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Journal of Child Psychology and Psychiatry 53:11 (2012), pp 1157–1166 doi:10.1111/j.1469-7610.2012.02600.

Severe mood problems in adolescents


with autism spectrum disorder
Emily Simonoff, 1 Catherine R.G. Jones, 2 Andrew Pickles, 3 Francesca Happé, 4
Gillian Baird, 5 and Tony Charman6
1
Department of Child and Adolescent Psychiatry, King’s College London, Institute of Psychiatry and NIHR Biomedical
Research Centre for Mental Health, De Crespigny Park, London, UK; 2Department of Psychology, University of Essex,
Wivenhoe Park, Colchester, Essex, UK; 3Department of Biostatistics, King’s College London, Institute of Psychiatry,
London, UK; 4MRC SDGP Research Centre, King’s College London, Institute of Psychiatry, London, UK; 5Guy’s & St
Thomas’ NHS Foundation Trust, Newcomen Centre, London, UK; 6Centre for Research in Autism and Education,
Institute of Education, London, UK

Introduction: Severe mood dysregulation and problems (SMP) in otherwise typically developing youth
are recognized as an important mental health problem with a distinct set of clinical features, family
history and neurocognitive characteristics. SMP in people with autism spectrum disorders (ASDs) have
not previously been explored. Method: We studied a longitudinal, population-based cohort of
adolescents with ASD in which we collected parent-reported symptoms of SMP that included rage, low
and labile mood and depressive thoughts. Ninety-one adolescents with ASD provided data at age
16 years, of whom 79 had additional data from age 12. We studied whether SMP have similar correlates
to those seen in typically developing youth. Results: Severe mood problems were associated with
current (parent-rated) and earlier (parent- and teacher-rated) emotional problems. The number of prior
psychiatric diagnoses increased the risk of subsequent SMP. Intellectual ability and adaptive
functioning did not predict to SMP. Maternal mental health problems rated at 12 and 16 years were
associated with SMP. Autism severity as rated by parents was associated with SMP, but the relationship
did not hold for clinician ratings of autistic symptoms or diagnosis. SMP were associated with difficulty
in identifying the facial expression of surprise, but not with performance recognizing other emotions.
Relationships between SMP and tests of executive function (card sort and trail making) were not
significant after controlling for IQ. Conclusions: This is the first study of the behavioural and cognitive
correlates of severe mood problems in ASD. As in typically developing youth, SMP in adolescents
with ASD are related to other affective symptoms and maternal mental health problems. Previously
reported links to deficits in emotion recognition and cognitive flexibility were not found in the
current sample. Further research is warranted using categorical and validated measures of
SMP. Keywords: Severe mood dysregulation, mood disorders, childhood autism, autism spectrum
disorder, SNAP.

functional impairment. In support of this new diag-


Introduction nosis, Leibenluft and colleagues provide evidence for
Severe mood problems (SMP) in children and ado- distinctive presenting and longitudinal clinical fea-
lescents include high levels of irritability, often tures, family history and neurocognitive profile (Lei-
manifested by temper tantrums, as well as low and benluft, 2011). They argue that, while features
labile mood; together, these have been identified as aligned with irritability are included in several diag-
an important cause of psychosocial impairment. nostic categories, the syndrome of severe and
Debate has raged about the aetiology of mood dys- impairing irritability with predominant negative
regulation symptoms, most specifically the extent to mood includes features not adequately captured by
which these are best conceptualized as part of the other diagnoses. Unlike classic juvenile bipolar dis-
spectrum of juvenile bipolar disorder, attention def- order, manic episodes do not appear to be common
icit hyperactivity disorder (ADHD) or as a separate adult outcomes in SMD (Brotman et al., 2006),
syndrome (Leibenluft, 2011). Leibenluft Cohen, whereas unipolar depression and anxiety are
Gorrindo, Brook, & Pine, (2006) argue persuasively (Stringaris et al., 2009). One small family study
for a new diagnostic category, severe mood dysre- failed to find elevated rates of bipolar disorder in
gulation (SMD), currently under consideration for parents of children with SMD, in contrast with the
DSM-5 (www.dsm5.org). Under current proposals, parents of children with juvenile bipolar disorder
SMD would include severe and prominent mood (Brotman et al., 2007). Neurocognitive differences
abnormalities, hyperarousal and increased reactivity exist in young people with SMD in relation to:
to negative emotional stimuli, with consequent labelling facial emotions (Guyer et al., 2007);
response to frustration (Rich et al., 2011); and
Conflict of interest statement: No conflicts declared. performance on response reversal paradigms

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
Published by Blackwell Publishing, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main St, Malden, MA 02148, USA
14697610, 2012, 11, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2012.02600.x by Cisug, Wiley Online Library on [11/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1158 Emily Simonoff et al. J Child Psychol Psychiatry 2012; 53(11): 1157–66

