Sleep Medicine 81 (2021) 410e417

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Sleep Medicine
journal homepage: www.elsevier.com/locate/sleep

Original Article

Daily light exposure, sleepewake cycle and attention in adolescents

from different urban contexts
Sabinne D. Galina a, Jane C. Souza b, Pablo Valdez c, Carolina V.M. Azevedo a, *
a
rio de Cronobiologia e Comportamento, Departamento de Fisiologia e Comportamento, Universidade Federal do Rio Grande do Norte, Brazil
Laborato
b
Faculdade de Ci^encias da Saúde do Trairí, FACISA, Universidade Federal do Rio Grande do Norte, Brazil
c
noma de Nuevo Leo
Laboratorio de Psicofisiología, Facultad de Psicología, Universidad Auto
n, Monterrey, NL, Mexico

a r t i c l e i n f o a b s t r a c t

Article history: Objective: to compare daily light exposure, activity-rest rhythm, sleepewake cycle (SWC) and attention
Received 3 December 2020 in Brazilian students living in different levels of urbanization.
Received in revised form Methods: 115 adolescents (74 girls), aged 14e18 years (mean 15.5 ± 0.7 years), from the first years of high
5 March 2021
school have participated. The SWC was evaluated by actimetry and a Sleep Diary for 10 days. Besides, the
Accepted 6 March 2021
Available online 16 March 2021
“Health and Sleep” Questionnaire, the Morningness and Eveningness Scale for adolescents, the Pitts-
burgh Sleep Quality Index, and the Pediatric Daytime Sleepiness Scale were answered. Attention was
assessed by a Continuous Performance Task.
Keywords:
Light-dark cycle
Results: In the less urbanized region, there were a greater exposure to light during the day accompanied
Light intensity by a higher proportion of morning-types and less occurrence of excessive daytime sleepiness. Otherwise,
Level of urbanization in the more urbanized region, adolescents showed a trend to sleep less in weekdays and presented more
School schedule irregularity in sleep duration between weekdays and weekend, with 83 ± 15% of sleep efficiency,
Actimetry 01:04 ± 1:30 h of WASO and 7 ± 6.7 awakenings per night on the weekdays, suggestive of poor sleep
quality. Despite of this, they showed better attentional performance: more correct responses (tonic and
phasic alertness, and sustained attention) and less omissions (for all components). Regardless of the
degree of urbanization, there was partial sleep deprivation, irregular sleep schedules and poor sleep
quality in adolescents.
Conclusions: The daily light exposure and activity-rest profiles, SWC and attention in adolescents varied
according to the degree of urbanization. Besides, the negative impacts of early school starting times
leading to sleep deprivation, irregular sleep times and poor sleep quality were observed irrespective of
the degree of urbanization, reinforcing that the early school starting time at morning is a strong temporal
challenge for teenagers, having negative impacts on cognition and academic performance.
© 2021 Elsevier B.V. All rights reserved.

1. Introduction hypothesized that the circadian process shows changes in light

One of the most striking changes in adolescence is the delayed
sleep phase [1,2] that is associated to changes in the homeostatic
and circadian processes of regulation of sleepewake cycle (SWC).
Regarding the homeostatic process, there are evidence that the
elevation of sleep pressure during waking hours is slower in
adolescence than in other phases of ontogenesis, extending the
wakefulness and delaying the onset of sleep [2,3]. Meanwhile, it is
* Corresponding author.
E-mail addresses: carolina@cb.ufrn.br, carolinavmazevedo@gmail.com
(C.V.M. Azevedo).
sensitivity during adolescence [3,4].
The presence of light at specific moments of circadian rhythms
can modulate the phase of SWC. In adolescents, less light sensitivity
is suggested in the morning [5], what attenuates the phase advance
expected at this time [4]. In contrast, unexpected results were
observed in adolescents regarding the responses to light at night,
when phase delays occur. Crowley et al. [3] observed more pro-
nounced delays in young pubescents, going in opposition to the
longer delays usually observed in more mature pubescents [1].
Thus, the delay on SWC would be due to a combination of puberal
related changes in homeostatic process, characterized by a pro-
longed wakefulness, associated to circadian responses to the
extension of exposure to artificial light at night [2,3].

