leptin - circadian rhythms - electronic device - screen time - obesity
INTRODUCTION
A decline in average sleep duration and quality has been reported over the past few
decades[1], contributing to numerous chronic diseases including obesity[2]. Poor sleep can lead to increased feelings of hunger and subsequent increases in
food portion sizes[3] as well as poor food choices[4]
,
[5]. Indeed, in Western societies, where chronic sleep deprivation has become common
and food is widely available, changes in appetite regulatory hormones (leptin and
ghrelin) associated with poor sleep may contribute to obesity[6]. One factor strongly implicated in the decline of sleep quality and quantity in
modern society is the use of light-emitting electronic devices (televisions, smartphones,
computers, etc.) at night and specifically during the hours before sleep[7]. In particular, self-luminous displays that emit high levels of short-wave-length
(blue) light seem to cause significant circadian disruptions[7].
A representative survey of 1,508 American adults revealed that 90% of Americans used
some type of electronics at least a few nights per week within 1 hour of bedtime[8]. Adolescents (13-18 y) and young adults (19-29 y) were the highest users of smart-phones
in the hour before bed, with 72% and 67% of the surveyed population reporting use
of these devices, respectively. Exposure to light-emitting devices has been shown
to suppress the release of the sleep-facilitating hormone melatonin[7]
,
[9]
,
[10], which causes a shift to the circadian clock making it difficult to fall asleep
and reducing sleep quality and quantity[11]
,
[12]. Chang et al. (2015) reported that, compared with reading a printed book, reading
on an electronic device in the four hours before bedtime for five consecutive nights
suppressed the late evening rise of pineal melatonin secretion, decreased subjective
sleepiness, lengthened sleep latency; sleep propensity and impaired morning alertness[12].
Light has an impact on hormone production through stimulation of the suprachiasmatic
nuclei. Sensitivity to the light from the retina in our eyes to the suprachiasmatic
nuclei are the major circadian synchronizer of human daily biological rhythms. Pilot
research has shown that blue-enriched light exposure immediately before and during
the evening meal acutely increases hunger and alters metabolism in comparison to dim
light[13]. Night time exposures to certain light levels and spectra will reduce or impair
the production of melatonin[14]. In humans, nocturnal melatonin suppression is maximally sensitive to short-wavelength
(blue) light peaking close to 460 nanometers (nm)[15]. Changes in melatonin have also been linked to perturbations in a hormone related
to satiety - leptin[16]. Leptin plays a key role in food intake inhibition, body weight regulation and energy
homeostasis[17], where it provides information about the state of fat stores to the brain, and the
neurodendocrine systems adapt their function to the current state of energy homeostasis
and fat stores[18]. Melatonin is involved in leptin synthesis and release by adipose tissues[19] and its absence is related to metabolic syndrome, diabetes, and increased body weight[20]. While the relationship between melatonin suppression and the use of electronic
devices are well understood, the direct link between electronic device use and leptin
is yet to be established in healthy, non-sleep-restricted humans.
Recent technological advancements have attempted to reduce the potential negative
impact of short-wavelength blue-light by adjusting the spectral composition of self-luminous
displays. Apple Inc. released a function called 'Night Shift' on their e-devices in
2016, which proposed to filter the blue-light wave-length emitted by the devices at
night, thereby improving sleep. To the authors' knowledge, only one study has investigated
the efficacy of the Night Shift feature. Nagare et al. (2017) compared two different
Night Shift modes (low and high correlated color temperature) with a dim-light control
(wearing orange goggles) and a blue-light intervention for melatonin suppression in
12 participants[17]. The results from their study showed that both Night Shift modes suppressed melatonin
significantly more than the control trial, but significantly less than the blue-light
trial. The authors also reported no difference between the two Night Shift modes and
suggested that future research should investigate the impact that this feature may
have on sleep and other factors associated with sleep. The study did not measure sleep
and failed to include a condition where the Night Shift feature was turned off.
