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S1389-9457(16)30030-2
http://dx.doi.org/doi: 10.1016/j.sleep.2016.04.008
SLEEP 3051
To appear in:
Sleep Medicine
Received date:
Revised date:
Accepted date:
25-12-2015
25-4-2016
29-4-2016
Please cite this article as: Wakako Ito, Yoko Komada, Isa Okajima, Yuichi Inoue, Excessive
daytime sleepiness in adults with possible attention deficit/hyperactivity disorder (ADHD): a
web-based cross-sectional study, Sleep Medicine (2016), http://dx.doi.org/doi:
10.1016/j.sleep.2016.04.008.
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service
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Highlights
a common mechanism.
1
Page 1 of 26
ABSTRACT
Objective: Arousal dysregulation has been speculated to be involved in the pathological
mechanism of attention deficit/hyperactivity disorder (ADHD). However, there has been
no epidemiological study assessing the real condition of excessive daytime sleepiness
(EDS) in adults with ADHD. This study investigated the prevalence of EDS and the
relationship between sleepiness and ADHD symptoms in adults with possible ADHD.
Methods: An observational, cross-sectional, web-based study was performed.
Participants were 9822 Japanese adults aged 2069 years who completed an
internet-based questionnaire that assessed ADHD symptoms, autistic traits, depressive
symptoms, chronotype, sleepiness, and sleep disturbances.
Results: Participants with possible ADHD were more likely than non-ADHD participants to
have an evening chronotype and experience depressive symptoms, sleepiness, and
sleep disturbances. The rates of having moderate and severe sleepiness in the possible
ADHD group were higher than those in the non-ADHD group. Hierarchical logistic
regression analyses revealed that the presence of ADHD symptoms was independently
associated with EDS even after adjusting for factors related to the presence of sleepiness.
When examining inattention and hyperactivity scores among participants with possible
ADHD, the inattention score was significantly higher in the severe EDS group compared
with the moderate and non-EDS groups.
Conclusions: EDS was relatively common in adults with possible ADHD. ADHD
symptoms, especially inattentiveness, were associated with the formation of EDS in this
population.
Keywords:
ADHD
Excessive daytime sleepiness
Page 2 of 26
Sleep disturbances
Adult ADHD Self-Report Scale
Inattention
Hypoarousal
1. Introduction
Attention-deficit/hyperactivity
disorder
(ADHD),
characterized
by
inattention,
Page 3 of 26
problems or EDS in adults with ADHD [14,15], and it is unclear whether these sleep-related
problems are as common in the adult ADHD population as they are in children affected with
the disorder. Furthermore, EDS is sometimes caused by insufficient sleep or the delay of
sleep phase [16]. However, little is known about the prevalence of these sleep problems and
their relationship to EDS in individuals affected with ADHD.
Recently, the consensus working group of sleep medicine and ADHD suggested that
the association between hypoarousal and sleepiness in ADHD is one of the major research
areas in this field, and that arousal dysregulation is possibly involved in the pathological
mechanism of attention in the disorder [17]. Given this proposition, one might expect that
ADHD, especially inattentive symptoms, would be related to EDS. However, few studies
have systematically investigated the etiology of ADHD from the viewpoint of hypoarousal
and/or sleepiness. Most of the data on this clinical issue has been based on small clinical
samples. In this regard, an epidemiologic study on the general population would be
advantageous for assessing the relationship between EDS and ADHD symptoms.
Considering the above previous reports on the association between EDS and ADHD,
we hypothesized that adults with ADHD would demonstrate EDS irrespective of the
presence/absence of nocturnal sleep problems, and that inattentive symptoms in particular
would be associated with EDS. To test this hypothesis, we conducted a web-based survey
on a large sample of Japanese adults from the general population. In the present study, we
(1) assessed the prevalence and severity of EDS in adults with symptoms of ADHD, (2)
investigated factors associated with EDS, and (3) identified whether severity of sleepiness
was related to inattention or hyperactive symptoms in this population.
