Eto et al.
Journal of Physiological Anthropology(2022) 41:42
https://doi.org/10.1186/s40101-022-00316-x

ORIGINAL ARTICLE

Open Access

Circadian phase advances in children
during camping life according to the naturallight‑dark cycle
Taisuke Eto1,2,3,4 , Shingo Kitamura4 , Kana Nishimura1, Kota Takeoka1, Yuki Nishimura1,5 , Sang‑il Lee2,6 ,Michihiro Ohashi1,3 , Akiko Shikano7 , Shingo Noi7   and Shigekazu Higuchi2*   

Abstract
Background: It is known that the circadian rhythm phase in adults can be advanced in a natural light-dark cycle
without electrical lighting. However, the effect of advanced sleep-wake timing according to the natural light-darkcycle on children’s circadian phase is unclear. We investigated the effects of approximately 2 weeks of camping life
with little access to artificial lighting on children’s circadian phases. We also conducted an exploratory examination on
the effects of wake time according to natural sunrise time on the manner of the advance of their circadian phases.
Methods: Twenty-one healthy children (mean ± SD age, 10.6 ± 1.4 years) participated in a camping program withwake time (4:00) being earlier than sunrise time (EW condition), and 21 healthy children (10.4 ± 1.1 years) participatedin a camping program with wake time (5:00) being almost matched to sunrise time (SW condition). Salivary dim
light melatonin onset (DLMO) before the camping program and that after approximately 2 weeks of camping werecompared.
Results: DLMO was advanced by approximately 2 h after the camping program compared with the circadian phasein daily life in both conditions. In addition, the advances in DLMO were significantly correlated with mid-sleep points
before the camp in both conditions (EW: r = 0.72, p < 0.01, SW: r = 0.70, p < 0.01). These correlations mean that thephase advance was greater for the children with delayed sleep habits in daily life. Furthermore, in the EW condi‑
tion, mean DLMO after the camp (18:09 ± 0:33 h) was earlier than natural sunset time and there was no significant
decrease in interindividual variability in DLMO. On the other hand, in the SW condition, mean DLMO after the camp
(18:43 ± 0:20 h) matched natural sunset time and interindividual variability in DLMO was significantly lower than that
before the camp.
Conclusions: Camping with advanced sleep and wake timing under natural sunlight advances children’s circadianphases. However, DLMO earlier than sunset in an early waking condition may lead to large interindividual variability inthe circadian rhythm phase.
Keywords: Circadian rhythm, Melatonin, Children, Sleep, Camping, Lighting, Physiology, Photoperiods, Non-image
forming effect*Correspondence: higu-s@design.kyushu-u.ac.jp
2
Department of Human Science, Faculty of Design, Kyushu University, 4‑9‑1
Shiobaru, Minami‑ku, Fukuoka 815‑8540, Japan
Full list of author information is available at the end of the article

BackgroundIn modern society, electric lighting allows people to livein bright environments during the day and at night. The
modern light environments that are detached from anatural light-dark cycle, i.e., sunset and sunrise, disturb© The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to theoriginal author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images orother third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line
to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of thislicence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​
mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Eto et al. Journal of Physiological Anthropology(2022) 41:42