https://doi.org/10.1016/j.sleep.2021.03.012
1389-9457/© 2021 Elsevier B.V. All rights reserved.
S.D. Galina, J.C. Souza, P. Valdez et al.
This pattern is observed in several countries around the world
[2e4,6,7]. In contrast, the start time of morning classes shortens
sleep length. In USA, more than 52% of high schools start classes
before 8:00 am and less than 15% at 8:30 am or later. In some
districts, school buses pick up students at 5 am, who need to get up
even earlier [8]. In Brazil, morning classes start between 7 and 7:30
am, and for students who live far from schools, waking up happens
earlier [9]. The combination of these factors affects the homeostatic
and circadian processes leading to sleep deprivation [2,6] and ir-
regularity in sleep times between weekdays and weekends [10],
respectively, characteristic of social jetlag [11]. This scenario is
associated to deficits in cognitive performance, such as in attention,
memory consolidation, learning, and in the ability to make de-
cisions [6,12]; besides, psychiatric and behavioral problems, such as
an increase in depressive symptoms, suicidal ideation, risky be-
haviors, such as the use of alcohol and drugs, involvement in
criminal activity, pregnancy and car accidents [2,6,7,11]. In the long
term, it is a risk factor for obesity, diabetes, cardiovascular prob-
lems, cancer, among others [2,13,14].
The SWC presents individual differences, related to the inter-
action between genetic and environmental factors [15]. The
expression of chronotypes, in morning, evening or intermediate-
types [16], is influenced by exposure to light and by the degree of
urbanization [17,18]. In large urban areas, which are generally well
illuminated, adolescents tend to be more evening-types than those
in darker and/or rural regions [19]. In rural areas, with no elec-
tricity, teens sleep earlier and are less sleep-deprived than those in
urban areas [20e22].
Urbanization is a widely studied geographical process, which
involves modulations in populational size, socioeconomic activity,
built environment and infrastructure [23,24]. In more urbanized
regions, there is more opportunity and diversity of jobs, education,
entertainment, culture, among other aspects [25] that influence
social interactions and lifestyle. The environmental novelties,
usually associated with densely urban environments, generates
greater activation of the brain noradrenergic system [25], pro-
moting cognitive benefits, such as attentional improvements
[26,27].
Attention is a cognitive process that allows an increase in the
capacity to respond to the environment, through the selection of
sensory information processed quickly and efficiently, generating a
specific response that can be sustained over time [28]. According to
the model proposed by Valdez et al. [29], attention is composed by
the following components: (1) tonic alertness, ability to respond to
changes in the environment; (2) phasic alertness, ability to
respond, preceded by a warning signal; (3) selective attention,
which processes specific sensory information while ignoring the
others; and (4) sustained attention, the ability to maintain the
attentional focus, which deteriorates over time. Similar to sleep,
attention is regulated by the circadian and homeostatic processes
[29].
Thus, eveningness, high degrees of urbanization and exposure
to artificial light can be negative for morning students when
associated with early school hours. These aspects can contribute to
sleep deprivation, irregularity in sleep times and daytime sleepi-
ness, which can be related to a drop in attentional processes. In this
context, the evaluation of SWC in populations in different degrees
of urbanization is important for understanding human sleep, its
natural history and the increasingly occurrence of sleep deprivation
and disorders. Although modifications on SWC are described in
different urban contexts in adolescents, the impact of the degree of
urbanization on light exposure, sleep and activity-rest patterns
associated with cognition is unknown. Thus, the aim of this study is
to compare daily light exposure, activity-rest rhythm, sleepewake
cycle and attention in Brazilian students living in different levels
411
Sleep Medicine 81 (2021) 410e417
of urbanization. From the hypothesis that these parameters vary
depending on the degree of urbanization, we expect that lower
light exposure during the day, greater light exposure and activity
levels at night, shorter sleep duration, greater sleep irregularity and
worse sleep quality and attentional performance will be observed
in adolescents living in greater urbanization context.
2. Methodology
2.1. Participants and cities studied
In this cross-sectional study, there were 115 adolescents (74
girls), aged 14e18 years (mean 15.5 ± 0.7 years) that study in pri-
vate schools in two cities in Rio Grande do Norte, a state located in
the Brazilian Northeast. Of these, 56 adolescents (37 girls) studied