2. Method
2.1. Participants
Page 4 of 26
The study protocol was approved by the Ethics Committee of the Institute of
Neuropsychiatry, Tokyo, Japan. This was a web-based, cross-sectional study that recruited
the participants via Rakuten Research Inc., an online marketing research company that
holds approximately 2.3 million Japanese enrollments. The survey was conducted in
February 2015. An e-mail containing a link to an online questionnaire was randomly sent by
the research company to individuals throughout Japan who were stratified by district, gender,
and age. Participants ages ranged from 20 to 69 years. An informed consent form was
provided to participants via the survey website. We received 10,000 completed
questionnaires; however, questionnaires were not used if data were missing. As a result,
data from 9822 questionnaires were used in the analyses.
2.2. Assessments
Questionnaires consisted of demographic questions, the Adult ADHD Self-Report
Scale (ASRS-V1.1) for estimating ADHD symptoms, the Autism Spectrum Quotient
Japanese version (AQ) for quantifying autistic traits, the Japanese version of the Epworth
Sleepiness Scale (JESS) for assessing subjective sleepiness, the Diurnal Type Scale (DTS)
for estimating chronotypes, the 12-item version of the Center for Epidemiological
Studies-Depression Scale (CES-D ) for estimating depressive symptoms, and the Japanese
version of the Pittsburgh Sleep Quality Index (PSQI) for assessing sleep disturbances.
2.2.1. Demographic questionnaire. Participants provided answers related to their
gender, age, height, weight, occupation (regular worker, part-time worker, student,
inoccupation), family constitution (Do you currently live alone or with your family?),
smoking status (Do you currently smoke?), habitual alcohol ingestion (Do you drink
alcohol habitually?), and the presence/absence of currently treated diseases.
2.2.2. ASRS-V1.1. In this study, we used the ASRS-V1.1 for the screening of possible
ADHD. The ASRS was developed by the World Health Organization and has been widely
used in epidemiological studies on ADHD [18,19]. The six-item ASRS-V1.1 was designed as
Page 5 of 26
a tool for screening of ADHD in adults (aged 18 years and older) based on the diagnostic
criteria of the DSM--TR [18]. This scale is a standardized and well-validated tool for
assessment of current ADHD symptoms [18,20]. Each item requires participants to indicate
how often a particular symptom has occurred over the past six months on a 5-point Likert
scale from 0 = never to 4 = very often. The total score is summed and can range from 0 to
24. Based on the classification criteria recommended by Kessler et al. [20], participants in
this study were classified as possible ADHD if their ASRS score was 14 and non-ADHD
if the ASRS score was <14. We also used the sum of the first four items of the ASRS relating
to inattention symptoms for the Inattention Score and the sum of the last two items relating
to hyperactivity symptoms as the Hyperactive Score [21].
2.2.3. AQ. The AQ is widely used to quantify autistic traits [22,23]. The measure
consists of 50 items that are responded to on a 4-point Likert scale with definitely agree,
slightly agree, slightly disagree, and definitely disagree.
2.2.4. JESS. The JESS was used to measure subjective sleepiness and consists of
eight items regarding the likelihood of falling asleep in sedentary situations [24]. Response
options range from 0 (never) to 3 (high chance). In this study, a score of 11 was
considered as having EDS. Furthermore, total ESS score was used to categorize
respondents into without EDS (ESS < 11), moderate EDS (11 ESS < 16), or severe
EDS (16 ESS) according to a previous study [25].
2.2.5. DTS. The DTS was developed by Torsvall and Akerstedt (1980) to estimate
chronotypes [26]. The scale consists of seven items, such as When would you prefer to rise
if you were totally free to arrange your time? Scores range from 7 to 28, with higher scores
indicating a preference for morningness.