(Dickstein, Finger, Brotman, et al., 2010), with similar in our ASD sample to those seen in typically
neural circuitry differences on fMRI from juvenile developing populations.
bipolar disorder patients in the first two tasks
(Brotman et al., 2010; Rich et al., 2011).
There has recently been an appreciation that other Methods
psychiatric problems frequently occur in people with
Participants
autism spectrum disorders (ASDs), with rates as
high as 60–70%. These co-occurring disorders The sample in the present analyses comprises
include high rates of ADHD, anxiety and ODD in ninety-one 16-year olds with ASD from the 158
children (Joshi et al., 2010; Leyfer et al., 2006; participants with ASD in the original SNAP cohort. In
Simonoff et al., 2008). The emergence and timing of addition, longitudinal data from 12 years were
different psychiatric problems in ASD has not been available on 79 of the 91 individuals. As described
explicity studied, but comparison of cross-sectional previously [see Baird et al., (2006) for details], SNAP
studies of different age groups suggests that was drawn from a total population cohort of 56,946
depressive and obsessive-compulsive disorder may children. All those with a current clinical diagnosis of
be more common in older adolescents and adults pervasive developmental disorder (PDD, N = 255) or
(Bakken et al., 2010; Mazefsky et al., 2010) and one considered ‘at risk’ for being an undetected case by
longitudinal clinical study showed that affective virtue of having a statement of Special Educational
disorder was amongst the most common newly Needs (SEN; N = 1,515) were surveyed using the
emerging psychiatric disorders in adults with autism Social Communication Questionnaire [SCQ (Rutter,
(Hutton, Goode, Murphy, Le Couteur, & Rutter, Bailey, & Lord, 2003)]. A diagnostic assessment of a
2008). Affective disorders in autism have included stratified sample at 12 years (also 255 individuals)
bipolar disorder (Bradley & Bolton, 2006; Munesue identified 158 young people with ASD. The follow-up
et al., 2008), although the ascertainment methods assessment at 16 years focussed on the cognitive
and sample sizes in these studies do not provide a phenotype of ASD and therefore only those who had
conclusion on whether bipolar disorder is dispro- estimated IQs of ‡50 at 12 years were invited to
portionately increased in ASD. participate (Charman et al., 2011). From the SNAP
Most of the research on co-occurring psychiatric database, 131 possible participants were identified
symptoms and disorders in people with ASD has on the basis of IQ; of these, 19 indicated they were
used standardized instruments to measure recog- not interested in participating, 11 could not be con-
nized symptom patterns and diagnoses. The syn- tracted and 1 indicated interest, but was not in-
drome of SMD has not, to our knowledge, been cluded before the end of the study leaving 100
previously explored. There are several reasons to adolescent participants, for whom 91 had data to
consider this a useful concept to explore in people provide an SMP score for these analyses.
with ASD. First, several of the symptom domains For this cohort, consensus clinical ICD-10 ASD
that are increased in people with ASD, including diagnoses at 12 years were made using the Autism
ADHD and affective disorder, have been associated Diagnostic Interview-Revised [ADI-R (Le Couteur
with SMD. Second, people with ASD have high levels et al., 1989)] and Autism Diagnostic Observation
of psychosocial impairment that are greater than Schedule-Generic [ADOS-G (Lord et al., 2000)] as well
would be expected based on their level of intellectual as IQ, language and adaptive behaviour measures.
functioning. While this has often been attributed to The 91 in the contemporaneous analyses included 83
the core autistic deficits, it is an empirical question male, 8 female; 48 met consensus criteria for child-
whether co-occurring psychiatric problems, such as hood autism and 43 for another ASD. For the subset of
SMD, contribute to this psychosocial impairment. 79 included in the longitudinal analyses, 73 were
Third, the relationship between low mood and male and 41 had a diagnosis of autism. The sample
‘challenging’ behaviour has long been recognized in had a mean age of 15 years 6 months (SD =5 months;
intellectual disability, where communication is sig- range 14 years 8 months–16 years, 9 months) with a
nificantly impaired (Hayes, McGuire, O’Neill, Oliver, mean time interv al from the 12 year assessment of
& Morrison, 2011). Challenging behaviour occurs in 4 years 0 months (SD =11 months, range 1 year
10–20% of people with ASDs, affects the entire 7 months–5 years 8 months).
intellectual ability spectrum (Emerson et al., 2001), The study was approved by the South East
but its causes are less well-understood than in those Research Ethics Committee (05/MRE01/67) and
with intellectual disability without ASD. One possi- informed consent was obtained from all participants.
bility is that unrecognized mood problems partially
explain high rates of challenging behaviour in ASD.
Measures
In the present study, we use data collected from
the Special Needs and Autism Project (SNAP) cohort Questionnaires and interviews. A scale comprising
(Baird et al., 2006) at age 16 years to create a ‘SMP’ was generated a priori from four items on the
measure of SMP. We test whether the psychiatric, parent-reported Profile of Neuropsychiatric Symp-
family and neurocognitive correlates to this scale are toms (PONS), completed at 16 years. The PONS is a