circadian rhythm and sleep timing [1–3]. Circadianrhythm and sleep timing are delayed by light exposure
during the early biological night [4, 5], and late circadian rhythm, late sleep timing and a concomitant lackof sleep duration are associated with adverse effects
such as a decline in cognitive function [6] and increased
risk of mood disorder [7], diabetes [8], and obesity [9].
The use of electric lighting at night has been shown
to be associated with later circadian and/or sleep timing by field surveys in rural areas [2, 10, 11] and urban
areas [12, 13], and it has been shown that the internal
circadian clock synchronizes with the natural light-darkcycle in camping life without electric lighting [1] insummer and winter [3].
Although these findings provide evidence that modern
light environments contribute to later circadian rhythm
and that adult humans have the capability for entrainment of the circadian clock to the natural light-darkcycle, the influence of living without electric lighting onchildren’s circadian clock is not known. Recently, even inchildren and adolescents, many studies have shown that
insufficient sleep due to a later circadian clock caused byelectric lighting at night [14, 15] could be associated withsome health problems [16–19]. Furthermore, it has beenreported that children’s circadian systems are highly sensitive to light at night [20–22]. The behavior of children’s
circadian rhythm in the natural light-dark cycle should beclarified in order to better understand the effects of modern light environments on the circadian clock in children.
In addition, it is important to consider how the sleepwake schedules affect the photoentrainment function of
the circadian clock. In a previous study in which adults’circadian rhythms in a natural environment were investigated [1], sleep-wake schedules were selected by participants themselves, and the effects of sleep schedule on theprocess by which the circadian clock entrains the naturallight-dark cycle are therefore unclear.
We had the opportunity to obtain data for the circadianphases in camping programs conducted in 2016 and 2017with the cooperation of an organization that coordinates
camping programs with little access to artificial lighting for children every summer. The sleep schedule had awake time set approximately one hour before the natural sunrise time in the 2016 camping program, whereas
the wake time in the 2017 camping program was set toapproximately matched sunrise time. In the two camping programs with different wake times, circadian phasechanges due to camping life for approximately 2 weeks
were observed in an exploratory manner. Therefore, inthis study, we investigated the effects of camping life withlittle access to artificial lighting on children’s circadianphases, and we also conducted an exploratory examination on the effects of wake time according to natural

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sunrise time on their circadian phases by comparisons ofresults obtained in 2016 and 2017.

Methods
Participants and experimental conditions

Twenty-one healthy children (age range, 9–13 years;
mean ± SD age, 10.6 ± 1.4 years; sixteen boys and fivegirls) participated in a camping program from July toAugust in 2016, and 21 healthy children (age range, 9–14
years; mean ± SD age, 10.4 ± 1.1 years; eighteen boys andthree girls) participated in a camping program from Julyto August in 2017. All subjects had no existing medical
conditions and were not taking any routine medications.
All of the participants gave written informed consent
for participation in the study, which was approved by
the Ethical Committee of Kyushu University. Informed
consent forms for the children were completed by theparents after confirming their child’s agreement for participation. The experiments were conducted in accordance with the Declaration of Helsinki.
The camping programs were conducted by Mobilityland Corporation in Japan. The campsite was locatedin Tochigi Prefecture, Japan (latitude: 36.5°N, longitude: 140.2°W). According to the Sunrise Sunset Times
Lookup website [23], the average times of sunset andsunrise during the camping program were 18:50 and 4:42,
respectively, in 2016 and 18:49 and 4:43, respectively, in
2017. Bedtimes and wake times were set by the organizerof the camping program for 19:30 and 4:00, respectively,
in 2016 (Earlier wake time condition [EW condition]:wake time being earlier than sunrise time) and for 20:00
and 5:00, respectively, in 2017 (synchronized wake time
condition [SW condition]: wake time being almost
matched to sunrise time). Meal times during the camping
life were breakfast at 6:30, lunch at 12:00 and dinner at
17:00 in both the EW and SW conditions. At times otherthan sleep and meal times, the children participated incamping program events including playing in the forest,
playing in a river and craftwork workshops. During theevening hours, participants prepared and ate dinner andstudied in a shed with incandescent lamps. Illuminanceinside the shed in the evening was less than 30 lx. For 2
weeks before the first day of the camping program, theparticipants were instructed to maintain their habitual
bedtime and wake time and to keep a sleep diary bythemselves. Sleep-wake habits and daily light exposure inthat 2-week period were recorded by wrist activity monitors with a light sensor to verify compliance with instructions (in 2016: ActiSleep BT Monitor, Acti Japan; in 2017:
MotionWatch 8, CamNtech). Although recording of
sleep-wake habits and light exposure by the sleep diaryand wrist activity monitors was also performed during
the camping program (Fig. 1), the data obtained from