2.2.6. CES-D. The 12-item version of the CES-D, which is commonly used in
epidemiological studies [27,28], was used to measure depressive symptoms. Items are
Page 6 of 26
2.3. Statistics
First, we compared demographic variables, and scores on the ASRS, AQ, and
CES-D between the possible ADHD group and non-ADHD group using the unpaired t-test
for continuous variables and Pearson Chi-square test for categorical variables. The
sleep-related variables (scores on the ESS, PSQI, sleep duration, midpoint time and DTS)
were compared using the unpaired t-test, and distribution of ESS severity categories (no
sleepiness, moderate sleepiness, severe sleepiness) was compared between the two
groups using the Chi-square test. Second, we conducted hierarchical logistic regression
analyses to identify factors associated with EDS. In order to investigate whether the
association changes after adjusting for specific variables, the following variables were put
into the models in the described order. In model 1, only the presence/absence of possible
ADHD was set as an explanatory variable. Model 2 was adjusted for demographic
variables, including gender, age, body mass index (BMI), occupation (regular worker,
part-time worker, student, inoccupation), living alone (yes/no), current smoker (yes/no),
habitual alcohol ingestion (yes/no), and currently treated disease (yes/no), in addition to
Page 7 of 26
the presence/absence of possible ADHD. Model 3 was adjusted for AQ scores and DTS
scores in addition to the variables in model 2. Before the analysis, we examined Pearson
product-moment correlation coefficients for diurnal type and midpoint on weekends
because these parameters are likely to cause a problem of multicollinearity. The correlation
was r = 0.566 (p<0.001). To avoid the problem of multicollinearity, only DTS scores were
used to represent the circadian rhythm variable. In model 4, continuous variables including
PSQI scores and CES-D scores were entered in addition to the variables in model 3.
Finally, in order to explore the effect of ADHD symptoms on the severity of EDS, inattention
scores and hyperactivity scores were compared among the three EDS severity groups with
a one-way analysis of covariance (ANCOVA) followed by Bonferroni post hoc test. In this
analysis, DTS scores and PSQI total scores were set as covariates. We used SPSS
statistics version 19 (SPSS Japan, Inc., Tokyo, Japan) to conduct all analyses. A p-value of
less than 0.05 was considered statistically significant. Effect size was measured with
Cohen's d, , Cramers V, or 2. Typically, Cohens d-values of 0.2 or below reflect a small
effect size, around 0.50 reflect a moderate effect size, and 0.80 and above reflect a large
effect size [31]. Cramers V and values of 0.1 or below reflect a small effect size, around
0.3 reflect a moderate effect size, and 0.5 and above reflect a large effect size. A 2 value of
0.01 is considered a small effect size, around 0.06 represents a moderate effect size, and
0.14 is considered a large effect size.
3. Results
Table 1 shows the descriptive statistics for the total sample and the groups stratified
by the presence/absence of possible ADHD. The number of individuals with possible
ADHD based on ASRS scores was 602 (6.1%), and the number of non-ADHD individuals
was 9,220 (93.9%). There were significant differences between the two groups with regard
to gender (2 (1) = 14.2, = 0.04, p<0.001), age (t (5764) = 14.7, Cohen's d = 0.70,
Page 8 of 26
p<0.001), ASRS score (t (5200) = 23.6, Cohen's d = 2.72, p<0.001), AQ score (t (5575) =
13.1, Cohen's d = 0.84, p<0.001), CES-D score (t (4518) = 17.7, Cohen's d = 1.33,
p<0.001), and percentage of participants living alone (2 (1) = 22.4, = 0.05, p<0.001).
The effect sizes for age and scores on the ASRS, AQ, and CES-D were large. Chi-square
test and rest-error test revealed that there were significant differences between possible
ADHD and non-ADHD groups in occupation status (2 (4) = 83.6, Cramers V = 0.09,
p<0.001) with regard to regular workers (59.6% vs 55.2%, p<0.05), students (7.0% vs 2.1%,
p<0.01), and inoccupation (20.3% vs 28.8%, p<0.01). Meanwhile, there were no significant
differences in BMI (t (668) = 1.143, Cohen's d = 0.05, p= 0.25), and in the number of
smokers (2 (1) = 2.18, =0.02, p= 0.14), individuals with habitual drinking (2 (1) =1.72,
= 0.01, p= 0.19), and individuals having disease currently treated (2 (1) = 0.03, = 0.00,
p= 0.87).
