association between symptoms and subtypes of attention-deficit

8/19/2019 Association Between Symptoms and Subtypes of Attention-Deficit

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type (ADHD-C), according to the DSM-IV (Diagnostic and

Statistical Manual of Mental Disorders, Fourth edition)

diagnostic criteria for ADHD. Both sleep problems ⁄ disorders

and ADHD are the major concerns in clinical practice, and in

parental care (Corkum et al., 1999; Gau, 2006; Mick et al.,

2000). Symptoms and consequences of ADHD and sleep

problems frequently overlap (Chervin et al., 2002b; OBrien et

al., 2003), and both cause behavioral problems (Gregory and

OConnor, 2002; Willcutt et al., 1999) and impaired academic

performance (Gozal and Pope, 2001; Todd et al., 2002).

Studies have demonstrated increased symptoms of inattention

(Chervin et al., 2002b; OBrien et al., 2003) and hyperactivity

(Chervin et al., 2002b; Gau and Chiang, 2009; OBrien et al.,

2003) among individuals with primary sleep disorders,

increased sleep problems, and disorders in patients with

ADHD (Corkum et al., 1999; Cortese et al., 2009; Gau and

Chiang, 2009; Walters et al ., 2008), and potential effects from

medication, especially psychostimulants, and other psychiatric

comorbidities on sleep problems (Corkum et al., 1999; Cortese

et al., 2009; Gau and Chiang, 2009; Mick et al., 2000; Stein,

1999). However, there are limited data on whether specific

sleep problems ⁄ disorders are more associated with either

inattentive or hyperactive-impulsive symptoms (Gau, 2006;

Gau et al., 2007, 2009; OBrien et al., 2003), and few studies

have explored the contribution of the DSM-IV ADHD

subtypes on sleep problems ⁄ disorders (Corkum et al., 1999;

OBrien et al., 2003).

Studies examining the associations between ADHD core

symptoms (Chervin and Archbold, 2001; Gau, 2006; Gau and

Chiang, 2009; Gottlieb et al., 2003; Lecendreux et al., 2000;

Willoughby et al., 2008) and subtypes (Corkum et al., 1999;

LeBourgeois et al., 2004; Mayes et al., 2009; Wiggs et al.,

2005), and sleep problems have revealed inconsistent results.

Although Corkum and colleagues reported no ADHD subtypedifference in dyssomnias and parasomnia (Corkum et al .,

1999), Mayes et al. (2009) found that the ADHD-C had

more sleep problems than the ADHD-I and controls, yet

ADHD-I was associated with daytime sleepiness (Mayes et al .,

2009). LeBourgeois and colleagues reported that parent-

reported chronic nocturnal snoring was more frequently seen

in children with ADHD-HI (LeBourgeois et al ., 2004), whereas

Wiggs et al. (2005) reported no subtype differences in

sleep-disordered breathing. Regarding ADHD symptoms,

community-based questionnaire surveys have demonstrated

that inattentive and hyperactivity-impulsivity symptoms are

related to dyssomnia (Gau, 2006; Gau et al., 2007), sleep-

disordered breathing (Gau, 2006; Gottlieb et al., 2003), and

nightmares (Gau, 2006; Gau et al., 2007), but no significant

association between hyperactivity and objective measures of

apneas and hypopneas among clinic-referred children with

suspected disordered breathing (Chervin and Archbold, 2001).

Moreover, little is known about the relationship between

ADHD symptoms and sleep problems in patients with ADHD

(Gau and Chiang, 2009).

Previous studies have been limited by inconsistent diagnostic

criteria [rating scale (OBrien et al ., 2003) and DSM criteria

(LeBourgeois et al., 2004; Mayes et al., 2009)], small sample

sizes (Wiggs et al., 2005; especially for the ADHD-HI subtype;

LeBourgeois et al., 2004), no inclusion of ADHD-HI (Mayes

et al ., 2009), inadequate consideration for medication status

(LeBourgeois et al., 2004; OBrien et al., 2003) and psychiatric

comorbidities (OBrien et al., 2003; Wiggs et al., 2005), and

only inclusion of limited sleep problems, such as snoring

(LeBourgeois et al., 2004; OBrien et al., 2003) or sleep-

disordered breathing (Chervin and Archbold, 2001; Gottliebet al., 2003; OBrien et al., 2003) in each study except one

(Mayes et al ., 2009), or grouping a wide range of sleep

problems into dyssomnias and parasomnias for subtype

comparison (Corkum et al., 1999). To the best of our

knowledge, despite well-known relationships between sleep

measures and ADHD (Cortese et al., 2009; Walters et al .,

2008), there is a lack of information about the comparisons

of sleep problems ⁄ disorders among the three ADHD subtypes

in the ethnic Chinese population, and no study has included

both subtype and symptom dimension approaches in one

paper. Therefore, we conducted this study with a strict study

design to test the hypothesis that there are differences in sleep

schedules, daytime inadvertent napping, and sleep prob-

lems ⁄ disorders among patients with different ADHD subtypes

or between inattention and hyperactivity-impulsivity symptom

dimensions as compared with children and adolescents without

lifetime ADHD.