Eto et al. Journal of Physiological Anthropology(2022) 41:42

Fig. 1 Overview of the experimental protocol with data obtained by
actigraphy. Data obtained in 2017 for a participant’s activity and light
exposure measured by a wrist activity monitor with a light sensor(MotionWatch 8). Black ticks denote activity and yellow ticks denotelight exposure. The vertical axis shows the number of days in thecamping program session and the horizontal axis shows the time ofday. PreCamp-DLMO assessment was performed on the first day ofthe camping program both in the earlier wake time (EW) condition
and the synchronized wake time (SW) condition. Camp-DLMO
assessment was performed on the 11th day of the camping programin the EW condition and on the 14th day of the camping program in
the SW condition

wrist activity monitors were excluded from further analysis because the data were frequently missing because theparticipants sometimes forgot to wear the monitors ordevices failed and because the devices used in the two
conditions were different due to technical reasons. The
environmental light illuminance in the campsite wasrecorded by light intensity loggers (HOBO CO-UA-002,
Climatec). Figure 2 shows the average environmental
light illuminance in the campsite measured by HOBO in
the EW and SW conditions. The mean illuminances fromsunrise to sunset during the camping program were 1067
± 691 lx and 662 ± 417 lx in the EW and SW conditions,
respectively.
Circadian phase assessments

The internal circadian phase was determined by salivary melatonin secretion onset time at evening,which is known as DLMO (dim light melatonin onset)[24, 25]. The first internal circadian phase assessment for determining the circadian phase in daily life

Page 3 of 10(PreCamp-DLMO) was performed on the first day ofthe camping program both in the EW condition and in
the SW condition. The second internal circadian phaseassessment for determining the circadian phase during
camping life (Camp-DLMO) was performed on the 11th
day of the camping program in the EW condition and on
the 14th day of the camping program in the SW condition. The different assessment days between the two
conditions were due to the schedule of the camping program. The circadian phase assessments were performed
in a shed located at the camping site with dim lighting (<30 lx) [25, 26] in the angle gaze when participants wereseated and looking straight ahead, and saliva samples
were collected to determine melatonin concentration
every hour using the Salivette saliva collection device
with a plain cotton plug from 17:00 until bedtime. Participants were instructed to finish dinner by 17:00 on the
day of circadian assessments and sit in a chair until finishing the saliva sample collection procedure, i.e., until
bedtime. Participants did not drink any water for 15
min prior to each salivary sample collection. Except forthe saliva collection time, the participants were allowed
to study, talk, and read. Participants were instructed towear sunglasses if they went outside the shed to use therestroom or for other purposes during the saliva sample
collection procedure. Bedtime, i.e., end time of collection of saliva samples, was defined as each participant’s
habitual bedtime in the PreCamp-DLMO assessment,
while it was set to 20:00 in the Camp-DLMO assessment. Salivary melatonin concentrations were quantified
by using a radioimmunoassay kit (RK-DSM2, Bühlmann
Laboratories). The time of DLMO, which is a marker ofthe circadian phase, was determined by linear interpolation between two time points at which melatonin concentration crossed the 4.0 pg/mL threshold [27, 28].
Data and statistical analysis

Information on sleep habits (bedtime, wake time, midsleep point, and sleep duration) was obtained fromsubjective sleep diaries because actigraphy data were
frequently missing because the participants sometimes
forgot to wear the monitors or the devices failed, as mentioned above. Data for sleep habits were averaged data fora period of 2 weeks before the camping program and datafrom the day of the first circadian phase assessment to
the day of the second circadian assessment as representative values of sleep habits in daily life and camping life,
respectively. DLMO and sleep schedule before the camping program and those during the camping program
were compared by a two-tailed paired t test, and DLMO,
sleep-wake cycles and light exposure in the EW condition
and those in the SW condition were compared by a twotailed Welch’s t test.