Therefore, the aim of the current study was to examine the acute effect of 1-hour
of night-time iPad use with and without the Night Shift feature turned on, compared
to a control trial using a printed hard-copy book. Perceived tiredness, hunger levels,
salivary leptin and sleep (via wrist-actigraphy and perceived ratings of sleep duration
and quality) were measured in healthy young adults.
MATERIALS AND METHODS
Participants
Thirteen healthy young adults (6 male/7 female, age; 29 ± 5 y) volunteered to take
part in the study. All participants were free of any diagnosed sleep disorders and
were required to have a Pittsburg Sleep Quality Index global score of < 7 (mean ±
SD; 4.4 ± 1.8). Participants with chronic medical or psychological conditions or sleep
disorders and those taking prescription sleep medications were excluded from the study.
During the study, participants were also asked to sleep alone (no bed-partners) and
parents with children under 2-years of age were excluded from taking part in the study.
Ethical approval for the study was obtained through the institution's Human Research
Ethics Committee.
Study Design
In a randomized, crossover design, participants performed three experimental trials,
each separated by five to seven days. For two of the trials, participants were required
to read an e-book on an electronic device (9.7" iPad Pro, Apple Inc. Cupertino, CA,
USA) held at a standardised angle ~30 cm from eyes (as enforced by the researchers)
either with the Night Shift feature turned on (iPad+NS) or off (iPad), with the same
brightness settings (full warmness/brightness). A third trial involved participants
reading the same book as a hard-copy paperback (CON). The order of the trials was
counterbalanced between the participants. All trials involved reading the same self-help
book ("How to win friends and influence people" by Dale Carnegie) for one hour in a dimmed room, with just one table-lamp as the
only light source. Reading took place for the hour leading up to each participants
habitual bedtime (as identified by the Pittsburg Sleep Quality Index), while participants
remained in a seated position. The photopic lux of the room was measured in the same
position across the three trials using a Digitech QM1587 light meter. The spectrometry
and wave-length of the light emitted by the iPad (with and without Night Shift) is
reported using methods and techniques described previously[21] via the online tool found at fluxometer.com. Based on these methods, the spectral
power of both the iPad and iPad+NS is further detailed in [Table 1] and [Figure 1] below.
Figure 1 The relative spectral power distributions for the two interventions in the current
study as described by Lucas et al.[21] Thick black line represents iPad condition and dashed line represents iPad+NS condition.
Table 1
Calculations of five α-opic irradiances for experimental conditions (iPad+NS and iPad),
following the SI-compliant approach recommended by the International Commission on
Illumination.
|
Intervention
|
Cyanopic irradiance (µWcm[2])
|
Melanopic irradiance (µWcm[2])
|
Rhodopic irradiance (µWcm[2])
|
Chloropic irradiance (µWcm[2])
|
Erythopic irradiance (µWcm[2])
|
|
iPad+NS
|
3.46
|
6.04
|
8.38
|
11.3
|
13.1
|
|
iPad
|
9.43
|
12.2
|
15.0
|
17.3
|
18.0
|
To control for dietary variables, participants recorded their meals using a 24-hour
diet diary for the day of the first testing session and were instructed to replicate
their diet for the subsequent testing sessions. Participants were to refrain from
any vigorous physical activity and alcohol consumption on the day of testing and caffeine
consumption after 12pm. Participants were required to have dinner 3.5 hours before
their habitual bedtime. Following dinner, participants were allowed to only drink
water until up to 30 minutes before 'reading time' (i.e., one hour before bedtime)
in order to guarantee good quality of saliva samples.