M A T E R I A L S A N D M E T H O D S

Participants

The sample consisted of 325 patients (265 boys, 81.5%) aged

10–17 years, who were observed to have overt ADHD

symptoms at the mean age of 4.24 ± 1.66 years by theirmothers, started to receive clinical treatment (mainly psychi-

atric intervention) at the mean age of 8.22 ± 2.97 years after

being clinically diagnosed with ADHD according to the DSM-

IV criteria, and were assessed by using the Chinese version of

the Kiddie epidemiologic version of the Schedule for Affective

Disorders and Schizophrenia (K-SADS-E) at the mean age of

12.63 ± 1.71 years. They were recruited mainly from National

Taiwan University Hospital (87.7%). The patients who had

psychosis, autism spectrum disorders, or a full-scale IQ score

less than 80 were excluded. Among them, 90 patients in 45

pairs came from the same families. At the current assessments,

the ADHD subtype distributions were 174 (53.5%) for

ADHD-C, 130 (40.0%) for ADHD-I, and 21 (6.5%) for

ADHD-HI, based on best estimate of psychiatric diagnosis.

The comparison sample consisted of 257 (155 boys, 60.3%)

participants without lifetime diagnosis of ADHD: 173 from

the same school districts of the patients with ADHD; and 84

unaffected siblings of patients with ADHD. They did not have

ADHD at childhood and at the assessments at the mean age of

12.99 ± 2.27 years by clinical assessments according to the

DSM-IV diagnostic criteria and psychiatric assessments using

the Chinese K-SADS-E. The other inclusion criteria were

536 H.-L. Chiang et al.

2010 European Sleep Research Society, J. Sleep Res., 19, 535–545


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children and adolescents who had an IQ greater than 80; and

who and whose parents consented to this study and would like

to complete all the assessments. Those who had pervasive

developmental disorder or major psychosis were excluded.

In summary, there were 582 participants consisting of 325

with a current diagnosis of ADHD (280 probands and 45

siblings) and 257 without lifetime ADHD (84 siblings and 173

school controls). All the participants have complete data based

on the K-SADS-E interviews, assessments of sleep prob-lems ⁄ disorders, and parent and teacher reports on the Con-

nors Rating Scales. Two papers have been published using the

sample of probands with childhood diagnosis of ADHD and

school controls to investigate psychiatric outcomes at adoles-

cence among children with ADHD (Gau et al., 2010), and to

compare the sleep problems ⁄ disorders between adolescents

with persistent and subthreshold ADHD (Gau and Chiang,

2009). There is no overlap of the content of this study with that

of the two published papers.

Measures

Chinese version of the K-SADS-E

The K-SADS-E is a semi-structured interview scale for the

systematic assessment of both past and current episodes of

mental disorders in children and adolescents. The detail of the

development of the Chinese K-SADS-E has been described

elsewhere (Gau et al., 2005; Gau and Soong, 1999). Previous

studies have shown that the Chinese K-SADS-E is a reliable

and valid instrument to assess DSM-IV child psychiatric

disorders (Gau et al., 2005) and sleep disorders (Gau and

Chiang, 2009; Gau and Soong, 1999), and has been used

extensively in a variety of studies regarding childhood mental

disorders in Taiwan (Gau et al., 2005, 2009; Gau and Chiang,2009; Gau and Soong, 1999).

Chinese version of the Conners Parent Rating Scale-Revised:

short form and Conners Teacher Rating Scale-Revised: short

form (CPRS-R: S and CTRS-R: S)

Both the CPRS-R: S, a 27-item parent-reported rating scale

(Conners, 1997; Conners et al., 1998a), and the CTRS-R: S, a

28-item teacher-reported rating scale (Conners, 1997; Conners

et al., 1998b), consist of three factor-derived subscales (those

with the highest loadings on the CPRS-R: long form) and the

ADHD index. The three subscales are inattention ⁄ cognitive

problems, hyperactivity ⁄ impulsivity, and oppositional. The

ADHD index is used to assess children and adolescents at risk

for ADHD based on diagnostic criteria of DSM-IV (Conners,

1997). Each item on both scales is rated on a four-point Likert

scale – 0 for never, seldom; 1 for occasionally; 2 for often,

quite a bit; and 3 for very often, very frequently (Conners,

1997). The Chinese versions of the CPRS-R: S and CTRS-R:

S have been found to be reliable and valid instruments for

measuring ADHD-related symptoms in Taiwan (Gau et al.,

2006, 2008).

Sleep variables

The sleep variables included sleep problems measured by the

Sleep Disturbance Questionnaire (Gau, 2006; Gau et al., 2007),

DSM-IV-defined sleep disorders, such as primary insomnia,

primary hypersomnia, circadian rhythm sleep disorder, sleep

terror disorder, sleep walking disorder, and nightmare disor-

ders included in the Chinese K-SADS-E interview (Gau and

Chiang, 2009), and sleep schedules and the frequency of

daytime naps based on child reports. The frequency of

inadvertent daytime napping was rated on a four-point scale:

1 for never; 2 for once–twice per month; 3 for once–twice per

week; and 4 for almost every day.