We compared sleep-related variables between the possible ADHD and non-ADHD
groups (Table 2). ESS score was significantly higher in the possible ADHD group (11.26 vs
8.00, Cohen's d = 0.67, p<0.001). There was also a significant difference in the distribution
of individuals with respect to EDS severity between the groups (2 (2) = 251.5, Cramers V
= 0.16, p<0.001). Residual analysis revealed that in the possible ADHD group the rate of
having moderate (p<0.001) and severe sleepiness (p<0.001) was higher than in the
non-ADHD group. There were significant differences between the two groups in total PSQI
score (t (4946)= 17.7, Cohen's d =0.82, p<0.001), all PSQI component scores (C1: t (655)
= 9.28, Cohen's d = 0.46; C2: t (655) = 8.83, Cohen's d = 0.44; C3: t (669) = 3.76,
Cohen's d = 0.17; C4: t (653) = 5.03, Cohen's d = 0.26; C5: t (655) = 6.21, Cohen's d =
0.32; C6: t (637) = 5.55, Cohen's d = 0.34; C7: t (637) = 16.8, Cohen's d = 1.00), total
sleep time (TST) on weekdays (t (5231) = 12.8, Cohen's d = 0.14, p<0.01), midpoint of
sleep on weekend (t (668) = 6.93, Cohen's d = 0.31, p<0.001), and DTS score (t (677) =
9.3, Cohen's d = 0.40, p<0.001). Only TST on weekends did not differ between the groups
Page 9 of 26
(t (644) = -0.97, Cohen's d = 0.05, p=0.33). There were small effect sizes for TST on
weekdays, midpoint on weekends, number having EDS, and the PSQI components of C3,
C4, C5, and C6. PSQI C1 and C2, DTSe scores, and ESS scores had moderate effect
sizes. PSQI C7 had a large effect size.
As shown in Table 3, the presence of ADHD symptoms was significantly associated
with EDS (odds ratio (OR) = 3.30, 95% (confidence interval) Cl = 2.793.90, p<0.001) in
reference to non-ADHD in Model 1. After adjusting for demographic variables in Model 2,
and adjusting for demographic variables, AQ and DTS scores in Model 3, the ORs
decreased gradually (Model 2: OR = 2.78, 95% Cl = 2.343.29, p<0.001; Model 3: OR =
2.45, 95% Cl = 2.062.92, p<0.001). However, in the final model with the addition of PSQI
and CES-D scores (Model 4), the relationship between ADHD and EDS was attenuated but
the OR remained significant (OR = 1.91, 95% Cl = 1.592.29, p<0.001).
A one way ANCOVA was conducted to assess the differences in inattention score and
hyperactivity score among EDS severity groups controlling for DTS scores and PSQI total
scores (Fig. 1). Results indicated a significant difference in inattention score among the
EDS severity groups (F(4,597) = 13.24, 2 = 0.05, p<0.001). The effect size was
considered moderate. The post hoc test revealed that the score was significantly higher in
the group with severe EDS than in the non-EDS group (p<0.001) and group with moderate
EDS (p<0.001). There was no significant difference in inattention score between the
non-EDS group and the group with moderate EDS (P = 1.00). With regard to hyperactivity,
there was no significant difference in hyperactivity scores among the three EDS groups
(F(2,597) = 1.42, P = 0.226).
4. Discussion
To our knowledge, the current study is the first to compare the level of subjective
sleepiness between individuals classified as possibly having ADHD (ie, possible ADHD
10
Page 10 of 26
group) and those classified as not having ADHD (ie, non-ADHD group) in a large adult
sample population. In this study, the number of individuals having EDS was significantly
higher in the possible ADHD group. Mean ESS score in the possible ADHD group was 11.3,
which is in the pathological range of sleepiness, whereas the mean score in the non-ADHD
group was within the normal range (mean = 8.0). The PSQI score also indicated a
significantly higher level of sleep-related problems in the possible ADHD group (mean =
8.81) than in the non-ADHD group (mean = 5.82) These results are consistent with a
previous clinical study which showed that 126 adult patients diagnosed with ADHD had
scores indicating poor sleep quality, EDS, and elevated fatigue relative to normative data
[32]. Previous studies also indicate that the later chronotype and delayed sleep phase are
common in ADHD patients [33,34]. Similarly, the present study showed that evening
chronotype and midpoint of sleep was later in the group with possible ADHD. However,
even after adjusting for factors associated with EDS, such as sleep disturbances and
chronotype, ADHD was a significant predictor of the presence of EDS. Thus, individuals
with possible ADHD could have excessive sleepiness irrespective of the presence/absence
of other causative factors related to sleepiness.