Eto et al. Journal of Physiological Anthropology(2022) 41:42

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Fig. 2 Mean environmental light illuminance in the campsite. Mean environmental light illuminance during the camping program in the campsite
measured by HOBO in the earlier wake time (EW) condition (A) and in the synchronized wake time (SW) condition (B)Although all of the children who participated completed all of the procedures of the experiment, fivechildren were excluded from further analysis because
PreCamp (two children in the EW condition and one
child in the SW condition) or CampDLMO (two children in the SW condition) could not be detected due tono melatonin secretion until bedtime, and six children(three children in the EW condition and three children
in the SW condition) were excluded because of the omission of recording in sleep diaries. p < 0.05 was considered
to be statistically significant in all statistical analyses. All
results are presented as means ± SD.

Results
Table 1 shows sleep-wake schedules in daily life before
the camp (PreCamp) and in the camping program(Camp). The bedtime, wake time and mid-sleep point in
the camping program were significantly earlier than those
before the camp in both EW and SW conditions due tothe forced earlier sleep-wake cycle in the camping program (EW condition: n = 16, all p < 0.0001; SW condition: n = 15, all p < 0.0001). On the other hand, there wasno significant difference between sleep duration before
the camp and that during the camp (EW condition: p= 0.12; SW condition: p = 0.43). A comparison of thesleep-wake cycles during the camping program between
the EW and SW conditions showed that the Camp-waketime and mid-sleep point in the EW condition were significantly earlier than those in the SW condition and
the Camp-sleep duration in the EW condition was significantly shorter than that in the SW condition (Table 1,
EW condition: n = 16 and SW condition: n = 15, waketime: p < 0.001; mid-sleep point: p < 0.01; sleep duration:p < 0.05). The Camp-bedtime in the EW condition had atendency for being earlier than that in the SW condition(p = 0.08).
DLMO, which is a marker of circadian phase, at thesecond circadian assessment (Camp-DLMO) was significantly advanced by the camping program compared withthat at the first assessment in both the EW condition and
the SW condition (EW: n = 16, p < 0.0001; SW: n = 15,
p < 0.0001). The average advances of DLMO were about
2 h in both conditions (EW condition: 2:02 ± 0:48 h, SW
condition: 2:06 ± 0:45 h, Fig. 3). The circadian advancewas significantly correlated with changes in bedtime andwake time in both conditions (EW condition: [bedtime]r = 0.75, p < 0.001, [wake time] r = 0.60, p < 0.05; SW
condition: [bedtime] r = 0.77, p < 0.001, [wake time] r =0.51, p < 0.05, Pearson’s correlation test). A comparisonof DLMO between the EW and SW conditions showedthat Camp-DLMO in the EW condition was significantly earlier than that in the SW condition (Table 1, p
< 0.01). Camp-DLMO in the EW condition (18:09 ±0:33) was significantly earlier than sunset time at thesecond DLMO assessment day (sunset time: 18:46, p <0.01, one-sample t test) and the inter-individual varianceof Camp-DLMO was not significantly lower than that of
PreCamp-DLMO (p = 0.21, F test; Fig. 4A). On the other
hand, Camp-DLMO in the SW condition (18:43 ± 0:20)
almost matched sunset time at the second DLMO assessment day (sunset time: 18:43, p = 0.66, one-sample t-test)
and the large inter-individual variance of PreCampDLMO was significantly decreased by the camping life (p< 0.01, F test; Fig. 4B). In addition, there were significant
correlations between circadian advances and mid-sleep
point before the camp in both conditions (EW condition: r = 0.72, p < 0.01; SW condition: r = 0.70, p < 0.01;
Fig. 5). These results indicate that the Camp-DLMO

Eto et al. Journal of Physiological Anthropology(2022) 41:42

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Table 1 Sleep habits and circadian phase
Earlier wake time (EW) condition (n = 16)

Synchronized wake time (SW) condition (n = 15)[h:m]

PreCamp(Mean ± SD)