in Natal (HU e high urbanization) and 59 (37 girls) in Santa Cruz (LU
e low urbanization). All participants studied in the first (juniors) or
second (sophomores) grades of high school, in the morning shift
and their classes started at 7:15 am.
The city of Natal is the capital of the state (Lat.: 05
47 04200
South, Long.: 35
120 3400 West), with the largest population
(890.480 people and only 39.988 in Santa Cruz) and demographic
density (4805.24 inhabitants/km2 and 57.33 inhabitants/km2 in
Santa Cruz - Lat.: 6
130 4600 South, Long.: 36
10 2400 West) [30].
Natal presents a higher degree of urbanization and development in
areas of human interest, such as commerce, industry, health,
entertainment and basic education, showing a lifestyle different
from the one in Santa Cruz. However, despite the differences, these
cities are characterized as university towns, encompassing students
from other regions and being urban areas in full development.
This study was approved by the Ethics Committee of the Federal
University of Rio Grande do Norte (CEP UFRN - protocol number
1,489,057 and 1,245,086).
2.2. Inclusion and exclusion criteria
There were included adolescents of both sexes from the morn-
ing shift of private schools, in the first (juniors) or second (sopho-
mores) grades of high school, who agreed to participate in the study
after providing written consent from their parents or legal guard-
ians, and themselves. Those who reported attention disorder, epi-
lepsy and/or symptoms related to anxiety were excluded, as well as
those who reported, in the food intake questionnaire, the ingestion
of substances that affect the nervous system, and consequently,
their performance in the Continuous Performance Task (CPT).
2.3. Data collection
Data collection was carried out in 2016 and consisted of
different stages. No data was collected during vacation, holidays
and school evaluation periods.
Prior to the data collection, the students were recruited in
classrooms. After the consent of parents and the assent of students,
the first stage of the study started, characterizing the sample and
applying the exclusion criteria. The following questionnaires were
applied: (1) “Health and Sleep”; (2) Morningness and Eveningness
Scale for adolescents; (3) Pittsburgh Sleep Quality Index; and (4)
Pediatric Daytime Sleepiness Scale.
The second stage, that lasted 10 consecutive days, started on
Fridays with the delivery of actigraphs and sleep diaries. In the
following week, participants performed the Continuous Perfor-
mance Task between 7:30 h - 9:30 h from Tuesdays to Fridays. One
participant at a time was directed to the room where the CPT would
be performed, without the presence of peers and with minimum
external noise. The teenager remained at rest for 5 min before the
S.D. Galina, J.C. Souza, P. Valdez et al.
CPT, a moment when the orientation to perform the task was
delivered and the Food Intake Questionnaire was filled, to appli-
cation of the exclusion criterion. It is worth noting that no partic-
ipant was excluded. The steps, the instruments used, and their
descriptions are detailed in Chart 1.
2.4. Data analysis
In order to characterize variables related to the urban context,
the economic classification, means of transportation and travel
time of students from home to school were evaluated. These vari-
ables were obtained from data collected through the "Health and
Sleep" Questionnaire. Each of the variables was compared with Chi-
square tests and Bonferroni corrections, both between urban con-
texts, between economic classifications and means of
transportation.
In order to compare the profiles of daily light exposure and
activity-rest between urban contexts, data from the actimetry was
used. The light data was transformed into a logarithm (logLux) to
normalize the sample. The levels of activity collected by actimetry
were used in its raw form from the ActStudio (Condor Instruments)
output to build the activity-rest profiles. The average of light and
activity levels were calculated for each 1 h, resulting in 24 values for
each day of week per individual that generated the profiles of daily
light exposure and activity-rest. The levels of daily light exposure
and activity-rest were compared between groups by repeated
measures ANOVA and Tukey post-hoc tests, in two ways: consid-
ering and irrespective of the days of week.
In order to assess the SWC in both urban contexts, we obtained
the following variables from actimetry analyzed by the ActStudio
program (Condor Instruments): sleep onset and wake up times,
sleep duration, time in bed, sleep latency and efficiency, night
awakenings and wake after sleep onset (WASO). For the compari-
son between variables, the repeated measures ANOVA with the
Tukey post-hoc test was used, having (1) the times of the week
(weekdays and weekend) as measures for repetition (within factors
effect) and (2) the city studied, to evaluate the between factors
effect. The irregularities for sleep onset and wake up time were