Interviewer training and best estimate of diagnosis

The details of the K-SADS-E interview training and best

estimate of each DSM-IV psychiatric diagnosis including

sleep disorders have been described elsewhere (Gau et al.,

2010; Gau and Chiang, 2009), and are provided upon

request. Four interviewers, who had undergone 1 year of

intensive clinical and research training in child psychiatrybefore the Chinese K-SADS-E interview training, reached

over 90% agreement on all mental disorders assessed by

the Chinese K-SADS-E (ranging from 98.25 ± 1.91 to

99.38 ± 1.06) against the rating of each item in the K-

SADS-E by Gau for 30 clinical subjects before study

implementation. Their K-SADS-E interviews were audio-

taped periodically and monitored by Gau, who was blind to

the personal information of the participants, to ensure the

quality of interviews.

The best estimate of each diagnostic category was made by

Gau, who was blind to the diagnostic status and name of the

participant, and who was not involved in direct K-SADS-E

interviews of any of the participants or their parents at

follow-up. The diagnosis was made based on the K-SADS-E

interviews of the participants and their mothers, medical

records, and teachers reports. The diagnostic coding was

categorized into definite (reaching full DSM-IV diagnostic

criteria), probable (either not reaching full, but more than

half of the DSM-IV symptoms criteria, or no functional

impairment), possible (some symptoms but no impairment),

and no diagnosis. Those patients who received a rating as

definite or probable by best estimate were categorized as

having a particular mental disorder. The three ADHD

subtypes (ADHD-C, ADHD-I and ADHD-HI) were assigned

based on the DSM-IV diagnostic criteria for ADHDsubtypes.

Procedures

The Research Ethics Committee of National Taiwan Univer-

sity Hospital approved this study, and written informed

consent was obtained from both parents and children. All the

participants received the Weschler Intelligence Scale for

Children – Third edition before recruitment to ensure that

their full-scale IQ reached 80 or above. All the adolescent

ADHD subtypes ⁄ symptoms and sleep 537



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participants and their mothers were interviewed indepen-

dently by separate well-trained interviewers for DSM-IV

psychiatric diagnoses including sleep disorders using the

Chinese K-SADS-E to confirm whether their symptoms at

childhood reached the diagnosis of ADHD before 7 years old

according to the DSM-IV diagnostic criteria, the child

diagnosis of ADHD for the ADHD group and no diagnosis

of ADHD for the controls. Subsequently, all the participants

and their mothers were interviewed using the Chinese K-SADS-E to make the current psychiatric diagnosis (past

6 months) in 2005–2008. The interviewers were blind to the

case ⁄ control status. The sleep problems and disorders were

integrated into the K-SADS-E interviews for DSM-IV

diagnosis of sleep disorders (Gau and Chiang, 2009). The

medication history was validated by medical records of

prescription. The interviewers were blind to the case ⁄ control

status.

Data analyses

We used the SAS 9.1 version (SAS Institute, Cary, NC, USA)

to conduct data analysis. Four comparison groups were 174

with ADHD-C, 130 with ADHD-I, 21 with ADHD-HI, and

257 without ADHD (non-ADHD). The descriptive results are

presented as frequency and percentage for categorical

variables; for continuous variables, mean and SD. We used a

multi-level model with random and fixed effects to addressthe lack of independence within the same family. For the

comparisons of continuous variables such as sleep schedules

and ADHD symptom scores measured by the CPRS-R: S,

CTRS-R: S, and K-SADS-E, we used the Proc Mixed proce-

dure to compare the mean scores and the Bonferroni method to

adjust for multiple comparisons in post hoc analysis controlling

for sex, age, use of methylphendidate, and psychiatric comor-

bidity. For the comparisons of binary variables such as sleep

Table 1 Demographic characteristics

ADHD-C ADHD-I ADHD-HI Non-ADHD

Statistics

(n = 174) (n = 130) (n = 21) (n = 257) Chi -squ are P-value

Gender, n (%)

Male 148 (85.1) 101 (77.7) 16 (76.2) 155 (60.3) v23 ¼ 34:52


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problems and disorders, the Proc Glimmix procedure with

binomial distribution and logit link for non-linear mixed model

was used to compare the rate of sleep disorders at adolescence

among the four groups. The odds ratios (OR) and 95%

confidence interval (CI) were also calculated. The alpha value

was pre-selected at the level of two-tailed P < 0.05.

R E S U L T S

Sample description

Table 1 presents the demographics and medication history for

the four groups. A higher proportion of males was noted in the

three ADHD groups than the non-ADHD group. Participants

with ADHD-HI were younger, and less likely to be treated

with methylphenidate than the other two ADHD groups.

There was no statistical difference in parental characteristics,

such as age, level of education and job levels, and household

condition (Table 1).