Camp(Mean ± SD)t valuep value

PreCamp(Mean ± SD)

Bedtime21:26 ± 0:54†

19:48 ± 0:15

7.03

< 0.0001‡

8.92< 0.0001

22:05 ± 0:52†

23:58 ± 0:09‡

8.90< 0.0001

1.65

0.12

18:09 ± 0:33‡

9.74< 0.0001

Wake timeMid-sleep point
Sleep duration
DLMO

6:06 ± 0:59

4:08 ± 0:17

8:40 ± 0:46

8:20 ± 0:25†

25:46 ± 0:51
20:11 ± 0:49†

Camp(Mean ± SD)t valuep value

19:56 ± 0:12

10.56

< 0.0001

6:41 ± 0:58

4:35 ± 0:16‡

8.85< 0.0001

11.21< 0.0001

8:36 ± 0:36

24:12 ± 0:13‡
8:45 ± 0:34†

0.80

0.43

18:43 ± 0:20‡

10.38< 0.0001

26:23 ± 0:52
20:50 ± 0:45†

Each index was compared between PreCamp and Camp using the paired t test. Data for sleep habits (bedtime, wake time, mid-sleep point, and sleep duration) wereaveraged data for a period of 2 weeks before the camping program and averaged data from the day of the first circadian phase (DLMO) assessment (first day of thecamping program in both conditions) to the day of the second DLMO assessment (11th day in the EW condition and 14th day in the SW condition)
DLMO Dim light melatonin onset

advance was greater for children who had delayed sleep
habits in daily life.

Discussion
Children’s circadian rhythm phase, i.e., DLMO, advanced
approximately 2 h after 1.5 or 2 weeks of living in accordance with a natural light-dark cycle compared with thecircadian rhythm phase in daily life. We showed that theforced earlier sleep-wake cycle and light exposure by
natural sunlight may have caused the children’s circadianrhythm phase to advance. We provided new evidence
that children’s circadian clock may be capable of entrainment to the natural light-dark cycle.
Interestingly, mean Camp-DLMO in the EW condition
was earlier than sunset time and interindividual variability in Camp-DLMO remained large and was not significantly different from PreCamp-DLMO, while mean
Camp-DLMO in the SW condition almost matched sunset time and interindividual variability in Camp-DLMO

was significantly lower than that in PreCamp-DLMO.
Wake time that was earlier than the natural sunrise timein the EW condition may have contributed to the DLMO
advance to before sunset time and to the interindividual
variability in the circadian phase. The advance of DLMO
to before sunset time in the EW condition would be dueto the exposure of children who were already awake
to natural light before sunrise (Fig. 2A). Regarding thecontribution of waking up earlier than sunrise to interindividual variability in the circadian phase, it is possiblethat exposure around DLMO to natural light before sunset affected the results. The average environmental lightilluminance around Camp-DLMO in the EW condition(18:09) was 60.7 lx (illuminance range, 10.8–161.5lx; n= 11 days, measured by HOBO) and the children in the
EW condition were presumed to have been exposed,though not excessively, to sunlight at the start of biological night. On the other hand, the amount of light exposure around Camp-DLMO in the SW condition (18:43 ±Fig. 3 Change in mean salivary melatonin onset and mean sleep-wake timing. Mean dim light melatonin onset (DLMO) and sleep-wake timing
were compared during daily life (PreCamp) and during the camping program (Camp) in the earlier wake time (EW) condition (A) and in thesynchronized wake time (SW) condition (B). Salivary melatonin onset is shown as colored triangles. Blue triangles indicate PreCamp-DLMO andred triangles indicate Camp-DLMO. Bedtimes and wake times were set for 19:30 and 4:00, respectively, in the EW condition and for 20:00 and 5:00,
respectively, in the SW condition