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
14697610, 2012, 11, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2012.02600.x by Cisug, Wiley Online Library on [11/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
doi:10.1111/j.1469-7610.2012.02600.x Mood problems in autism 1159

62-item questionnaire that assesses the severity and symptoms that comprise the autism spectrum dis-
impact of 31 symptoms commonly reported in chil- order diagnoses. The Social Responsiveness Scale
dren and young people with neurodevelopmental [SRS (Constantino et al., 2003)] T scores were used
disorders (Santosh, Baird, Pityaratstian, Tavare, & as a quantitative measure of autism severity, scored
Gringras, 2006). For each symptom, a brief definition at 12 years in 60 participants and at 16 years in 27,
is given and the respondent is asked to endorse the where data were missing at 12 years.
overall frequency and impact on everyday life. Each Adaptive functioning at 12 years was measured
component (frequency and impact) is each scored 0–5 using the Vineland Adaptive Behaviour Scales com-
(‘not at all’ to ‘all the time’/‘extremely’), with a com- posite score (Sparrow, Balla, & Cichetti, 1984). A
bined score ranging from 0 to 10. Four items were quantitative measure of the shortfall, or adaptive
included in the SMP scale, taking into consideration, ‘under-function’, was generated by subtracting the
the proposed DSM-5 criteria: ‘explosive range’, ‘low Vineland score from the full-scale IQ, both measured
mood’, ‘depressive thoughts’ and ‘labile mood’. A at 12 years and standardized to mean of 100, SD 15
description of the PONS, the presentation of the indi- and.
vidual items and the means and ranges for the SNAP Maternal self-reports on the General Health
ASD samples are described in the supplementary Questionnaire [GHQ-30 (Goldberg & Muller, 1988)]
online appendix and Supplementary Table S1. The when the participants were 12 and 16 years pro-
scale had good internal consistency with a Cronbach’s vided a measure of maternal psychiatric symptoms
a of .92. The raw scale was nonnormally distributed with particular emphasis on mood, anxiety and so-
with a mean of 7.8 (SD 8.0, range 0–36) and a square- matic difficulties. The Parenting Stress Index [PSI
root transformation was applied to generate a more Short Form; (Abidin, 1995)] measures difficulties in
normally distributed continuous measure with the parent-child relationship on three subscales:
skewness of 0.16 and kurtosis 2.78. A binary classi- disturbed child, parental distress and parent-child
fication divided the top 25% of scores (13–36, N = 24) dysfunctional interaction. Parental distress was
from the rest of the distribution (0–12, N = 67). This used, herein, to index the parental component of
threshold was chosen pragmatically because (a) it was stress, as it attempts to measure parental charac-
likely to have reasonable power to detect mean dif- teristics rather than aspects of the parent-child
ferences and (b) it is conservative compared to the relationship, which may be affected by the presence
rates of ADHD (28%) and anxiety disorders (42%) re- of an ASD in the child.
ported in this cohort and is therefore, a plausible
threshold to select. Neurocognitive measures. IQ was measured at
The Strengths and Difficulties Questionnaire [SDQ 12 years with the Wechsler Intelligence Scales for
(Goodman, Ford, Simmons, Gatward, & Meltzer, Children-Third Edition [WISC-IIIUK (Wechsler,
2000)], rated by parents at 12 and 16 years and 1992)] and at 16 years with the Wechsler Abbrevi-
teachers at 12 years, was also used to measure ated Scales of Intelligence [WASI (Wechsler, 1999)].
mental health symptoms. The SDQ is a widely used Details of the neurocognitive tasks are given in the
screening instrument for child psychiatric problems Supplementary online appendix. All were adminis-
and its psychometric properties have been estab- tered at 16 years. The emotion recognition task has
lished in several samples, including UK (Goodman been previously described (Jones et al., 2011). In the
et al., 2000) and US studies (Bourdon, Goodman, present analysis, we used the Ekman-Friesen test of
Rae, Simpson, & Koretz, 2005). The present analyses affect recognition (Ekman & Friesen, 1976), as this
use the hyperactivity, conduct and emotional sub- was most similar to tasks undertaken in typically
scales. developing youths with SMD (Brotman et al., 2008).
At 12 years, the parent-reported Child and Ado- We measured total number of correct responses.
lescent Psychiatric Assessment [CAPA (Angold & The Card Sort was included as a measure of cog-
Costello, 2000)] was completed on 69 of the present nitive flexibility and response reversal (Tregay, Gil-
sample. The CAPA is a semistructured psychiatric mour, & Charman, 2009). The task requires the
interview and the following diagnostic areas were participant to correctly sort cards to one of three
included: all anxiety and phobic disorders (including alternative sets across three trials, with the correct
obsessive-compulsive disorder); major depression set varying in each trial. The key variable was the
and dysthymic disorder; ODD and conduct disorder number of sorts required to reach criterion. In the
(CD); ADHD; tics/Tourette/trichotillomania; enure- present analyses, we included only those partici-
sis and encopresis. The prevalence rates and diag- pants who demonstrated an understanding of the
nostic correlates have been reported previously rule in the first trial by reaching criterion before the
(Simonoff et al., 2008). end. The number of sorts required in the second and
Autism severity was assessed in three ways. We third trials was divided into four levels: top half
used the diagnostic dichotomy of childhood autism/ (scores 12–18, N = 42); third quartile (scores 19–24,
other PDD. Clinicians undertaking the review of N = 22), bottom quartile (scores 25–40, N = 17) and
autism diagnostic information based on the ADI-R those who did not reach criterion by the end of both
and ADOS-G described above scored the 12 ICD-10 trials (N = 8).