Chart 1
Characterization of the instruments used in each stage of the research.
STAGE INSTRUMENT
1 “Health and Sleep” Questionnaire
Morningness and Eveningness Scale for
adolescents
Pittsburgh Sleep Quality Index
Pediatric Daytime Sleepiness Scale
2 Sleep diary
Actigraph
Food Intake Questionnaire
Continuous Performance Task (CPT)
Sleep Medicine 81 (2021) 410e417
calculated by the standard deviation of these times obtained from
the ActStudio program. For the irregularity of sleep duration, the
average of weekdays was subtracted from weekend. The same
method was used to calculate the irregularity of time in bed. These
variables were compared using One-Way Anova.
In order to compare chronotype, sleep quality and daytime
sleepiness between the urban contexts, the scores were first
calculated from the questionnaires: Morningness and Eveningness
Scale for adolescents, the Pittsburgh Sleep Quality Index and the
Pediatric Daytime Sleepiness Scale, respectively. The percentages of
the distribution of each of the variables were compared by Chi-
square tests and Bonferroni corrections, while the average scores
were compared by One-Way Anova and Tukey post-hoc test.
The analysis of tonic and phasic alertness and selective attention
was performed using the following variables: (1) reaction time; (2)
percentage of correct answers; and (3) percentage of omissions.
While for the assessment of sustained attention: (1) general sta-
bility (standard deviation of correct answers and reaction time
throughout the task); and (2) stability throughout the task (linear
regression coefficient of the percentage of correct answers and the
reaction time during the task). The variables were compared be-
tween urban contexts by One-Way Anova and Tukey post-hoc test.
The software IBM SPSS Statistics, version 20 and Statsoft Sta-
tistica, version 8.0 were used to perform the statistical analyzes, as
well as a significance level of 5% for all tests was considered.
3. Results
Regarding the general characterization, 59 adolescents (37 girls)
aged 14e18 years (mean 15.4 ± 0.8 years) lived in the less urbanized
region (LU) while 56 aged 14e17 years (15.5 ± 0.6 years), lived in
the high urbanized region (HU). The groups showed differences in
the distribution of economic classification (c2 ¼ 76.32, p < 0.05)
and means of transportation from home to school (c2 ¼ 102.34,
p < 0.05). The less urbanized region had a lower economic level that
was reflected in the means of transportation used, since LU uses
more ‘motorcycle’ and HU more ‘car’ (Table 1). As for the travel
time, LU takes less time on the journey (LU: 6 ± 3 min and HU:
DESCRIPTION
Questions about health, sleeping habits, means and time to travel to school, and socioeconomic
status [31]. The socioeconomic level was assessed using a model adapted from that created by the
Brazilian Association of Research Companies (ABEP) [32].
It predicts the chronotype based on time preferences for performing tasks. The maximum score of
the scale is 43 (maximum morning preference) and the minimum is 10 (minimum morning
preference). The version adapted to the Brazilian population was used [33].
It evaluates sleep quality by asking questions about sleep patterns and sleep disorders or problems.
The scores can vary between 0 and 21. Scores between 0 and 5 are characterized as good sleep
quality, and above, poor sleep quality [34].
It evaluates sleepiness in everyday situations of children and adolescents. The scores range from
0 (less sleepiness) to 32 points (more sleepiness). The Brazilian version was used [35].
It is used to assess the ways of waking up and naps (occurrence, times and duration) [36,37]. Also,
the data about sleep times were used to score actimetry.
It collected data on light exposure and activity-rest, which was used as an objective measure of the
SWC. It collected at 1 min intervals. The Condor ActTrust Model actigraph (Condor Instruments)
collected data in the PIM, TAT e ZCM activity modes, in the three axes, with 12 bits of resolution and
25 Hz of sampling rate. The ActStudio program (Condor Instruments) was used to obtain the sleep
variables, according to the Cole-Kripke algorithm [38]. The sleep variables obtained with this
actigraph are very similar to those calculated with other brands of actigraphs [39]. The sleep
variables obtained from the actigraph are described in the data analysis section.
Adapted from Teixeira [40], it investigates the intake and quantity of substances that could alter the
CPT result.
Neuropsychological task. ‘1, 2 and 3’ are pressed on the numeric keypad, according to the numbers
that appear on the computer screen (0e9). ‘1’ is pressed for numbers 0e8 (indicative of tonic
alertness); the ‘2’ for number 9 (selective attention); and ‘3’ for number 4, preceded by 9 (phasic
alertness). The complete task is an indicative of sustained attention (duration ~ 12 min) [29].
412
S.D. Galina, J.C. Souza, P. Valdez et al. Sleep Medicine 81 (2021) 410e417