Sleep monitoring
Participants were required to wear a wrist actigraphy device (Readiband(tm), Fatigue
Science, Vancouver) on either the dominant or non-dominant wrist[22] for the experimental trials. Participants were instructed to leave the actigraphy
devices on at all times during the study. The Readiband has been validated against
PSG, with accuracy levels of up to 93% being reported[23]
,
[24] and research from our laboratory has also shown that the Readiband results are in
acceptable levels of inter-device reliability (ICC = >0.90)[25]. At the conclusion of the recording period, actigraphy data were wirelessly downloaded
to a computer, which was then analysed using Fatigue Science software (16Hz sampling
rate: Readiband(tm), Fatigue Science, Vancouver). The raw activity scores were translated
to sleep-wake scores based on computerized scoring algorithms. Sleep indices including
total sleep time, sleep latency, sleep onset time and wake time were used to assess
sleep variables.
Hormonal measures
Whole saliva samples were collected pre and post the 1-hour reading intervention during
all three trials (iPad+NS, iPad and CON). Participants expectorated a sample via passive
drool into a 50-mL polyethylene tube, which was stored at -20°C until assayed. On
the day of testing, saliva samples were thawed to room temperature and centrifuged
at 3000 rpm for 15 minutes to remove mucins. Leptin concentrations were determined
using saliva from the upper phase of the centrifuged samples in duplicate using commercially
available enzyme-linked immunosorbent assay kits (ELH-LEPTIN, RayBio, USA) as per
the manufacturer's instructions. Leptin assay sensitivity was 2 Archie11 pg.mL-1 with intra-assay variation (calculated from the saliva samples of between 25.8 and
32.0% and an inter-assay CV (calculated from the standards) of between 2.4 and 13.0%.
Saliva samples for each participant were analyzed on the same assay plate to eliminate
the possibility of inter-assay variance.
Perceived hunger and tiredness measures
At various time points (pre, post and next morning), perceptual measures of hunger
and tiredness were given by participants. The perceived hunger scale consisted of
one-item (i.e., How hungry are you feeling right now) that was rated on a Likert-style
scale ranging from 'so full you feel sick'[1] to 'starving and feeling weak/dizzy'[10]. Similarly, the perceived tiredness scale also consisted of one item (i.e., How
tired are you feeling right now) that was rated on a Likert-style scale ranging from
'not at all'[1] to 'extremely'[10].
Pittsburg Sleep Quality Index (PSQI)
The PSQI is a self-rated 19-item instrument intended to assess sleep quality and sleep
disturbance in clinical and nonclinical populations[26]. Global scores range from 0 to 21 with higher scores indicating poorer overall sleep
quality. The PSQI has been demonstrated to have good internal reliability, validity
and is perhaps the most commonly-used subjective sleep measure not only in the research
literature, but also in the sleep community[26].
Statistical Analysis
Simple descriptive scores are shown as means ± standard deviations unless stated otherwise.
Statistical analyses were performed using the Statistical Package for Social Science
(V. 22.0, SPSS Inc., Chicago, IL), with statistical significance set at p < 0.05. One-way repeated measures analyses of variance (ANOVA) were performed to
determine the effect of different treatments (iPad+NS, iPad, CON) on sleep measures.
Two-way repeated measures ANOVAs (treatment x time) were performed on leptin and perceived
tiredness and hunger variables. There were no outliers in the data, as assessed by
visual inspection of a boxplot and all data was normally distributed, as determined
by Shapiro-Wilk's test (p > 0.05). There was homogeneity of variances, as assessed by Levene's test for equality
of variances. Where significance was found, comparisons were performed using Tukey's
post-hoc analysis. When sphericity was violated, Greenhouse-Geisser corrections were
used. Magnitudes of the standardized effects between treatments were calculated using
Cohen's d and interpreted using thresholds of 0.2, 0.6, 1.2 and 2.0 for small, moderate, large and very large effect sizes, respectively 27. An effect size of < 0.2 was considered to be trivial and the effect was deemed unclear if its 90% confidence interval overlapped the thresholds for both small positive and negative effects[28].
RESULTS
There were no significant differences between trials for photopic lux in the rooms
where testing took place (p > 0.05).
The results revealed no significant differences between the three experimental trials
(p > 0.05) for any of the outcome variables ([Table 2] and [Table 3]).