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
14697610, 2012, 11, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2012.02600.x by Cisug, Wiley Online Library on [11/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1160 Emily Simonoff et al. J Child Psychol Psychiatry 2012; 53(11): 1157–66

Trail Making was included as a measure of atten- overall effect and those specific to an emotion.
tional switching and response reversal. The task was Ordinal logistic regression was also used for ordinal
comprised of three separate trials (Reitan & Wolfson, outcomes, such as number of diagnoses. For sets of
1985). The participant was asked to ‘join the dots’ in ordinal items, such as SDQ items, specificity of
numerical order, then, in a second trial, in alpha- association was tested using similar models esti-
betic order, followed by a third trial switching be- mated in gllamm (www.gllamm.org) using a gener-
tween numbers and letters. The difference score alized estimating equations approach with an
between the time taken on the first and the third trial Independent Working Model. The models allowed
comprised a measure of switching ability. The mean separate threshold parameters for each item and
difference score was 57.8 (SD 40.7, range 10.5– estimated a common and an item-specific effect in
229.1). As the data were highly skewed, a square- the manner of testing for differential item function-
root transformed score was used in the present ing. Significance of effects was determined from
analyses. Wald tests using the robust form of the parameter
covariance matrix.
Statistical analysis
Data reduction and statistical analysis were Results
undertaken in Stata version 11 (StataCorp, 2009). Participant characteristics, according to high/low
Linear regression was used to examine the contin- SMP are shown in Table 1.
uous outcome of the transformed SMP score and
logistic regression for the binary variable of high
Emotional and behavioural characteristics
versus low SMP scores. Ordinal logistic regression
associated with SMP
was used for the Card Sort, where a 4-level scale
was generated, and for the analyses using the total Examining the contemporaneous relationships be-
number of psychiatric diagnoses on the CAPA. tween the three parent-rated mental health problems
Multivariate regression, analogous to multiple domains of the SDQ (Table 2) revealed that hyper-
analysis of variance, was employed to analyse the activity, conduct and emotional problems all were
emotion recognition profile to allow for tests of an associated with SMP in bivariate analyses, but that

Table 1 Sample characteristics according to severe mood dysregulation and problems (SMP) classification [M (SD)]

High SMP (N = 24) Low SMPa (N = 67)

Raw PONS scores on individual items


Explosive rage 4.9 (2.4) 1.2 (1.4)
Low mood 4.8 (2.3) 1.2 (1.4)
Labile mood 4.8 (2.8) 0.8 (1.6)
Depressive thoughts 4.6 (2.8) 0.6 (1.2)
Other characteristics at 16 years
Full-scale IQ 80.0 (16.6) 85.8 (17.5)
SDQc Hyperactivity 6.6 (2.6) 5.7 (2.4)
SDQc Conduct problems 2.6 (1.1) 1.5 (1.6)
SDQc Emotional problems 5.3 (2.1) 2.9 (2.3)
Maternal GHQ score 8.0 (8.5) 4.1 (6.3)
Other characteristics at 12 years
Adaptive behaviour 50.6 (12.3) 52.1 (14.4)
Diagnosed childhood autism N (%) 13 (54) 35 (52)
ICD-10 symptom severity 8.4 (2.4) 8.0 (2.5)
SRSb 101.3 (25.9) 90.3 (22.4)
SDQc Hyperactivity (parent) 7.4 (2.8) 7.5 (2.5)
SDQc Conduct problems (parent) 3.5 (1.9) 2.9 (2.1)
SDQ3 Emotional problems (parent) 6.3 (2.5) 3.8 (2.4)
CAPA Any emotional problem N (%) 11 (57.9) 13 (26.0)
CAPA Oppositional defiant/conduct disorder N (%) 8 (42.1) 9 (18.0)
CAPA ADHD N (%) 8 (42.1) 9 (16.0)
Maternal GHQ score 7.3 (7.3) 4.9 (6.5)
Neurocognitive measures at 16
Ekman faces total score 41.8 (8.2) 42.8 (7.7)
Card sort errors to criterion 24.5 (8.3) 21.8 (8.7)
Trail making difference score 69.1 (48.8) 61.9 (43.7)

ADHD, attention deficit hyperactivity disorder; CAPA, Child and Adolescent Psychiatric Assessment; GHQ, General Health
Questionnaire; SDQ, Strengths and Difficulties Questionnaire; SRS, Social Responsiveness Scale.
a
High SMP refers to those scoring in the top quartile, whereas low SMP is the rest of the distribution.
b
Measured at 12 years in 60, at 16 years in 27.
c
Parent-reported measures at 12 and 16 years.

