Senior Seminar - Beyond the Two-Factor Model of the ASD Diagnostic Criteria

BRIEF REPORT

Brief Report: DSM-5 Sensory Behaviours in Children With and Without an Autism Spectrum Disorder

Dido Green1 • Susie Chandler2 • Tony Charman3 • Emily Simonoff2,5 •

Gillian Baird4

Published online: 30 July 2016

� Springer Science+Business Media New York 2016

Abstract Atypical responses to sensory stimuli are a new

criterion in DSM-5 for the diagnosis of an autism spectrum

disorder (ASD) but are also reported in other develop-

mental disorders. Using the Short Sensory profile (SSP)

and Autism Diagnostic Interview-Revised we compared

atypical sensory behaviour (hyper- or hypo-reactivity to

sensory input or unusual sensory interests) in children aged

10–14 years with (N = 116) or without an ASD but with

special educational needs (SEN; N = 72). Atypical sensory

behaviour was reported in 92 % of ASD and 67 % of SEN

children. Greater sensory dysfunction was associated with

increased autism severity (specifically restricted and

repetitive behaviours) and behaviour problems (specifically

emotional subscore) on teacher and parent Strengths and

Difficulties Questionnaires but not with IQ.

Keywords Autism spectrum disorder � Sensory reactivity � Sensory interests � DSM-5 � Diagnostic criteria � Behaviour

Introduction

Kanner’s (1943) original description of autism referred to

negative reactions to sensory stimuli, ‘‘loud noises or

moving objects, which are therefore reacted to with horror

or panic’’ (p. 245) while noting that the child ‘‘can happily

make as great a noise as any that he dreads and move

objects to his heart’s desire’’ (p. 245). Asperger (1944) also

described children as demonstrating hypersensitivity in

some circumstances but in other situations either ignoring

(appearing hyposensitive) or seeking out particular stimuli.

The Third Diagnostic and Statistical Manual of Mental

Disorders (DSM-III) (American Psychiatric Association

(APA) 1980) included atypical sensory responsiveness as

an associated feature of infantile autism under diagnostic

criterion E: ‘‘Bizarre responses to various aspects of the

environment’’ (APA 1980, p. 90). However, the subsequent

two editions of the DSM did not include specific reference

to sensory responsiveness in the diagnostic criteria (DSM-

IV, APA 1994; DSM-IV-TR, APA 1987). Since then,

atypical responses to sensory stimuli have been reported as

occurring in 65–95 % of individuals with ASD (Lane et al.

2014; Leekam et al. 2007; Tomchek and Dunn 2007;

Zachor and Ben-Itzchak 2014). Different types of response

to the sensory environment in ASD have been described;

hyper-responsivity, hypo-responsivity and over focussed

sensory interests (described in the literature as sensory

seeking) (Ausderau et al. 2014). Single or mixed sensory

modality responsivity and association with core features of

ASD and comorbidities have also been explored. A meta-

analysis of sensory behaviours in individuals with ASD

showed significant variation between studies with three

important moderators identified; chronological age, sever-

ity of autism and type of control group (whether compar-

ison groups were matched for chronological or mental age

& Dido Green [email protected]

1 Centre for Rehabilitation, Oxford Brookes University,

Marston Road Campus, Jack Straw’s Lane, Oxford OX3 3FL,

UK

2 Department of Child and Adolescent Psychiatry, Institute of

Psychiatry, Psychology and Neuroscience, King’s College

London, London, UK

3 Department of Psychology, Institute of Psychiatry,

Psychology and Neuroscience, King’s College London,

London, UK

4 Guy’s and St Thomas’ NHS Foundation Trust, King’s Health

Partners, London, UK

5 NIHR Biomedical Research Centre for Mental Health,

Institute of Psychiatry, Psychology and Neuroscience, King’s

College London, London, UK

123

J Autism Dev Disord (2016) 46:3597–3606

DOI 10.1007/s10803-016-2881-7

or other developmental disorder) (Ben-Sasson et al. 2009).