Of interest were the findings related to the severity of EDS. Those participants with
severe EDS in the possible ADHD group showed a significantly higher inattention score,
but not hyperactivity score, when compared with the non-EDS and moderate EDS groups.
In this regard, one study reported that individuals with ADHD Inattentive Type were sleepier
than individuals with ADHD Hyperactive/Impulsive Type, despite no significant differences
in sleep quality between ADHD subtypes [9]. Another study that assessed daytime
sleepiness using the MSLT showed a positive correlation between inattentiveness and the
number of sleep-onsets (total number of times falling asleep during four sessions of MSLT)
[35]. In addition, some studies showed that relative theta power or theta/beta power ratio in
the electroencephalogram, which was used as a marker of central nervous system arousal,
11
Page 11 of 26
was elevated in children and adults with ADHD [3638], and absolute theta power had a
positive correlation with inattention, whereas there was a negative correlation with
hyperactivity [39]. These findings lend support to our results, suggesting that arousal
dysregulation is possibly related to the underlying mechanism in inattentive symptoms in
ADHD. The reason why hyperactivity symptoms did not show any relationship to EDS is
unclear; however, we should consider the possibility that the mechanism in hyperactivity
symptoms and inattentive symptoms is somewhat different [40].
There is substantial evidence that the underlying mechanisms in neurochemical and
anatomical modulation of arousal and attention considerably overlap. Methylphenidate, a
central nervous system stimulant, is known to maintain wakefulness by blocking the
reuptake and increasing the release of dopamine and norepinehrine [41]. Many studies
have also revealed that methylphenidate is effective in alleviating symptoms of ADHD,
supporting the idea that the core symptoms of ADHD appear based on dysregulation of the
dopaminergic and norepinehrinergic systems [42, 43]. Similarly, the noradrenergic system
arising from the locus coeruleus plays a role in the mechanism in maintaining attention [17],
and the activation of the system is involved in the action mechanism in pharmacological
treatment not only for EDS [44] but also for ADHD [45]. Structural abnormalities in the
prefrontal cortex and subcortical areas, which play a crucial role in attention, executive
functions, and control of arousal, have been found in ADHD [46]. Similarly, anatomical
abnormality in the frontal cortex has been reported in narcoleptic patients [47]. Considering
these research findings, we can speculate that EDS in individuals with ADHD is caused by
the same neurochemical or anatomical abnormalities that are associated with the core
symptoms of ADHD, in particular the symptom of inattentiveness.
This study has several limitations that deserve mentioning. First, we used a cutoff
score on the ASRS to identify those participants who had possible ADHD. Although the
ASRS is used in epidemiological studies worldwide, a structured clinical interview is
12
Page 12 of 26
needed to obtain an actual diagnosis of ADHD. Second, the subjects who participated in
this study were not representative of the general population because this study was
conducted as an internet-based survey in which response rate cannot be calculated.
According to previous studies, the prevalence of adults with ADHD assessed using the
ASRS was 34% in other countries [19,48], whereas the prevalence of adults with
(possible) ADHD in the sample in this study was estimated at 6.1%. This higher percentage
may be due to sampling bias, in that individuals interested in the topic of the survey are
more likely to respond to the questionnaire [49]. Third, sleepiness and sleep disturbances
were assessed subjectively by study participants as opposed to using polysomnography
and the MSLT. These methods are necessary not only for making a diagnosis of
hypersomnia but also for detecting secondary EDS caused by other sleep disorders, such
as sleep apnea and periodic leg movements during sleep. Additionally, although a previous
review pointed out the high frequencies of sleep apnea and restless legs syndrome in the
ADHD population [50], we also did not employ specific questionnaires for the screening of
these
disorders,
such
as
the
STOP-BANG
[51]
and
National
Institutes
of
13
Page 13 of 26
sleepiness, the presence of ADHD symptoms was independently associated with EDS.
Thus, sleepiness in ADHD was not due to co-existing sleep problems. The results of the
present study also suggest that excessive sleepiness and inattentive symptoms share a
common underlying mechanism.