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
14697610, 2012, 11, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2012.02600.x by Cisug, Wiley Online Library on [11/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
doi:10.1111/j.1469-7610.2012.02600.x Mood problems in autism 1161

Table 2 Personal characteristics under various scales associated with severe mood problems [95 per cent confidence intervals]

Unadjusted Adjusted

B (95% CIs) p b (95% CIs) p

Emotional and behavioural problems at 16 (parent-rated)


SDQ Hyperactivity .15 (.03, .28) .02 .03 ().08, .14) .56
SDQ Conduct problems .37 (.19, .56) <.001 .27 (.11, .44) <.01
SDQ Emotional problems .35 (.22, .45) <.001 .30 (.19, .41) <.001
Emotional and behavioural problems at 12 (parent-rated)
SDQ Hyperactivity .000 ().13, .13) .98
SDQ Conduct problems .14 ().03, .30) .10
SDQ Emotional problems .25 (.13, .36) <.001
Emotional and behavioural problems at 12 (teacher-rated)
SDQ Hyperactivity ).02 ().19, .13) .75
SDQ Conduct problems .11 ().08, .30) .27
SDQ Emotional problems .29 (.16, .42) <.001
Other personal characteristics
Full-scale IQ (current) ).01 ().03, .00) .13
Adaptive functioning (12 years) ).02 ().04, .01) .17
IQ-adaptive functioning discrepancy (12 years) .00 ().02, .02) .99
Social Responsiveness Scale (SRS) Autism severity .02 (.01, .03) <.01
ICD-10 total autism symptom score .10 ().04, .23) .15
Maternal distress
Maternal GHQ, 16 years .07 (.02, .11) <.01
Maternal GHQ, 12 years .08 (.03, .13) .01

GHQ, General Health Questionnaire; SDQ, Strengths and Difficulties Questionnaire.

only conduct and emotional problems remained size, with correlations for parent and teacher
significant in multivariate regression. The conduct emotional scores at 12 and SMP of 0.44 and 0.18,
problems scale includes amongst its five items ‘often respectively. These associations remained signifi-
has temper tantrums or hot tempers’, which is clo- cant using the truncated SMP scale of explosive
sely related to the SMP concept; we hypothesized this rage and labile mood (b = .16, p = .002; b = .20,
item might underpin the association of SMP with p = .001 for parent and teacher SDQ emotional
conduct problems. Fitting an ordinal response model scale respectively), indicating that common emo-
to the five SDQ conduct items showed a significant tional symptoms predict to the less emotional
association with SMP (common proportional odds components of SMD. Finally, in the subsample of
ratio (OR) 1.43, 95% CIs 1.23, 1.66; p < .001). 69, we used CAPA diagnoses at 12 years to predict
However, the inclusion of an additional effect specific the category of high (top quartile) SMP score.
to tempers reduced the common partial OR to 1.18 Having any CAPA emotional or behavioural disor-
(95% CIs 1.00, 1.40; p = .055), whereas the specific der at 12 years substantially increased the odds of
effect item was itself large and significant being in the top quartile for SMP (OR = 9.6,
(OR = 2.09, 95% CIs 1.38, 3.16; p < .001). This 95%CIs 2.43, 37.00, p < .001), as did a diagnosis
provides concurrent validity for the concept of SMP in each of the three domains: ADHD (OR = 3.82,
as defined in the current study. Furthermore, al- 95%CIs 1.17, 12.47, p = .03.,); ODD/CD (OR =
though the emotional subscale of the SDQ includes 3.32, 95%CIs 1.04, 10.59, p = .04); and any emo-
items on anxiety as well as mood, this can also be tional (anxiety/depressive/phobic) disorder (OR =
considered an index of concurrent validity. To ad- 3.92, 95%CIs 1.29, 11.86, p = .02). There were
dress the issue of whether the association with the strong associations among the CAPA diagnoses and
SDQ emotional scale was simply due to overlapping a multivariable analysis including all three CAPA
item content, we repeated the regression with a domains as predictors of the high SMP category
truncated version of the SMP scale that included failed to distinguish an independent domain pre-
only explosive rage and labile mood. The results re- dicting SMP 4 years later. However, ordinal logistic
mained highly significant (b = .19, p < .001), indi- regression indicated a significant trend in the
cating the relationship is due to co-occurrence of association between the number of the 12 possible
common mood and anxiety symptoms and those CAPA disorders and being in the high SMP group
specifically related to severe mood dysregulation. (p value from ordinal logistic regression = .006). In
In examining the prediction of SMP at 16 years relation to the high SMP category, rates were as
from mental health symptoms at 12 years, bivari- follows: for no CAPA disorder, 3%, 95% CIs 0–19%;
ate analyses showed the same pattern for parent one CAPA disorder, 32%, 95% CIs 9–55%; ‡2 dis-
and teacher ratings at 12 years; only SDQ emo- orders 44%, 95% CIs 23–65%. The finding repli-
tional symptoms were significantly associated cated when the CAPA diagnoses were collapsed to
(Table 2); however, these effects were of moderate the three domains described above (ordinal logistic