Sleep schedules and ADHD subtypes

The ADHD-C and ADHD-HI groups significantly went to

bed earlier, got up later in the morning, and had longer

nocturnal sleep duration than the ADHD-I and non-ADHD

groups on schooldays. There were no significant differences in

sleep schedules on weekends among the four groups (Table 2).

There was a greater difference in bedtime between weekends

and schooldays in the ADHD-C than the ADHD-I and non-

ADHD groups. The ADHD-C and ADHD-I groups, but not

the ADHD-HI group, exhibited more daytime inadvertent

napping than the non-ADHD group (Table 2).

Sleep problems ⁄ disorders and ADHD subtypes

We compared the sleep problems and current and lifetime

DSM-IV sleep disorders among the four groups (Table 3). The

findings of the ADHD-HI group are summarized below

without presentation in Table 3. Both the ADHD-C and

ADHD-I groups were more likely than the non-ADHD group

to have problems of early insomnia, middle insomnia, sleep

terrors, bruxism, and snoring; and to have current and lifetime

early insomnia. Participants with ADHD-C, rather than those

with ADHD-I, were more likely to have problems of circadian

rhythm, sleep-talking, and nightmares; current and lifetime

nightmare disorders; and lifetime primary circadian rhythm

sleep disorder than participants without ADHD. Participants

with ADHD-HI were more likely than those without ADHD

to have nightmares. Participants with ADHD-I were more

likely to have hypersomnia symptoms and lifetime primary

hypersomnia than those without ADHD. However, we did not

find a significant difference between the ADHD-C and

ADHD-I groups in these sleep problems (P > 0.05).

There was no difference between the ADHD-HI and non-

ADHD groups in sleep problems ⁄ disorders (P > 0.05), with

some exceptions. Participants with ADHD-HI were more T

a b l e 2

S l e e p s c h e d u l e s a n d d a y t

i m e i n a d v e r t e n t n a p p i n g a m o n g t h e A D H D

- C , A D H D - I , A D H D - H I a n d n o n - A D H D

g r o u p s

A D H D - C

A D H D - I

A D H D - H I

N o n - A D H D

F - v a l u e

C o m p a r i s o n

( n =

1 7 4 )

( n =

1 3 0 )

( n =

2 1 )

( n =

2 5 7 )

W e e k d a y

B e d t i m e *

2 2 : 3 3

p m ( 5 8 )

2 2 : 5 1 p m ( 5 9 )

2 2 : 1 0 p m ( 4 8 )

2 2 : 4 6 p m ( 5 1 )

5 . 2 4 b

A D H D - C , A D H D - H

I <

A D H D - I , n o n - A D H D

R i s e t i m e *

0 6 : 4 9

a m ( 4 4 )

0 6 : 3 8 a m ( 2 8 )

0 6 : 4 3 a m ( 3 8 )

0 6 : 3 8 a m ( 3 2 )

3 . 5 0 a


I >


S l e e p d u r a t i o n

8 h 1

7 m i n ( 7 4 )

7 h 4 8 m i n ( 6 1 )

8 h 3 3 m i n ( 5 2 )

7 h 5 2 m i n ( 6 2 )

7 . 3 7 c


I >


W e e k e n d

B e d t i m e *

2 3 : 3 9

p m ( 8 2 )

2 3 : 3 8 p m ( 7 6 )

2 3 : 2 4 p m ( 5 9 )

2 3 : 2 8 p m ( 6 0 )

2 . 4 9

–

R i s e t i m e *

0 9 : 2 0

a m ( 9 8 )

0 9 : 2 0 a m ( 9 8 )

0 8 : 5 1 a m ( 9 3 )

0 9 : 0 4 a m ( 1 0 0 )

1 . 4 9

–


9 h 4

1 m i n ( 9 9 )

9 h 4 3 m i n ( 8 2 )

9 h 4 9 m i n ( 7 9 )

9 h 3 5 m i n ( 1 0 3 )

0 . 1 7

–

D i ff e r e n c e b e t w e e n w e e k e n d a n d

w e e k d a y s ( i n m i n )

B e d t i m e

6 6 ( 7

3 )

4 7 ( 7 1 )

5 3 ( 5 7 )

4 2 ( 5 6 )

4 . 5 2 b

A D H D - C >


R i s e t i m e

1 5 1 (

1 0 4 )

1 6 2 ( 9 8 )

1 2 8 ( 8 8 )

1 4 6 ( 1 0 0 )

0 . 9 8

–


8 4 ( 1

0 7 )

1 1 5 ( 9 1 )

7 5 ( 8 0 )

1 0 4 ( 1 0 6 )

2 . 5 1

–

D a y t i m e n a p p i n g

2 . 0 6 ±

0 . 9 5

2 . 1 9 ±

0 . 9 8

1 . 9 2 ±

0 . 6 7

1 . 8 6 ±

0 . 9 0

4 . 1 3 b

A D H D - C , A D H D - I >

n o n - A D H D

C u r r e n t m e d i c a t i o n h a d n o s i g n i fi

c a n t e f f e c t o n s l e e p s c h e d u l e s ( P - v a l u e s r a n g i n g f r o m 0 . 3 7 4 t o 0 . 8 5 1 ) , e x p e c t a s i g n i fi c

a n t e ff e c t i n b e d t i m e d u r i n g t h e w e e k e n d ( F =

4 . 3 4 ,

P =

0 . 0 4 5 ) .

