et al. Validation of the Karolinska sleepiness scale against performance and EEG variables. Clin. Neurophysiol. 117, 1574–1581 (2006).
Berry, R. B. et al. The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, version2.2. American Academy of Sleep Medicine. Darien, IL (2015).
Takeuchi, M. et al. Does sleep improve memory organization?. Front. Behav. Neurosci. 8, 1–8 (2014).
We thank K. Tagami, K, Kumihashi, Y, Shimada and H. Takakuwa of Kao Corporation for their support. This study was financially supported by Kao Corporation. We would like to thank Editage (www.editage.com) for English language editing.
Dr. M. Uchiyama has received research support from Astellas Pharma, Eisai, Meiji Seika Pharma, MSD, Taisho Pharmaceutical, Kao Corporation, and Takeda Pharmaceutical, and has consulted for Kao Corporation, Taisho Pharmaceutical and Takeda Pharmaceutical. He has also received honoraria for giving lectures and/or contributing text from Eisai, Meiji Seika Pharma, MSD, and Takeda Pharmaceutical. Dr. M. Suzuki has received research support from Novartis and Otsuka Pharmaceutical, and has received honoraria for giving lectures from Dainippon Sumitomo, Eisai, Meiji Seika Pharma, MSD, Otsuka Pharmaceutical and Takeda Pharmaceutical. Dr. M. Suzuki has received research support from Novartis and Otsuka Pharmaceutical, and has received honoraria for giving lectures from Dainippon Sumitomo, Eisai, Meiji Seika Pharma, MSD, Otsuka Pharmaceutical and Takeda Pharmaceutical. T. Ichiba is an employee of Kao Corporation. Dr. S. Aritake-Okada declares no potential conflict of interest.
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Ichiba, T., Suzuki, M., Aritake-Okada, S. et al. Periocular skin warming promotes body heat loss and sleep onset: a randomized placebo-controlled study. Sci Rep 10, 20325 (2020). https://doi.org/10.1038/s41598-020-77192-x
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