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
14697610, 2012, 11, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2012.02600.x by Cisug, Wiley Online Library on [11/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1162 Emily Simonoff et al. J Child Psychol Psychiatry 2012; 53(11): 1157–66

Table 3 Multivariate regression of association between severe mood problems and emotion recognition

Emotion Overall
testa

Happiness Sadness Rear Anger Surprise Disgust

B (95% CIs) p B (95% CIs) p B (95% CIs) p B (95% CIs) p B (95% CIs) p B (95% CIs) p F(6) p

).09 ().21, 020) .11 ).01 ().31, .29) .96 ).15 ().54, .24) .45 .05 ().22, .32) .75 ).45 ().77, ).13) <.01 18 ().22, .58) .37 3.00 .01
a
Bonferroni-corrected test of overall significance.

regression p < .001); the rate of high SMP category Table 4 Severe mood problems score according to Card sort
for one disorder domain 44%, 95% CIs 19–70%; ‡2 trials to criterion
disorder domains 50%, 95% CIs 22–78%. SMPa

Mean score 95% CIs


Other participant characteristics
Card-sort trials to criterion
Full-scale IQ, whether measured at 16 (Table 2) or Top 50% 2.03 1.58, 2.47
12 years (b = .01, 95%CIs ).02, .01, p = .42) was not 51–75% 2.57 1.68, 3.25
associated with SMP. Similarly, neither adaptive 76%+ 2.84 1.68, 3.25
Did not meet criterion 3.09 2.23, 3.96
functioning at 12 years nor the difference between
cognitive ability and adaptive functioning was sig- SMP, severe mood problems.
nificantly associated with SMP. a
Square root transformed score.
Autism symptoms on the parent-reported SRS
were strongly and positively related to SMP. In con-
trast, the relationship was not replicated when using tion and SMP (F(6,86) = 3.00, p = .010), which post
either the clinician-rated ICD-10 symptom score or hoc tests identified as being due to a specific asso-
the diagnostic classification of childhood autism/ ciation with surprise (Bonferroni corrected p = .04)
other PDD. For the latter, the mean transformed (Table 3). Covarying for full-scale IQ and including
SMP scores were 2.38 (childhood autism) versus only those 72 participants with IQ ‡70 showed sim-
2.32 (other PDD), t = 0.20, p = .84). ilar overall significant findings, but the Bonferroni-
adjusted significance level is associated with sur-
prise fell to 0.11 and 0.37 respectively. Results on
Maternal mental health
the Card Sort using ordinal logistic regression, in
Using maternal GHQ scores, we found a significant which the three response categories were predicted
relationship between SMP and high scores at both by SMP, showed that SMP was associated with more
ages. The latter relationship remained significant errors or decreased cognitive flexibility (OR = 1.35,
when the other contemporaneously assessed 95%CIs 1.04, 1.73, p = .02) (Table 4). However, the
parental variables of educational and socioeconomic Card Sort trials to criterion were strongly associated
status and contextual factors of family-based and with IQ (ordinal logistic regression OR = 0.91, 95%
neighbourhood deprivation were included as cova- CIs 0.88, 0.94, p < .001), and when this was added
riates (b = .08, 95% CIs .02, .14, p = .01). To address as a covariate, the relationship between Card Sort
the possibility that maternal mental health was trials and SMP became nonsignificant (OR = 1.24,
indexing distress in relation to having a challenging 95% CIs 0.94, 1.63, p = .13). A sensitivity analysis
child with ASD, rather than a characteristic of the limiting the participants to those with IQ ‡70
mothers, we undertook a further regression in which (N = 72) replicated the nonsignificant finding
we included as independent variables both the (p = .13).
maternal GHQ score and the parental distress sub- In the Trail Making, there was no significant rela-
scale from the Parenting Stress Index, both mea- tionship between transformed time difference score
sures at 12 years. The GHQ retained a similar level and SMP (b = .17, 95% CIs ).17, .51, p = .33). IQ was
of prediction (b = .08, p = .002) as seen in the also strongly related to Trail Making (b = .07, 95%
bivariate analysis (Table 2) while the index of CIs ).10, ).04, p < .001), but its addition, as a co-
parental distress was nonsignificant (b = .02, variate did not alter the pattern of results (p = .63),
p = .43). nor did the exclusion of participants with IQ <70
(p = .64).
Neurocognitive performance associated with SMP
Association with all emotions was tested using Discussion and conclusions
multivariate regression, which revealed a significant This is the first examination of the mental health
overall association between poorer emotion recogni- and neurocognitive correlates of SMP in adolescents