Eto et al. Journal of Physiological Anthropology(2022) 41:42

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Fig. 4 Change in individual salivary melatonin onset and individual sleep-wake timing. Individual dim light melatonin onset (DLMO) andsleep-wake timing were compared during daily life (PreCamp) and during the camping program (Camp) in the earlier wake time (EW) condition(A) and in the synchronized wake time (SW) condition (B). Salivary melatonin onset is shown as colored triangles. Blue triangles indicate
PreCamp-DLMO and red triangles indicate Camp-DLMO. Bedtimes and wake times were set for 19:30 and 4:00, respectively, in the EW condition
and for 20:00 and 5:00, respectively, in the SW condition

Fig. 5 Relationships between habitual sleep timing and change in salivary melatonin onset time. Change in salivary dim light melatonin onset(DLMO), which is a marker of circadian phase, was related to habitual sleep timing (mid-sleep point) before the camping program in the earlier
wake time (EW) condition (A) and in the synchronized wake time (SW) condition (B). The vertical axis shows the change in DLMO [h] and thehorizontal axis shows the mid-sleep point [h] before the camping programEto et al. Journal of Physiological Anthropology(2022) 41:42

0:20) was 1.54 lx (illuminance range, 0.0–10.8 lx; n = 14days) and was significantly less than that in the EW condition (p < 0.01, two-tailed Welch’s t test; Fig. 2). Light
exposure around DLMO, i.e., the start of biological night,
has been reported to contribute not only to the delay ofthe biological clock [4, 5, 29] but also to the expansion ofindividual variability in the circadian phase [30]. DLMO
advanced to before sunset by waking earlier than sunrise;consequently, the environmental light before sunset was
exposed to the biological night. Thus, a decrease in theinter-individual variability of the circadian phase during
camping life might have been inhibited in the EW condition. Although the mechanism by which biological night
light exposure contributes to increased individual differences in circadian rhythms is unknown, individual differences in light sensitivity of the circadian system may haveaffected the interindividual variability in the circadianphase [31, 32]. The light exposure around DLMO may
seem low, but it may be sufficient to induce a non-image
forming response given the high light sensitivity of children [20, 21, 33].
It should be noted that the fact that the mean CampDLMO in the SW condition was almost matched to sunset time may be coincidental. Therefore, a future study
is needed to determine whether similar findings can beobtained under different day-length conditions, suchas different seasons, different latitudes and different
environmental illuminance. In addition, it is debatable
whether natural light was essential to this study’s findingsthat the circadian phase advanced by about 2 h. To verify
this, an experiment in which only the sleep schedule isadvanced in an artificial lighting environment is needed
as a control experiment. Furthermore, we cannot rule out
the possibility that the baseline circadian phase, i.e., PreCamp-DLMO, had an effect on the earlier Camp-DLMOin the EW condition than that in the SW condition. The
PreCamp-DLMO in the EW condition was significantly
earlier than that in the SW condition (Table 1). However, PreCamp-DLMO did not significantly correlatewith Camp-DLMO in both the EW condition (r = 0.32,
p = 0.24) and the SW condition (r = 0.14, p = 0.62).
This means that earlier Camp-DLMO in the EW condition cannot be explained by only early PreCamp-DLMO.
Therefore, we suspect that Camp-DLMO in the EW condition was earlier than that in the SW condition due tothe influence of waking before natural sunrise time rather
than earlier PreCamp-DLMO.
This study has some limitations. First, the intervals
between the first and second circadian phase assessments were different in the EW condition (11 days)
and SW condition (14 days). The DLMO earlier thansunset time in the EW condition might be considered
to be the result of detecting the state of the middle ofPage 7 of 10