Table 2
Mean ± SD values for perceived and measured sleep variables, perceived tiredness and
measured hormonal and hunger variables for the three interventions (iPad+NS, iPad,
CON).
|
|
iPad+NS
|
iPad
|
CON
|
|
Perceived Sleep Duration (h:mm)
|
7:19 ± 0:54
|
6:57 ± 1:14
|
7:28 ± 0:49
|
|
Perceived Sleep Quality (/10)
|
6.6 ± 1.8
|
5.6 ± 2.3
|
7.3 ± 1.7
|
|
Pre-Post Δ Tiredness (/10)
|
1.9 ± 1.2
|
0.6 ± 1.9
|
1.5 ± 2.2
|
|
Next morning Tiredness (/10)
|
4.1 ± 1.9
|
4.5 ± 2.3
|
3.2 ± 1.7
|
|
Total Sleep Time (h:mm)
|
7:09 ± 0:45
|
7:31 ± 0:22
|
7:36 ± 0:26
|
|
Sleep Latency (h:mm)
|
0:35 ± 0:37
|
0:36 ± 0:39
|
0:23 ± 0:26
|
|
Sleep Onset Time (time of day)
|
23:12 ± 0:26
|
23:10 ± 0:37
|
23:06 ± 0:32
|
|
Wake Time (time of day)
|
6:57 ± 0:22
|
7:00 ± 0:33
|
7:00 ± 0:32
|
|
Pre-Post Δ Hunger (/10)
|
0.6 ± 0.7
|
0.5 ± 1.0
|
0.3 ± 0.5
|
|
Next Morning Hunger (/10)
|
6.0 ± 0.4
|
6.2 ± 0.7
|
6.1 ± 0.8
|
|
Leptin Pre (pg.mL-1
|
2.263 ± 1.113
|
2.976 ± 2.079
|
2.584 ± 1.431
|
|
Leptin Post (pg.mL-1
|
3.059 ± 1.450
|
2.752 ± 1.118
|
3.446 ± 1.157
|
|
Pre-Post Δ Leptin (pg.mL-1
|
0.796 ± 1.807
|
-0.224 ± 1.228
|
0.861 ± 2.008
|
Table 3
Comparison between interventions (iPad+NS, iPad and CON) for measured sleep and hunger
variables. Data presented as raw difference in values (mean ±90% confidence intervals)
with effect sizes for comparison between experimental trials.
|
|
iPad+NS - iPad mean ± 90%CI (effect size)
|
iPad+NS - CON mean ± 90%CI (effect size)
|
iPad - CON mean ± 90% CI (effect size)
|
|
Perceived Sleep Duration (h:mm)
|
0:22 ± 0:22 0.28 ± 0.28
Small
|
-0:09 ± 0:21 -0.11 ± 0.27
Trivial
|
-0:31 ± 0:26 -0.39 ± 0.33
Small
|
|
Perceived Sleep Quality (/10)
|
0.9 ± 1.4 0.37 ± 0.56
Small
|
-0.7 ± 1.1 -0.29 ± 0.45
Small
|
-1.6 ± 1.0 0.66 ± 0.41
Moderate
|
|
Pre-Post Tiredness (/10)
|
1.3 ± 1.2 0.73 ± 0.67
Moderate
|
0.5 ± 0.7 0.38 ± 0.57
Small
|
0.8 ± 1.7 0.44 ± 0.88
Unclear
|
|
Next Morning Tiredness (/10)
|
-0.5 ± 1.6 -0.19 ± 0.67
Unclear
|
0.8 ± 0.8 0.35 ± 0.33
Small
|
1.3 ± 1.5 0.53 ± 0.61
Small
|
|
Total Sleep Time (h:mm)
|
-0:23 ± 0:25 -0.96 ± 1.04
Moderate
|
-0:27 ± 0:27 -1.15 ± 1.15
Moderate
|
-0:05 ± 0:16 -0.19 ± 0.67
Unclear
|
|
Sleep Latency (mins)
|
-0:01 0:21 -0.03 ± 0.48
Unclear
|
0:12 ± 18 0.27 ± 0.42
Small
|
0:13 ± 0:23 0.31 ± 0.54
Unclear
|
|
Pre-Post Δ Hunger (/10)
|
-0.1 ± 0.6 -0.09 ± 0.67
Unclear
|
-0.3 ± 0.4 -0.43 ± 0.59
Small
|
-0.2 ± 0.6 -0.27 ± 0.68
Unclear
|
|
Pre-Post Δ Leptin (pg.mL-1
|
1.020 ± 1.118 0.77 ± 0.85
Moderate
|
-0.065 ± 1.745 -0.05 ± 1.30
Unclear
|
1.086 ± 1.249 0.90 ± 1.03
Moderate
|
Effect size analysis ([Table 3]) revealed small to moderate effects between trials for perceived sleep quality, with CON (7.3 ± 1.7) having the
highest value when compared to iPad+NS (6.6 ± 1.8, d = 0.29) and iPad (5.6 ± 2.3,
d = 0.66). Although these findings for perceived sleep quality were not statistically
significant, the repeated measures ANOVA revealed an interaction effect that approached
significance, F
2,20 = 3.13, p = 0.066, with participants reporting higher sleep quality after reading a hard-copy
book than reading from an iPad (p = 0.046). There were moderate effects associated with iPad+NS when compared to iPad (d = 0.77) and for iPad compared
to CON (d = 0.90) for pre-post change in leptin concentration ([Figure 2]).