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
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doi:10.1111/j.1469-7610.2012.02600.x Mood problems in autism 1163

with ASDs. The strongest mental health correlates disorders (Simonoff et al., 2008) or the stability of
are with emotional symptoms both in contempora- psychiatric symptoms over time (Simonoff et al.,
neous and predictive analyses. We considered the 2012).
possibility that the SMP scale could be dominated Neither full-scale IQ nor adaptive functioning was
by mood symptoms and therefore be not more than associated with SMP. This is consistent with previ-
a proxy for emotional symptoms. However, all four ous findings regarding co-occurring psychiatric dis-
symptoms contribute similar to the high SMP group orders in SNAP (Simonoff et al., 2008) but it should
and the scale has high internal consistency. Fur- be noted that other studies report a relationship
thermore, the specific link to the ‘tempers’ item of between lower IQ and psychiatric problems in ASD
the conduct scale adds additional support for the (Totsika, Hastings, Emerson, Lancaster, & Berridge,
SMP construct in our sample. In addition, the 2011). Our prediction of an association between
association with the teacher emotional score at adaptive under-function and SMP was also not
12 years excludes the possibility of a parental rater substantiated, excluding this as one reason for the
bias. This finding is consistent with the literature in IQ-adaptive functioning discrepancy.
typically developing children showing that the lon- We replicate the finding in otherwise typically
gitudinal course of SMP involves affective problems developing children with SMD that parents are at
primarily (Brotman et al., 2006; Stringaris et al., increased risk of affective disorder (Brotman et al.,
2009). 2007) and show that this is independent of the
The relationship between SMP and ADHD has possible confounders of family background, neigh-
been previously identified, with a suggestion that bourhood deprivation and parental distress associ-
emotional lability may be prominent in people with ated with having a challenging child with ASD.
ADHD (Sobanski et al., 2010). Our findings in ASD Families of individuals with ASDs have higher rates
do not provide a clear answer. SDQ ADHD symp- of affective disorder, both major depression and
toms were neither predictive nor independently bipolar disorder, and the nature of this association is
correlated with SMP. On the other hand, the pres- not fully understood (Bolton, Pickles, Murphy, &
ence of any psychiatric disorder at age 12 was Rutter, 1998; Ingersoll, Meyer, & Becker, 2011).
highly predictive of being in the top quartile for SMP However, this relationship does not appear to be
at 16 (OR>9) and the prediction was equally strong solely a consequence of stress induced by raising a
for disorders in each of the three domains of emo- child with ASD as some cases of affective disorder in
tional, oppositional/conduct and ADHD. Previously, parents commenced prior to the child’s birth and
we showed that, in this sample, more than 80% of other instances of affective disorder occurred in
those with ADHD also had an emotional and/or second degree, and other relatives not directly in-
oppositional/CD (Simonoff et al., 2008), and this volved in the care of the autistic child. The current
may be consistent with the SMP concept. However, analyses suggest a specific relationship between
it is interesting that a high SMP score at 16 is maternal affective symptoms and SMP in offspring
predicted not only by the presence of any disorder, within the ASD group that warrants additional
but also by the number of individual diagnoses, exploration with more detailed psychiatric mea-
further highlighting that there may be a number of sures, as the GHQ is a nonspecific measure of psy-
different psychiatric correlates to SMP in people chiatric symptoms.
with ASD. We find very little support for the same neuro-
We found that autism severity, as measured on cognitive correlates of SMD in our ASD sample as
the parent-reported SRS was strongly associated are reported in typically developing youth, i.e.
with SMP, whereas the clinician-rated symptom poorer performance on emotion recognition (Guyer
score generated at 12 years was not. The SRS con- et al., 2007) and response reversal tasks (Dickstein
tains many more items with a wider range of scores et al., 2007; Dickstein, Finger, Skup, et al., 2010).
than the other measures. The possibility of corre- Previous analyses of the emotion recognition tasks
lated measurement error in parents’ responses to in SNAP demonstrated that participants with ASD
the SRS and SMP scale cannot be excluded without were not generally deficient in emotion recognition
another data source. Whatever the explanation for compared to controls of the same intellectual abil-
the discrepancy between parent- and clinician- re- ity, but rather had specific difficulties correctly
ported autism severity scores and SMP, the finding identifying the emotion of surprise (Jones et al.,
that SMP are not associated with childhood autism 2011). We report an association of SMP to the same
versus another PDD is important for service provi- emotion, but not for a wider range of emotions, as
sion. As autism is generally considered more severe described in typically developing populations with
than Asperger syndrome or atypical autism/ ASDs, SMD.
there is a temptation for clinicians to assume that The Card Sort task used in this study is a measure
all aspects of psychosocial functioning will be less of cognitive flexibility; in fact, the ID/ED task used
impaired in the latter group. Our previous findings by (Dickstein et al., 2007) in youth with SMD is de-
highlight that this diagnostic dichotomy does scribed as being based on the Wisconsin Card Sort.
not predict the rate of co-occurring psychiatric We found a significant relationship between SMP