A D H D - C , a t t e n t i o n - d e fi c i t ⁄ h y p e r a c t i v i t y d i s o r d e r ( A D H D ) , c o m b i n e d t y p e ; A D H D - H I , A D H D , p r e d o m i n a n t l y h y p e r a c t i v e - i m p u l s i v e t y p e ; A D H D - I , A D H D , p r e d

o m i n a n t l y i n a t t e n t i o n t y p e .

P - v a l u e s : a P <

0 . 0 5 ;

b P <

0 . 0 1 ;

c P <

0 . 0 0 1 .

* M e a n s o f b e d t i m e a n d r i s e t i m e

e x p r e s s e d b y t i m e t a b l e s a n d S D e x p r e s s e d

i n m i n u t e s .

M e a n s e x p r e s s e d b y h o u r s ( h ) a n d m i n u t e s ( m i n ) , a n d S D e x p r e s s e d b y m i n

u t e s .




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likely to have symptoms of nightmare (OR: 2.97; CI: 1.11– 7.96), bruxism (OR: 2.60; CI: 1.02–6.63), and snoring (OR:

3.28; CI: 1.25–8.56) than the non-ADHD group. The only

difference between ADHD groups was that the ADHD-HI

group was less likely to have primary insomnia than the

ADHD-C group (Fishers exact P = 0.016 for current,

P = 0.008 for lifetime) and the ADHD-I group (P = 0.033

for lifetime). Sleepwalking disorder, regardless whether current

or lifetime, was the only sleep disorder without difference

between the ADHD groups and non-ADHD group.

Sleep schedules and problems related to ADHD symptoms

Regarding sleep schedule, inattention, and hyperactivity-

impulsivity were all associated with earlier bedtime, later rise

time and longer nocturnal sleep hours on schooldays, and with

earlier bedtime for teacher- and youth-reported inattention

and parent-reported hyperactivity on weekends (Table 4).

Although univariate analysis revealed a significant associa-

tion between ADHD symptoms and sleep problems (all

P-values < 0.05), except for hypersomnia (P-values ranging

from 0.113 to 0.996) and circadian rhythm problems (P-values

ranging from 0.095 to 0.368 for hyperactivity-impulsivity),

there were only some sleep problems that remained significantin the final model summarized in Table 4. The most-related

current sleep problems for both inattention and hyperactivity-

impulsivity were more daytime inadvertent napping (hyperac-

tivity-impulsivity based on K-SADS-E interviews excluded),

early insomnia, sleep terrors, sleep-talking, bruxism, and

snoring. In general, teacher-reported ADHD symptoms were

not associated with sleep problems, except for daytime

napping, sleep-talking with inattention ⁄ cognitive problems,

and snoring with hyperactivity-impulsivity.

D I S C U S S I O N

This large-scale study, one of few studies examining the sleep

schedules, problems, and disorders associated with ADHD

subtypes and symptoms in one study, has several major

findings. First, earlier bedtime and later rise time with longer

sleep duration in children and adolescents with ADHD-C and

ADHD-HI than those with ADHD-I and those without

ADHD were noted on schooldays. Increased bedtime differ-

ence between weekends and schooldays is greater in the

ADHD-C group than in the ADHD-I and non-ADHD

groups. Second, the ADHD-C and ADHD-I groups, not the

Table 3 Sleep problems and disorders for the ADHD-C, ADHD-I and non-ADHD groups

Sleep problems

ADHD-C

n (%)

(n = 174)

ADHD-I

n (%)

(n = 130)

Non-ADHD

n (%)

(n = 257)

Odds ratio (95% confidence intervals)

ADHD-C versus

non-ADHD

ADHD-I versus

non-ADHD

ADHD-C versus

ADHD-I

Symptoms

Early insomnia 46 (26.4) 25 (19.2) 24 (9.3) 3.50 (2.03–6.04) 2.31 (1.25–4.27) 1.52 (0.87–2.66)

Middle insomnia 20 (11.5) 14 (10.8) 10 (3.9) 3.19 (1.43–7.09) 2.97 (1.26–7.00) 1.08 (0.51–2.26)

Hypersomnia 5 (2.9) 5 (3.9) 1 (0.4) 7.56 (0.85–67.06) 10.21 (1.15–90.75) 0.74 (0.21–2.66)Circadian rhythm 6 (3.5) 3 (2.3) 1 (0.4) 9.13 (1.06–78.63) 6.05 (0.61–60.51) 1.51 (0.36–6.29)

Sleep terror* 19 (10.9) 15 (11.5) 7 (2.7) 4.36 (1.77–10.72) 4.64 (1.82–11.81) 0.94 (0.46–1.94)