Figure 2 Bar graph represents the pre to post change in salivary leptin concentration (primary
axis) across the three interventions (iPad, iPad+NS and CON) and line graph represents
the perceived sleep quality (secondary axis) following each intervention. Error bars
represent standard deviations.
DISCUSSION
The main findings from the current study indicate that when the blue-light filtering
'Night Shift' feature is turned off, iPad use at night may result in moderate but not statistically significant (p > 0.05) suppression of leptin levels and impaired sleep quality in healthy young
adults when compared to reading a hard-copy book. When the Night Shift feature is
turned on, there is a small difference in sleep quality and tiredness measures in favour of the control trial
and an unclear difference in the change in leptin concentration when compared to the control. To
the authors' knowledge, this is the first study to evaluate the sleep and hunger responses
to the Night Shift feature on the iPad. The findings from this study have established
a somewhat novel link between electronic device use at night and trends towards affected
leptin and sleep responses that warrant further investigation.
The trends toward decreased leptin levels in the iPad intervention when compared to
both the control and the Night Shift interventions indicate that individuals were
more likely to feel hungry after higher levels of blue-light exposure. Interestingly,
the control and Night Shift trials showed increases in pre to post leptin concentrations,
indicating that appetite was further suppressed after the one-hour intervention. This
may be in response to the participants consuming food ~2 hours prior to the start
of the intervention, which is consistent with previous research showing that circulating
leptin levels peak ~4 hours post feeding[29]. In contrast, there was a slight decrease in pre to post leptin levels for the iPad
trial, suggesting that the use of the lit device may have led to suppression of leptin
levels, usually meaning an increase in ghrelin levels[5], and therefore, increased hunger. The pathways through which light might modulate
leptin concentrations are not known, however, previous research has also shown that
light exposure in the morning can influence leptin and ghrelin concentrations in sleep-restricted
individuals[15]. As leptin is the key hormone in regulating food intake inhibition, continuous suppression
of leptin following electronic device use might have significant long-term consequences
on weight control and may contribute to obesity in a chronic setting.
The differences in leptin concentrations between interventions do not necessarily
reflect the perceived hunger levels in the current study. There were no significant
differences between conditions for perceived hunger at any time point (pre and post
intervention and next morning). However, unlike leptin, satiety levels peak soon after
feeding (< 1 hour)[30] and it is possible that the length of the light intervention in the current study
(1 hour) was not long enough to cause perturbations in perceived hunger levels. Previous
pilot research has suggested that blue-light enriched exposure (260 lux for three
hours) before the evening meal in 10 healthy adults, resulted in increased feelings
of hunger for up to two hours following the meal, when compared to a dim-light control[13].