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
14697610, 2012, 11, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2012.02600.x by Cisug, Wiley Online Library on [11/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1164 Emily Simonoff et al. J Child Psychol Psychiatry 2012; 53(11): 1157–66

and cognitive rigidity, as measured by increased emotional construct. This is the first exploration of
trials to criterion after having learned one rule. SMD in autism and the findings indicate that SMD is
However, this relationship disappeared when IQ was a psychometrically coherent concept in which psy-
accounted for. The IQ range in SNAP is wide chiatric and family correlates are similar with those
(50–119), making it particularly important to con- seen in typically developing children, but where the
sider its role in the performance of all neurocognitive neurocognitive basis may be different. It will be
tasks. Trail Making, also tapping cognitive flexibility, important to test more definitively in larger samples
showed no association with SMPs in our ASD sam- that allow clinically meaningful subgroups whether
ple. Thus, we failed to replicate the neurocognitive these problems have similar or distinct origins. As
findings from typically developing samples. Our SMD could be a target for intervention in ASD, future
findings on neurocognitive tasks raise the possibility studies should also clarify its prevalence in ASD, its
that different brain mechanisms are involved in SMP relationship to other measures of ‘challenging
in people with ASD. behaviour’ and the additional impairment that it
This study has a number of strengths. The sample is causes, as well as investigating both the biological/
population–based and carefully characterized with cognitive and environmental risk factors and corre-
respect to both their autism and general cognitive lates for SMD.
features. The longitudinal nature of the sample allows
us to examine predictors of SMP as well as correlates.
Most importantly, the sample remains unusual in Supporting information
having been assessed with respect to a wide range of Additional Supporting Information may be found in the
both behavioural characteristics and neurocognitive online version of this article:
tasks. It is this feature that allowed us to explore the Appendix S1 The Profile of Neuropsychiatric Symp-
relationship of SMPs to neurocognitive performance toms (PONS)
in ASD. We have been conservative in our analytic Appendix S2 Details of neurocognitive tasks
approach, limiting these to the tasks (emotion recog- Table S1 Characteristics of individual PONS items for
nition, cognitive flexibility) associated with SMD in full ASD sample
typically developing children. Please note: Wiley-Blackwell are not responsible for
the content or functionality of any supporting materials
The limitations to this study are also important to
supplied by the authors. Any queries (other than
note. The study was not originally designed to assess
missing material) should be directed to the corre-
SMD and the bespoke measure used herein, while sponding author for the article.
carefully constructed, is not presently standardized
or validated. Therefore, our findings must be inter-
preted with caution. Furthermore, although the
Acknowledgements
concept of SMD is an evolving one, this measure may
We thank Ellen Leibenluft for her advice on the item
imperfectly characterize the current definition, as it
selection for the SMP scale and Paramala Santosh for
does not explicitly include an item on irritability permission to reprint the relevant items from the PONS.
(because this was not included in the PONS). Due to
the moderate sample size of SNAP and the lack of an
identified cut-off for the SMP score, most of the
Correspondence
present analyses use the continuous measure in
Emily Simonoff, Department of Child and Adolescent
contrast with the findings reported in non-ASD
Psychiatry, King’s College London, Institute of Psychi-
samples, which study ‘clinical’ groups.
atry and NIHR Biomedical Research Centre for Mental
Despite these limitations, the results are interest- Health, De Crespigny Park, London SE58AF, UK;
ing and important in showing that SMP in adoles- Email: emily.simonoff@kcl.ac.uk
cents with ASD represent a coherent and primarily

Key points
• Severe mood problems in young people are now considered a separate entity that predicts to subsequent
depressive disorder and has distinct neurocognitve and brain imaging correlates.
• A new diagnostic category of severe mood dysregulation is proposed for DSM-5.
• Young people with autism spectrum disorder (ASD) have high rates of psychiatric comorbidities, but the role
of severe mood problems has not previously been studied.
• In adolescents with ASD, we found links to emotional and behavioural problems and family history similar to
those reported in otherwise typically developing youth, but did not see the same associations with the
neurocognitive deficits in emotion recognition and response reversal.
• Severe mood problems may have different underlying causes in ASD and this requires further investigation.

 2012 The Authors. Journal of Child Psychology and Psychiatry  2012 Association for Child and Adolescent Mental Health.
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doi:10.1111/j.1469-7610.2012.02600.x Mood problems in autism 1165

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