Sleepwalking* 21 (12.1) 17 (13.1) 24 (9.4) 1.32 (0.70–2.50) 1.45 (0.73–2.87) 0.91 (0.45–1.84)

Sleep-talking* 111 (63.8) 71 (54.6) 114 (44.5) 2.17 (1.43–3.28) 1.51 (0.96–2.36) 1.44 (0.88–2.35)

Nightmare 41 (23.6) 28 (21.5) 37 (14.4) 1.83 (1.11–3.02) 1.63 (0.94–2.83) 1.12 (0.65–1.95)

Bruxism* 83 (47.7) 53 (40.8) 67 (26.2) 2.57 (1.67–3.94) 1.96 (1.23–3.14) 1.31 (0.81–2.12)

Snoring* 85 (48.9) 69 (53.1) 85 (33.2) 1.91 (1.27–2.88) 2.31 (1.47–3.63) 0.82 (0.51–1.32)

Current sleep disorders

Primary insomnia 34 (19.8) 18 (13.9) 18 (7.1) 3.22 (1.74–5.99) 2.09 (1.04–4.22) 1.54 (0.82–2.92)

Primary hypersomnia 3 (1.7) 1 (0.8) 0 (0) 0.066 0.339 0.320

Circadian rhythm sleep disorder 2 (1.2) 2 (1.5) 0 (0) 0.164 0.115 0.362

Sleep terror disorder* 0 (0) 0 (0) 0 (0) – – –

Sleepwalking disorder* 2 (1.2) 4 (3.1) 2 (0.8) 1.47 (0.20–10.80) 3.99 (0.71–22.61) 0.37 (0.07–2.08)

Nightmare disorder 21 (12.1) 14 (10.8) 16 (6.3) 2.05 (1.03–4.08) 1.79 (0.84–3.82) 1.15 (0.55–2.37)

Lifetime sleep disordersPrimary insomnia 39 (22.5) 22 (16.9) 23 (9.1) 2.92 (1.65–5.15) 2.03 (1.07–3.85) 1.44 (0.80–2.61)

Primary hypersomnia 3 (1.7) 4 (3.1) 0 (0) 0.066 0.013 0.222

Circadian rhythm sleep disorder 5 (2.9) 2 (1.5) 0 (0) 0.011 0.115 0.235

Sleep terror disorder* 4 (2.3) 5 (3.9) 2 (0.8) 2.97 (0.53–16.74) 5.01 (0.94–26.78) 0.59 (0.15–2.29)

Sleepwalking disorder* 14 (8.1) 12 (9.2) 18 (7.1) 1.15 (0.55–2.41) 1.34 (0.62–2.93) 0.86 (0.38–1.95)

Nightmare disorder 41 (23.7) 28 (21.5) 38 (15.0) 1.76 (1.07–2.89) 1.55 (0.90–2.69) 1.13 (0.65–1.96)

ADHD-C, attention-deficit ⁄ hyperactivity disorder (ADHD), combined type; ADHD-I, ADHD, predominantly inattention type; the

comparisons between ADHD-HI, predominantly hyperactive-impulsive type and the other three groups are not presented in this table but

are described in the text.

*Presence of a sleep disorder decided by either positive response by youth or mother reported at the psychiatric interview.Fishers exact P-value.




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ADHD-HI group, had more daytime inadvertent napping

than the non-ADHD group. Third, the three ADHD groups

had higher rates of several sleep problems ⁄ disorders than the

non-ADHD group, except for the ADHD-HI group, which

had a small sample size. Specifically, ADHD-C rather than

ADHD-I was associated with circadian rhythm problems,

sleep-talking, nightmares (also ADHD-HI), and ADHD-I was

associated with hypersomnia. Fourth, the most-related sleep

problems for inattention and hyperactivity-impulsivity wereearlier bedtime, later rise time, longer nocturnal sleep, more

frequent daytime napping (inattention mainly), insomnia,

sleep terrors, sleep-talking, snoring, and bruxism (hyperactiv-

ity-impulsivity symptoms mainly) across informants.

Sleep schedules

Consistent with prior findings in children and adolescents

(Corkum et al., 2001; Crabtree et al., 2003; Gau, 2006; Gau

and Chiang, 2009), yet different from our previous reports on

adult population (Gau et al., 2007), ADHD diagnosis and

symptoms are associated with longer sleep duration, mainly on

schooldays. Contradictory to the findings of LeBourgeois et al .

(2004) of no subtype difference on weekdays, and the findings

of Wiggs et al . (2005) of earlier bedtime in ADHD-I, we found

the associations of ADHD-C and ADHD-HI with earlier

bedtime, later rise time, and longer nocturnal sleep. Like the

findings of LeBourgeois et al . (2004), but unlike the findings of

Wiggs et al . (2005), there were no subtype differences on

weekends. Because of competitive academic demands at

adolescence in Taiwan, Taiwanese adolescents tend to have

shorter average nocturnal sleep time than Western adolescents

(Gau and Soong, 1995, 2003). The earlier bedtime and later

rise time in ADHD-C and ADHD-HI may be explained by

paying less attention in academic work or disinclining toattend cram schools during nighttime as other Taiwanese

adolescents do. On the contrary, adolescents with ADHD-I

might be less disobedient against the heavy academic demands

but take longer time to finish assignments (Coghill et al ., 2008),

and may go to bed as late as adolescents without ADHD but

later than the other two ADHD groups. Adolescents with

ADHD-I may not be as resistant as the other two ADHD

groups to go to school and, therefore, get up without delay on

schooldays.