15 ± 9.2 min, F(1,93) ¼ 35.336, p < 0.05). On the other hand, there Table 1
were no differences between these variables according to gender Distribution of economic classification and means of transportation of adolescents
living in two urban contexts (LU: low urbanization and HU: high urbanization) (%).
(c2 ¼ 36.58, p > 0.05) and age (t(113) ¼ 0,539, p > 0.05).
The daily profiles of exposure to light (F(6,276) ¼ 0.449, Economic classification Groups (%) p
p > 0.05) and activity-rest (F(6,276) ¼ 1.081, p > 0.05 - Fig. 1A), LU HU
considering the days of the week, showed no differences between
A 13 32 <0.05
groups. Even so, there is less activity during the afternoon B1 11 17
on weekdays in LU, close to the time of the registered naps. B2 21 6
In contrast, there are differences related to the time of the C1 10 1
C2 2 0
day, irrespective of the day of week (Fig. 1B). There is greater
D-E 2 0
light exposure (F(23,276) ¼ 7.489, p < 0.001) and activity
(F(23,276) ¼ 1.758, p < 0.05) during the day in LU, while HU has Means of transportation

greater activity and exposure to light at night. Car 11.3 49.5 <0.05
Regardless of urban context, both groups start sleep Bus 0 1
On foot 6.2 3.1
(F(9,180) ¼ 2.363, p ¼ 0.01) and wake up earlier (F(9,180) ¼ 23.735,
Motorcycle 23.7 0
p < 0,001), have shorter sleep duration (F(9, 189) ¼ 7.957, p < 0.001) Other 1 4.1
and time in bed (F(9,180) ¼ 6.708, p < 0.001), greater sleep efficiency
The letters indicating the economic classification estimates the following household
(F(9,180) ¼ 11.031, p < 0.001), shorter WASO (F(9,531) ¼ 4.416, income: A: R$ 20.272,56, B1: R$ 8.695,88, B2: R$ 4.427,36, C1: R$ 2.409,01, C2: R$
p < 0.001), less nighttime awakenings (F(9,180) ¼ 3.793, p < 0.001) 1.446,24 e D-E: R$ 639,78 [32].
and a trend towards lower sleep latency (F(9,531) ¼ 1.698, p ¼ 0.08)
in the weekdays when compared with weekend.
Considering the urban context, LU presents a tendency to p < 0.05). During weekends, there are no differences between
sleeping longer (F(1,21) ¼ 3.400, p ¼ 0.07) and showed a shorter groups (Anova, p > 0.05 - Table 2).
WASO (F(1,59) ¼ 4.993, p ¼ 0.02) in the weekdays. Besides, less For the way to wake up in the weekdays, both groups most
nighttime awakenings occurred in weekdays (F(1, 59) ¼ 7,917, frequently report the use of alarm clock (LU: 42.6% and HU: 56.5%)
p ¼ 0.006) and weekend (F(1, 59) ¼ 7.689, p ¼ 0.007). These results and the need to be awakened by someone (LU: 41% and HU: 34.6%)
were accompanied by less irregularity on sleep duration between (Х2 ¼ 10.96, p ¼ 0.004). While on weekends, spontaneous awak-
weekdays and weekend (F(1,59) ¼ 4.105, p ¼ 0.04). ening predominates (LU: 64% and HU: 53.3%) (Х2 ¼ 18.97, p < 0.001).
LU presents a lower percentage of naps in the weekdays Despite of the similarity in the mean scores of chronotype (LU:
(c2 ¼ 6.71, p ¼ 0.009) and starts napping earlier (F(1,47) ¼ 4.899, 26 ± 3.7 and HU: 26.6 ± 3.6, F(1.94) ¼ 0.987, p > 0.05), LU showed a