the synchronization process due to the short interval
between the first and second circadian phase assessments. However, it has been shown that the circadianrhythm entrained the natural light-dark cycle within 1
week in a previous study in which the effects of the natural light-dark cycle on adults’ circadian clock were investigated [1]. Therefore, the intervals of circadian phaseassessments in both conditions are considered to be longenough to detect circadian rhythms in the synchronization state, and the differences in the manner of advance
between the EW and SW conditions could be due to differences in the wake time during the camping life. Second, natural light exposure might have been different in
the EW and SW conditions because weather conditions
could not be controlled across conditions. In fact, theaverage environmental light illuminance in the campsite
measured by HOBO was lower in the SW condition than
EW condition (Fig. 2), suggesting that the camp programin the SW condition may have had poor weather overall(see Figure S1 for daily environmental light illuminanceduring the camping program). Therefore, we cannot ruleout the possibility that the differences in weather conditions between the EW and SW conditions influenced theresults for circadian phase. Third, since the sleep schedule
was decided by the organizer of the camping program, we
also could not control the sleep opportunity. One of thegoals of the camping program was to improve children’s
sleep habits. Therefore, not only delaying the early waketime but also extending the sleep duration was conductedin the 2017 camping program (SW condition), based on
the results of the 2016 camping program (EW condition).
The sleep duration was significantly different between
the EW and SW conditions (show Table 1) and this difference may have affected the circadian phase results.
However, the difference in sleep duration between thetwo conditions would have occurred due to the earlier wake time in the EW condition rather than bedtime
because there was a significant difference in wake time
but no significant difference in bedtime between the two
conditions (show Table 1). Therefore, we assume thatthe earlier DLMO in the EW condition may have been
influenced by earlier waking time rather than sleep duration. Finally, although the illuminance in the dim lighting
condition (< 30 lx) during the saliva sampling was determined according to previous reports [25, 26], it may havebeen a relatively high level. Illuminance in DLMO measurements has recently been recommended to be less than
10 lx [34]. The illuminance level in the shed could not be
set to a sufficiently low level because the children neededsome brightness to cook dinner and study in the camping program. Although a previous study showed thatmelatonin is suppressed even at an illuminance of 15 lx in
pre- to mid-pubertal adolescents [35], it is possible that

Eto et al. Journal of Physiological Anthropology(2022) 41:42

the subjects in the previous study had stayed in a neardark environment (~ 0.1 lx) just prior to light exposureand thus had increased light sensitivity in the circadiansystem [36–38]. On the other hand, the light sensitivity
in the circadian system of participants in this study might
be decreased in the evening because they were exposed
to high-illuminance sunlight in the daytime during thecamping program. In addition, it has been shown that
low-color temperature lighting has a small effect on melatonin secretion even with 40 lx illuminance [39], and thedim light environment with an incandescent lamp in thisstudy also might have had a only small effect on melatonin secretion. Furthermore, the children in this study
were studying and reading during the DLMO assessment and their gaze was directed downward. Therefore,
the actual cornea illuminance may have been less than
30 lx. Nonetheless, the fact that DLMO was measured ata relatively high illuminance is a limitation of this study.
The DLMO in this study may not be accurate; however,
it is certain that the circadian phase was advanced by thecamping program since PreCamp-DLMO and CampDLMO were measured under the same illuminanceconditions.
We showed that constructed light environments inmodern society lead to a delay in children’s circadianphase or sleep-wake cycle and that the start of biologicalnight in children, i.e., DLMO, is significantly advanced
by 1.5 weeks or 2 weeks of camping life with a sleepwake rhythm according to the natural light-dark cycle(Fig. 3). The circadian phase advance was greater forchildren who have eveningness sleep habits in their daily
life (Fig. 5). In addition, the difference in wake times in
the camping program schedules in 2016 (EW condition)and 2017 (SW condition) indicated that wake time thatis earlier than natural sunrise time may lead to advanced
DLMO before sunset and large interindividual variability in DLMO (Fig. 4). The finding of this study will contribute to an understanding of the mechanisms by which
delayed circadian and sleep-wake rhythms develop inchildren in modern society [40, 41] and to the establishment of treatment for them [42]. For example, exposing
a patient with a delayed circadian phase to a light environment and sleep-wake cycle in accordance with thenatural light-dark cycle may result in proper timing of thecircadian clock. Recently, it has become possible to artificially create skylights indoors [43], and the feasibility oftreatments using natural light is increasing. Although it
has been shown that morning light exposure combinedwith a forced advanced sleep schedule can advance thecircadian phase in young adults [44] and adolescents [45],premature sleep-wake cycles may lead to circadian phaseinstability. Since exposure to sunlight, which is a strong
zeitgeber, and a properly set sleep-wake schedule canPage 8 of 10