Our findings that both inattention and hyperactivity-impul-

sivity were associated with later rise time and longer sleep

duration on schooldays rather than on weekends are consistent

with Gaus prior findings in a school-based sample aged 6–

15 years (Gau, 2006). Whether ADHD symptoms are related

to earlier bedtime on schooldays and weekends warrants

further investigation.

Daytime inadvertent napping

Similar to other studies (LeBourgeois et al ., 2004), we found

that patients with ADHD-I reported more frequent daytime

inadvertent napping than those with ADHD-HI. However,

our findings did not support higher subjective daytime

sleepiness in the ADHD-I group than the ADHD-C group

(LeBourgeois et al., 2004; Mayes et al., 2009; Wiggs et al.,

2005). This study lends evidence to support that inattention

rather than hyperactivity-impulsivity is associated with day-

time inadvertent napping (Lecendreux et al., 2000; Willoughby

et al., 2008) or sleepiness (Willoughby et al ., 2008). In

summary, the findings that both ADHD-C and ADHD-I

groups had more daytime napping than the ADHD-HI andnon-ADHD groups are further supported by the relationship

between daytime napping and inattention because both

ADHD-C and ADHD-I groups are assumed to have the

number of inattention symptoms reaching the DSM-IV

criteria.

Sleep problems ⁄ disorders and ADHD subtypes

Because of the large sample size and questionable validity of

diagnosing obstructive sleep apnea (OSA) and restless legs

syndrome ⁄ periodic limb movements (RLS ⁄ PLM) based on

psychiatric interviews and subjective self-administered ques-

tionnaire in this study, we did not specifically investigate

these associations; instead we examined snoring and more

general sleep problems and their associations with ADHD

subtypes and symptoms. The possible pathophysiological

mechanisms of the relationships between ADHD and OSA

and RLS ⁄ PLM have been revealed. For example, children

with OSA had poorer executive function in the prefrontal

cortex, which mimics ADHD symptoms observed during

daytime, via the effect of sleep fragmentation and episodic

hypoxia at night (Beebe and Gozal, 2002). As for

RLS ⁄ PLM, RLS ⁄ PLM, and ADHD may come from a

common central nervous system disease via the mechanism

of dopamine deficiency (Solanto, 2002; Trenkwalder et al.,2005) supported by the evidence of effectiveness of dopami-

nergic agents on improving both ADHD and RLS symp-

toms (Walters et al., 2000).

Consistent with literature (Chervin et al., 1997, 2002a;

Cortese et al., 2009; Gottlieb et al., 2003; OBrien et al.,

2003), our previous community-based study (Gau, 2006;

Gau et al., 2007) and a clinical study (Gau and Chiang,

2009), ADHD symptoms or disorders are related with more

sleep problems ⁄ disorders, except sleep walking. Such a

relationship can be partially explained by the fact that

lower nocturnal sleep efficiency caused by sleep problems

such as insomnia, sleep-disordered breathing, or periodic

limb movement (PLM) may induce or exacerbate ADHD-

related symptoms (Golan et al., 2004). As for parasomnia

and ADHD, although a seizure attack may be related to

ADHD (Kaufmann et al., 2009), and a seizure attack is

considered as a possible common pathophysiological mech-

anism to explain ADHD and parasomnia (Gaggero et al.,

2001; Silvestri and Bromfield, 2004), none of the participants

with ADHD has a clinical diagnosis of epilepsy. Therefore,

the underlying pathophysiological mechanism between

ADHD and parasomnia warrants further investigation.




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In general, our results did not provide strong evidence to

support different sleep problems ⁄ disorders across the three

ADHD subtypes. This notion is similar to some studies

showing no subtype differences in dyssomnia (Corkum et al .,

1999), parasomnia (Corkum et al ., 1999), and sleep-disordered

breathing (Wiggs et al ., 2005). Similar to prior findings (Mayes

et al ., 2009), ADHD-C is associated with more sleep prob-

lems ⁄ disorders than ADHD-I (Mayes et al ., 2009) as com-

pared with non-ADHD. Because of the small sample of theADHD-HI subtype (LeBourgeois et al ., 2004) or no inclusion

of ADHD-HI (Mayes et al., 2009) in most of the previous

studies, there has been no reported difference between ADHD-

HI and other subtypes in sleep problems ⁄ disorders except an

increased risk for snoring in the ADHD-HI group as

compared with other subtypes in a study conducted by

LeBourgeois et al . (2004). No subtype difference in snoring is

consistent with Wiggs et al .s study (2005), but might also be

explained by the small sample size in the ADHD-HI group

(n = 21). However, this discrepancy warrants further investi-

gation using a large sample of ADHD-HI.