Night time iPad use had a moderate effect on subjective perception of sleep quality, suggesting that after reading from
an iPad compared to reading a hard copy book, participants felt that they slept worse.
Insufficient or low-quality sleep has been shown to have deleterious effects on mental
and physical health and cognitive performance[31]. Notably, poor sleep has also been associated with reduced leptin and increased
body mass index[6]. Continuous use of blue-light emitting electronic devices prior to sleep is, therefore,
likely to contribute not only to sleep problems but also to a range of different health
outcomes[20].
There were no significant differences between groups for any of the sleep measures
identified via wrist actigraphy. However, moderate differences were found for total sleep time between the iPad+NS intervention and
both iPad and control interventions, with the iPad+NS intervention resulting in the
least sleep time. Sleep latency was the lowest in the control trial (26 minutes) compared
to both iPad+NS and iPad trials (35 and 36 minutes, respectively), with a small effect size between iPad+NS and CON. These results are not surprising, with previous
research suggesting longer times to fall asleep following electronic device use[14].
Alongside the minimal differences between trials for any of the objective sleep measures,
there were small trends towards increased tiredness the following morning after both iPad interventions,
when compared to the control. There were also moderate differences between iPad interventions for pre to post tiredness ratings, with iPad+NS
associated with greater increases in tiredness compared to iPad. This would support
previous research, suggesting that blue-light enriched exposure will reduce feelings
of tiredness[32], however, interestingly, in the current study there was an unclear difference between iPad and control trials for tiredness.
Future research would benefit from monitoring the effect of night time electronic
device use on sleep over longer periods of time (e.g. multiple weeks) with longer
exposure to the device each night (e.g. > 90 minutes). One study involving 13 young
adult participants showed that the night-time (23:00 to 01:00) use of iPad devices
suppressed melatonin by 7% and 23% following one-hour and two-hour exposures, respectively[33]. This would suggest that perhaps the one-hour exposure implemented in the current
study, on one single occasion, was not long enough to elicit significant responses
in any of our measures, despite the trends observed.
Further research is also required comparing blue-light filtering applications on devices
and blue-light blocking sunglasses for melatonin and sleep responses. Indeed, orange-tinted,
blue-light reducing sunglasses (blue-blockers) have been shown to have a positive
impact on preventing melatonin suppression when using lit devices[34], and also subsequent sleep[14]. The current study did not measure melatonin, which is the key sleep-facilitating
hormone. As melatonin has been associated with both night time electronic device use[17] and leptin[35], future studies should investigate the potential mediating effect of melatonin on
the relationship between night time electronic device use and leptin. While melatonin
measures in saliva have been well validated in the literature[36]
,
[37], future research should consider the use of blood samples to evaluate leptin levels,
for possible issues related to accuracy. It is acknowledged that when using the leptin
plate standards in the current study, the inter-assay CV across plates was calculated
at between 2 and 13% and, for saliva samples, the intra-assay CV was somewhat higher,
at between 26 and 32%. The relatively high CV indicates that the saliva is a difficult
matrix and the ELISA kit was operating near its detection sensitivity threshold. Therefore,
it is suggested that interpretation of the leptin data should be treated with caution,
and future research should consider using blood-plasma sampling as a more accurate
assessment of leptin levels.
In conclusion, based on the current study and previous related research, the use of
electronic devices at night may result in trends towards suppression of leptin levels
and impaired sleep quality, with negligible differences associated with whether or
not the 'Night Shift' feature on the iPad is initiated or not. This research has important
implications for the potential link between electronic device use at night and obesity
rates in young adults, however further research is required to expand on these findings
in a chronic setting, with additional plasma hormonal measures (leptin, ghrelin and
melatonin), greater sample sizes and greater exposure durations to blue-light.