adjust the internal biological clock to the desired timing
regardless of age, i.e., adults [1] or children, and regardless of daily sleep habits, i.e., morningness or eveningness, they would contribute to reduction of negative
effects due to circadian misalignments.

Conclusions
The results of our study in which advances in circadianphases in children during camping life suggested thatchildren’s circadian clock may be capable of entrainment
to the natural light-dark cycle. Our results also showedthat even when children spend time in a natural environment with sunlight, which is a strong zeitgeber, inappropriate sleep-wake schedules, e.g., waking earlier thansunrise, may lead to large interindividual variability of
the circadian rhythm phase. Our findings are expected
to contribute to an understanding of children’s circadianclock and to the establishment of appropriate light environments for improving health problems caused by circadian misalignment.
Supplementary Information
The online version contains supplementary material available at https://​doi.​
org/​10.​1186/​s40101-​022-​00316-x.
Additional file 1: Figure S1. Daily environmental light illuminance during
the camping program.
Acknowledgements
The authors would like to thank Ryuichiro Sakino, producer of the camping
program, and all camping staff in Mobilityland Corporation in Japan for theirunderstanding and cooperation in our study.
Authors’ contributions
SK, KN, KT, AS, SN, and SH contributed to the design of the experiment. TE, SK,
KN, KT, YN, SL, MO, and SH performed the experiment. TE, KN, and KT analyzed
the data. TE, KN, and KT wrote the manuscript. SK, YN, SL, MO, AS, SN, and SH
participated in the discussion and preparation of the manuscript. All authors
read and approved the final manuscript.
Funding
This work was supported by JSPS KAKENHI Grant Number JP15H02426,
JP17K18926.
Availability of data and materials
The datasets analyzed in this study are not publicly available due to a privacy
policy but are available from the corresponding author on reasonable
requests.

Declarations
Ethics approval and consent to participate
The study was approved by the Ethics Committee of Kyushu University(Approval No. 231). Written informed consent was obtained from allparticipants.
Consent for publication
Not applicable.

Eto et al. Journal of Physiological Anthropology(2022) 41:42

Competing interests
The authors declare that they have no competing interests.
Author details
1
Graduate School of Integrated Frontier Sciences, Kyushu University, 4‑9‑1
Shiobaru, Minami‑ku, Fukuoka 815‑8540, Japan. 2 Department of Human
Science, Faculty of Design, Kyushu University, 4‑9‑1 Shiobaru, Minami‑ku,
Fukuoka 815‑8540, Japan. 3 Research Fellow of the Japan Society for the Pro‑
motion of Science, 4‑9‑1 Shiobaru, Minami‑ku, Fukuoka 815‑8540, Japan.
4
Department of Sleep‑Wake Disorders, National Institute of Mental Health,National Center of Neurology and Psychiatry, 4‑1‑1 Ogawa‑Higashi, Kodaira,Tokyo 187‑8553, Japan. 5 Occupational Stress and Health Management
Research Group, National Institute of Occupational Safety and Health, 6‑21‑1
Nagao, Tama‑ku, Kawasaki, Kanagawa 214‑8585, Japan. 6 Laboratory of Environ‑mental Ergonomics, Faculty of Engineering, Hokkaido University, Kita 13, Nishi
8, Kita‑ku, Sapporo, Hokkaido 060‑8628, Japan. 7 Faculty of Sport Science, Nip‑pon Sport Science University, 7‑1‑1 Fukasawa, Setagaya‑ku, Tokyo 158‑8508,
Japan.
Received: 21 August 2022 Accepted: 6 December 2022

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