Our prior study is probably the first to report an association

between hypersomnia and ADHD (Gau and Chiang, 2009),

and this study is the first to report the ADHD subtype

difference in hypersomnia. Surprisingly, our findings suggest

that ADHD-I, not ADHD-C, is associated with hypersomnia

despite both groups having increased daytime inadvertent

napping. This warrants further investigation to more accu-

rately distinguish hypersomnia from daytime sleepiness sec-

ondary to other causes using objective measures (Millman and

Young, 2005), and to delineate the relationship between

ADHD subtypes and hypersomnia.

Another novel finding that adolescents with ADHD-C,

not ADHD-I, had a higher risk of primary insomnia than

those with ADHD-HI might be explained by more severesymptoms, particularly overt inattention in the ADHD-C

group than the ADHD-HI group (Hurtig et al ., 2007),

which are associated with insomnia (Gau and Chiang, 2009;

Mayes et al., 2009).

Sleep problems and ADHD symptoms

In addition to the categorical approach, we also used

dimensional approaches to delineate the relationship between

ADHD and sleep problems because the ADHD subtype

approach is not sufficient to clearly present the severity of

ADHD symptoms (Pickles and Angold, 2003). Despite some

varied results across the three informants (participants,

parents, teachers) and two methods (interviews, self-admin-

istered rating scales), the most-related sleep problems for

inattention and hyperactivity-impulsivity included insomnia,

sleep terrors, sleep-talking, bruxism (hyperactivity-impulsiv-

ity mainly), and snoring. These findings are consistent with

other community-based (Chervin et al., 2002a; Gottlieb

et al., 2003) studies and our prior community-based (Gau,

2006; Gau et al., 2007) and clinic-based studies (Gau and

Chiang, 2009) using subjective measures. The discrepancy in

reporting child and adolescent behavioral symptoms across

informants has been widely reported (Gau et al., 2006;

Mitsis et al., 2000; Valla et al., 1993). Searching for an

association between sleep problems and ADHD symptoms

based on data from a single informant may be of question-

able validity; accordingly, it is reasonable to take the

positive associations from multiple informants into consid-

eration (Mitsis et al ., 2000).

Methodological considerations

The strengths of this study are that standardized psychiatric

interviews of all the 582 participants and their mothers allow

us to obtain accurate diagnoses of ADHD and its subtypes,

sleep disorders, and comorbidities; that ADHD symptoms

were assessed by both interviews and rating scales reported by

three informants; and that potential confounding factors were

controlled in our statistical models including age, sex, use of

medication, and psychiatric comorbidities (Corkum et al.,

1999; Gau, 2006; Gau and Chiang, 2009; Mayes et al ., 2009).

The major limitation of this study is that the small sample

size of ADHD-HI has decreased the power to detect the

difference between ADHD-HI and other comparison groups.

The lowest prevalence rate of ADHD-HI (Lecendreux et al.,

2000; Wiggs et al., 2005) and higher prevalence rates of the

ADHD-C and ADHD-I subtypes (Graetz et al., 2001; Nolan

et al., 2001) among the three subtypes are consistent with many

previous studies as hyperactivity is the least persistent core

symptom of ADHD in adolescents (El-Sayed et al., 2003;

Hurtig et al., 2007). Moreover, despite self-reports and

parental reports frequently used to measure sleep prob-

lems ⁄ disorders based on self-administered questionnaires or

interviews (Gau, 2006; Gau et al., 2007), a lack of objective

measures and the use of the DSM-IV diagnostic criteria ratherthan the International Classification of Sleep Disorders for

diagnoses of sleep disorders make our findings less convincing.

Additionally, we did not clinically evaluate RLS, which has

been reported to be strongly associated to ADHD symptoms

in previous studies examining the relationship between sleep

disturbances and ADHD. Lastly, a clinic-based sample of

ADHD limits the generalization of our findings into a broader

ethnic Chinese population.

Implication

The findings imply that assessment of the sleep problems ⁄ dis-

orders in adolescents with ADHD regardless of ADHD

subtypes and the predominant ADHD symptoms is recom-

mended in clinical practice. Regarding research implication,

ADHD subtypes and symptoms should be taken into consid-

eration in sleep research in addition to a dichotomous

approach of ADHD. It warrants further investigation of the

association between ADHD subtypes and sleep problems ⁄ dis-

orders with an increased sample size in the ADHD-HI group

to fill the gap of our knowledge about sleep schedule,

problems, and disorders in this group.




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A C K N O W L E D G E M E N T S

This work was supported by grants from the National Health

Research Institute (NHRI-EX94-9407PC, NHRI-EX94-

9507PC, NHRI-EX94-9607PC, NHRI-EX94-9707PC) and

National Science Council (NSC96-2628-B-002-069-MY3),

Taiwan. We would like to express our thanks to Ms Chi-Mei

Lee for assisting in data analysis. There is no conflict of

interest related to this work to be disclosed.

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