Acknowledgments
This work was supported by a Grant from Japan Foundation for Neuroscience and
Mental Health.
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Fig.1.
Table 1. Descriptive statistics for the entire sample and for the presence/absence of possible ADHD.
Total
(N = 9822)
Possible ADHD
(N = 602)
Non-ADHD
(N = 9220)
p-Value
50.0
57.5
49.6
<0.001
0.04
45.64 (13.39)
36.98 (11.66)
46.20 (13.30)
<0.001
0.70
22.26 (3.53)
22.43 (3.86)
22.24 (3.51)
n.s.
0.05
8.44 (3.60)
16.14 (2.71)
7.94 (3.03)
<0.001
2.72
22.19 (6.63)
27.33 (6.31)
21.86 (6.51)
<0.001
0.84
4.48 (6.24)
11.91 (9.40)
4.00 (5.65)
<0.001
1.33
<0.001
0.09
Characteristic
Gender (%Male)
Age, mean (SD), years
Occupation N, (%)
Regular worker
5452 (55.5)
359 (59.6)
5093 (55.2)
<0.05
Part-time worker
1361 (13.9)
79 (13.1)
1282 (13.9)
n.s.
232(2.4)
42 (7.0)
190 (2.1)
<0.01
Student
23
Page 23 of 26
Inoccupation
2777 (28.3)
122 (20.3)
2655 (28.8)
<0.01
16.2
23.1
15.8
<0.001
0.05
20.1
22.4
19.9
n.s.
0.02
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Total
(N = 9822)
Possible
ADHD
(N = 602)
Non-ADHD
(N = 9220)
p-Value
Effect size
(d, , or
Cramer's V)
8.20 (4.92)
11.26 (5.58)
8.00 (4.81)
<0.001
0.67
<0.001
0.16
6593 (67.1)
263 (43.7)
6330 (71.9)
2133 (21.7)
212 (35.2)
1921 (20.8)
796 (8.1)
127 (21.1)
669 (7.3)
6.00 (3.73)
8.81 (4.78)
5.82 (3.58)
<0.001
0.82
1.24 (0.67)
1.53 (0.80)
1.22 (0.66)
<0.01
0.46
1.37 (1.59)
2.03 (1.90)
1.33 (1.56)
<0.01
0.44
1.28 (0.87)
1.42 (0.94)
1.27 (0.86)
<0.01
0.17
0.28 (0.68)
0.45 (0.83)
0.27 (0.67)
<0.01
0.26
0.72 (0.53)
0.88 (0.64)
0.71 (0.52)
<0.01
0.32
0.18 (0.64)
0.38 (0.92)
0.16 (0.62)
<0.01
0.34
0.92 (1.33)
2.13 (1.85)
0.84 (1.25)
<0.01
1.00
389.37
(69.96)
446.49
(8056)
380.28
(89.49)
450.50
(106.30)
389.96
(68.45)
446.23
(78.59)
<0.01
0.14
n.s.
0.05
4:01 (1:50)
4:33 (1:59)
3:59 (1:49)
<0.001
0.31
17.38 (3.95)
15.90 (4.05)
17.48 (3.92)
<0.001
0.40
ESS, Epworth Sleepiness Scale; n.s., not significant; ADHD, attention deficit/hyperactivity disorder; PSQI,
Pittsburgh Sleep Quality Index; SD, standard deviation.
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Table 3. Results of multivariable adjusted logistic regression models predicting EDS (N = 9822).
Model 1
Model 2
Model 3
Model 4
OR (95% Cl)
OR (95% Cl)
OR (95% Cl)
OR (95% Cl)
Possible ADHD
(N = 602)
3.30
(2.793.90)*
2.78
(2.343.29)*
2.45
(2.062.92)*
1.91
(1.592.29)*
Non-ADHD
(N = 9220)
1.00
1.00
1.00
1.00
ADHD,
attention-deficit/hyperactivity disorder; AQ, Autism Spectrum Quotient; BMI, body mass index;
CES-D, 12-item version of the Center for Epidemiological Studies-Depression Scale; Cl,
confidence interval; EDS, excessive daytime sleepiness; OR, odds ratio; PSQI; Pittsburgh Sleep
Quality Index.
*
p<0.001.
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