Fig. 1. Daily profiles of light exposure and activity-rest of adolescents living in two urban contexts (LU: low urbanization and HU: high urbanization): in the days of week (A); and
mean values irrespective of the day of week, according to the times of the day (B). *Significant differences between groups for light exposure. #Differences between groups for
activity.

413
S.D. Galina, J.C. Souza, P. Valdez et al. Sleep Medicine 81 (2021) 410e417

Table 2
Sleep-wake parameters of adolescents living in two urban contexts (LU: low ur-
banization and HU: high urbanization).

Parameters LU HU p1 p2

n n

Sleep onset 45 45 <0,05

Weekdays 22:40 ± 1:15 23:02 ± 1:02 >0,05
Weekends 23:49 ± 1:15 23:56 ± 1:21 >0,05
Wake-up time 45 45 <0,05
Weekdays 06:49 ± 1:29 06:39 ± 0:40 >0,05
Weekends 08:52 ± 0:50 09:15 ± 1:29 >0,05
Duration of sleep 45 45 <0,05
Weekdays 07:11 ± 1:16 06:40 ± 1:16 ¼0,07
Weekend 07:25 ± 1:12 07:47 ± 1:48 >0,05
Time in bed 45 45 <0,05 Fig. 3. Distribution of daytime sleepiness scores of adolescents living in two urban
Weekdays 07:58 ± 1:17 07:40 ± 1:06 >0,05 contexts (LU: low urbanization and HU: high urbanization).
Weekend 09:04 ± 1:10 09:15 ± 1:44 >0,05
Irregularity of sleep 45 45 e
Sleep onset 01:08 ± 1:29 00:54 ± 1:21 >0,05 sleepiness, there are no differences between the mean scores (LU:
Wake-up 02:03 ± 1:11 02:35 ± 1:26 >0,05 18.3 ± 5 and HU: 18.2 ± 5, F(1,94) ¼ 0.020, p > 0.05). However, LU has
Duration of sleep 00:13 ± 1:12 01:06 ± 1:57 <0,05 a trend toward alertness (c2 ¼ 33.35, p < 0.05, Fig. 3) in relation to
Time in bed 01:06 ± 1:19 01:34 ± 1:40 >0,05
Sleep latency (min) 45 45 ¼0,08
HU.
Weekdays 00:08 ± 0:11 00:12 ± 0:13 >0,05 For the attention variables, LU had longer reaction times for
Weekend 00:10 ± 0:23 00:14 ± 0:18 >0,05 tonic alertness (F(1.88) ¼ 4.233, p < 0.05) and for selective attention
Sleep efficiency (%) 45 45 <0,05 (F(1.88) ¼ 3.116, p < 0.05, Fig. 4A). LU still presented a lower per-
Weekdays 91,3 ± 10,5 83 ± 15 >0,05
centage of correct responses for tonic (F(1.88) ¼ 5.231, p < 0.05) and
Weekend 81,5 ± 17,8 79,2 ± 18 >0,05
WASO 45 45 <0,05 phasic alertness (F(1.88) ¼ 9.586, p < 0.05, Fig. 4B). In addition, there
Weekdays 00:24 ± 0:36 01:04 ± 1:30 <0,05 was a higher percentage of omissions in the tonic (F(1.88) ¼ 9.018,
Weekend 01:05 ± 1:15 01:53 ± 1:47 >0,05 p < 0.05) and phasic (F(1.88) ¼ 6.467, p < 0.05) alertness and se-
Night awakenings* 45 45 <0,05 lective attention (F(1.88) ¼ 3.980, p < 0.05, Fig. 4C). As for the vari-
Weekdays 3±5 7 ± 6,7 <0,05
Weekend 4±5 9 ± 8,6 <0,05
ables of sustained attention, there was no difference between urban
Naps** 44 44 contexts in terms of stability throughout the task (F(1.88) ¼ 0.436,
Week (%) 34,8 47,7 <0,05 p > 0.05, Fig. 4D). However, there is a trend towards greater vari-
Start 13:24 ± 1:48 14:59 ± 2:54 <0,05 ability in general stability for LU (F(1.88) ¼ 3.295, p ¼ 0.07, Fig. 4E),
End 15:12 ± 2:18 16:12 ± 2:42 >0,05
meaning a lower capacity for sustained attention.
Time in bed 01:42 ± 1:12 01:24 ± 0:48 >0,05
Weekends (%) 56,5 56,8 >0,05
Start 13:18 ± 3:48 13:42 ± 2:36 >0,05 4. Discussion
End 14:48 ± 3:54 14:30 ± 2:42 >0,05
Time in bed 01:30 ± 0:42 02:24 ± 4:30 >0,05 This study compared daily light exposure, activity-rest rhythm,
p1: differences between groups; p2: differences between days of the week. sleepewake cycle, sleep quality and attention with objective
* Result given in arbitrary units. measures in Brazilian students living in different levels of urbani-
** Naps data were obtained from sleep diaries.
zation in the state of Rio Grande do Norte located in the north-
All other variables were assessed by actimetry.
eastern of Brazil. Besides, sleep quality, chronotype and daytime
trend toward morningness on the distribution of scores in the sleepiness were evaluated by subjective measures.
sample (c2 ¼ 38.48, p < 0.05 - Fig. 2). Most results were in line with predictions, with exception of
Poor sleep quality is observed in most of the sample (LU: 81.4% attentional performance. The adolescents living in the less urban-
and HU: 84%), with no differences between urban contexts in terms ized city showed greater light exposure and activity levels during
of proportion (c2 ¼ 0.49, p > 0.05) or average scores (LU: 11.1 ± 5.5 the day, with a decrease in activity close to nap times, and chro-
and HU: 11.7 ± 5.4, F(1,113) ¼ 0.657, p > 0.05). Regarding daytime notypes toward morningness. There was a tendency for longer
sleep duration in weekdays accompanied by less irregularity in
sleep duration between weekdays and weekend, WASO and num-
ber of nighttime awakenings, as well as higher levels of alertness.
However, for the components of attention, there are longer reaction
times for tonic alertness and selective attention, lower percentage
of correct responses for tonic and phasic alertness, and higher
percentage of omissions for tonic and phasic alertness and for se-
lective attention.
These results seem to be counterintuitive as sleep and attention
are related to similar brain areas, such as the ascending reticular
activator system (tonic alertness) [28,29] and the prefrontal cortex
(phasic alertness and selective and sustained attention) [41e44].
Also, reduction in duration and quality of sleep is associated with
deficits in attentional performance [45]. Thus, we suggest that the
divergence between sleep and attention observed in our results
may be related to the greater degree of urbanization of HU, as it
Fig. 2. Distribution of the observed scores of chronotype of adolescents living in two modifies attentional and cognitive processing, increasing global
urban contexts (LU: low urbanization and HU: high urbanization). processing [46] and tonic alertness [47,48].
414
S.D. Galina, J.C. Souza, P. Valdez et al.
Fig. 4. Parameters of attention components of adolescents living in two urban contexts (LU: low urbanization and HU: high urbanization): (A) reaction time; (B) percentage of
correct answers; and (C) percentage of omissions of tonic alertness, selective attention and phasic alertness. Indicators of sustained attention: (D) stability during the task (mean ±
standard error), in relation to the reaction time and percentage of correct responses; and (E) general stability of the percentage of correct answers and reaction time during the task.
*p < 0.05. #p ¼ 0.08.
In addition, light pollution in cities with high levels of urban-
ization [49,50] changes the limits between day and night [51],
negatively modulating the temporal organization of the body
[49e51] from exposure to natural and artificial light and social
activities [52]. These factors may contribute to the differences in
the expression of chronotype observed in the two regions. How-
ever, these differences were not reflected in bedtime, which was
similar between groups. In addition to the chronotype, light
pollution may be contributing to poor sleep quality in the most
urbanized city.
A National Sleep Foundation panel about sleep quality, with
experts from various fields, evaluated objective data measured by
polysomnography and actimetry and proposed that adolescents
with good sleep quality should have 85% sleep efficiency (LU:
91.33 ± 10.5 and HU: 83 ± 15 in the weekdays, decreasing at the
weekend), 51 min WASO (LU: 24 ± 36 min and HU: 01: 04 h ± 1:
30 h in the weekdays, increasing at the weekend) and no more than
3 night awakenings (LU: 3 ± 5 and HU: 7 ± 6.7 in the weekdays,
increasing at the weekend) [53]. Despite the limitation to obtain
identical sleep quality measurements using different actigraph
devices [54], both in the NSF study and in ours, we observed that
adolescents living in HU are outside the standards. Therefore, we
suggest that this group has a worse quality of sleep that may be
associated with a higher degree of urbanization, as shown in other
studies [55,56]. However, studies with different types of measure-
ments are needed to confirm this proposition.
According to Zhou et al. [57], the sleep quality of adolescents
worsens with maturity, greater use of electronics at night, early
start classes in the morning and greater load of school activities on
weekends. These aspects could have contributed to the poor sleep
quality observed in this study, particularly in HU, similar to previ-
ous studies [58,59].
Regardless of the urban context, there is a strong influencing
factor modulating the SWC in adolescents: the beginning of
415
Sleep Medicine 81 (2021) 410e417
morning classes [1,2]. This aspect might have contributed to the
earlier sleep onset and wake up times, predominance of the use of
an alarm clock and being awakened by someone during the
weekdays, shorter time in bed and sleep duration on weekdays that
was less than the 8e10 h recommended for this age group [2,4,8],
inclusive in the weekend. Comparing the urban contexts, adoles-
cents of HU shows a trend to shorter sleep duration
(06:40 h ± 1:16 h) in the weekdays than LU which may be aggra-
vated by the time of transportation to the school. In HU most of the
participants, even using a car, present travel time almost 3 times
longer than LU, hampered by low urban mobility, as observed in
populations living in large urban centers [9].
Thus, shortened and poor-quality sleep may be contributing to
the excessive daytime sleepiness [60] of the group, resulting in
prolonged sleep over weekend. This effect, well described in ado-
lescents in the morning shift [1,2], is reflected in the greater ir-
regularity of sleep duration observed in this group. These patterns
are characteristics of a rebound of sleep as a mechanism of
compensation of sleep deprivation in the weekdays. In view of
these results, we reinforce that the early start times of morning
classes is a strong social force, capable of masking or entraining
biological rhythms, being a temporal challenge for the teenager.
Studies in Brazil and abroad show similar results [1,2,61].
This context of sleep deprivation and excessive daytime sleep-
iness is reflected in the naps. In general, napping is related to
environmental, cultural, and circadian factors, being common in
tropical regions, such as the northeast of Brazil, which would
explain its occurrence in both groups. LU presents a lower per-
centage (34.8%) of naps in weekdays, which, similar to tropical and
less urbanized regions [62e64], starts earlier, as it is reported in the
sleep diary and can be seen in the activity-rest profile. On the other
hand, HU has a higher percentage of naps (47.7%) spaced
throughout the afternoon, which may be due to a shorter poor-
quality nighttime sleep.
S.D. Galina, J.C. Souza, P. Valdez et al.
This study has limitations due to the small sample size and the
lack of information on habits of electronic device usage, making
further studies necessary, with a larger number of different loca-
tions and including a media usage measurement. Despite the lim-
itations, this study was a pioneering one, that proposed to verify
relationships between daily light exposure and activity-rest
rhythm, SWC and attention of Brazilian adolescents in different
urban contexts. In addition, this study was conducted in north-
eastern Brazil. A region formed by states that underwent urbani-
zation processes at different degrees and at different times, and is
still less urbanized than the southeast region, where most studies
evaluating the relationship between the urban context and the
SWC were carried out in Brazilian adolescents [20e22]. In this way,
this work becomes innovative both as it covers a region that does
not have studies about this aspect, but also because it encompasses
and relates many variables in a subjective and objective way.
It is important to highlight that this study pointed negative ef-
fects of urbanization in the SWC of adolescents, even though ur-
banization seems to be related to positive effects on attentional
performance. Studies with adolescents in different degrees of ur-
banization, lifestyles and school start schedules are necessary to
analyze the relationships of cause and consequence among the
variables studied. This will contribute to understand the factors
that influence the SWC in adolescents contributing to the elabo-
ration of sleep hygiene courses to be developed by teachers and
health professionals; in order to raise awareness among adoles-
cents and the community that healthy sleep and healthy light
exposure can prevent damage to health. Furthermore, these studies
contribute to the elaboration of public policies that aim at a smarter
and healthier urbanization process for its inhabitants.
Funding
This work was supported by Coordenaça ~o de Aperfeiçoamento
de Pessoal de Nível Superior (CAPES e Grant #001) and Uni-
versidade Federal do Rio Grande do Norte. The content is solely the
responsibility of the authors and does not necessarily represent the
official views of CAPES.
CRediT authorship contribution statement
Sabinne D. Galina: Conceptualization, Validation, Formal anal-
ysis, Investigation, Data curation, Writing e original draft, Project
administration. Jane C. Souza: Investigation, Resources, Writing e
review & editing. Pablo Valdez: Software, Resources, Writing e
review & editing. Carolina V.M. Azevedo: Conceptualization,
Methodology, Resources, Data curation, Writing e review & editing,
Supervision, Project administration, Funding acquisition.
Acknowledgment
We are grateful for the collaboration and support of the school's
teaching teams, and especially the students who agreed to partic-
ipate in this research. Also, we would like to thank Dr. Fernando
Louzada and Dr. John Araújo for their valuable suggestions. We
wish to acknowledge the help provided by Dayanne Medeiros,
Edileusa Leal, Emmanuelle Pereira, Juliana de Lima, Karlyne dos
Anjos e Xaize Lopes on data collection.
Conflict of interest
None declared.
The ICMJE Uniform Disclosure Form for Potential Conflicts of
Interest associated with this article can be viewed by clicking on the
following link: https://doi.org/10.1016/j.sleep.2021.03.012.
416
Sleep Medicine 81 (2021) 410e417
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