Altered sensory responsivity is reported as being associated

with restricted repetitive behaviours (Chen et al. 2009;

Foss-Feig et al. 2012) and need for sameness (Wigham

et al. 2015). Foss-Feig et al. (2012) considered sensory

subtypes in a study of 5–8 year olds with ASD (without a

comparison group) using both parent questionnaire and

direct observation of sensory behaviour. They found that

tactile hypo-responsiveness and sensory seeking correlated

strongly with increased social and communication impair-

ment on the Autism Diagnostic Interview-Revised (ADI-R)

(LeCouteur et al. 2003) and Autism Diagnostic Observa-

tion Schedule-Generic (ADOS-G) (Lord et al. 2000), and to

a lesser degree, repetitive behaviours. Tactile hyper-re-

sponsiveness did not significantly correlate with any of the

core features of ASD (Foss-Feig et al. 2012). Lane et al.

(2010; 2014) described four distinct sensory subtypes

showing different associations with age and IQ (e.g., taste/

smell versus postural inattentiveness) but noted that the

sensory phenotypes were not explained by gender or autism

severity (Lane et al. 2014). Altered sensory responsiveness

has been linked to anxiety (e.g., Lane et al. 2012; Ben-

Sasson et al. 2008; Wigham et al. 2015) and depression

(Bitsika et al. 2016) and may also have a significant impact

on adaptive function (e.g. Ben-Sasson et al. 2009; Lane

et al. 2010; Tomchek and Dunn 2007; Zachor and Ben-

Itzchak 2014).

The latest version of the DSM has again included

atypical sensory responsiveness (hyper- or hypo- reactivity

to sensory input) or unusual interest in sensory aspects of

the environment as one of four possible elements of which

two must be met in Criterion B: Restricted, repetitive

patterns of behaviour, interests, or activities. Combined

with persistent deficits in social communication and social

interaction across multiple contexts, these two domains

define autism spectrum disorder (DSM-5; APA 2013).

However, atypical responses to sensory stimuli are also

reported in people with intellectual disability and other

neurodevelopmental disorders (Watling et al. 2001; Green

et al. 2003; Tomchek and Dunn 2007; Lane et al. 2012),

leading to the suggestion that sensory symptoms are a non-

specific indicator, along with abnormalities in motor skills

or self-regulation, of brain network vulnerability in

developmental psychopathology (Levit-Binnun et al.

2013). While sensory behaviours are reported as occurring

more frequently in ASD than in comparator groups

(Watling et al. 2001; Tomchek and Dunn 2007), it is not

clear what proportion of individuals with conditions other

than ASD have hyper- or hypo-reactivity or sensory

interests and whether these involve the same sensory

modalities, single or multiple. We therefore contrasted the

proportion of individuals with hyper-or hypo-reactivity or

sensory interest to environmental sensory input, consistent

with DSM-5 criteria, in two groups of children from the

Special Needs and Autism Project (SNAP; Baird et al.

2006). Children with ASD and children with other forms of

special educational needs (SEN) without ASD were com-

pared using relevant items from the ADI-R (Lord et al.

1994) and the Short Sensory Profile (SSP) (Dunn 1999).

We also explored whether atypical sensory behaviours in

ASD were associated with autism symptom severity, IQ or

co-occurring emotional and behavioural problems. We

hypothesised that children with ASD would show a high

frequency of atypical responses to the sensory environ-

ment. These atypical responses would be more frequent

and more severe than in children with other neurodevel-

opmental problems and associated with autism severity and

behaviour problems.

Methods

The study was approved by the South East Multicentre

Research Ethics Committee (REC) (00/01/50). Parents

gave informed consent for participation.

Participants

The sampling methodology of the SNAP study has been

described previously (Baird et al. 2006) and is illustrated in

Fig. 1. In brief, this was a study of the prevalence of ASD

within a total population cohort of 56,946 children born

between July 1st 1990 and December 31st 1991 who were

assessed when aged 9–14 years. All those with a current

clinical diagnosis of ASD (N = 255) or considered ‘at risk’

of ASD by virtue of having a Statement of SEN 1

(N = 1515) were screened using the Social Communica-

tion Questionnaire (SCQ) (Rutter et al. 2003). Based on

SCQ score, a subsample stratified by four levels of SCQ

score 2

representing low (\8), moderately low (8–14), moderately high (15–21) and high ([21) scores (by coin- cidence also N = 255), received a face to face compre-

hensive diagnostic assessment by trained researchers which

included the ADOS-G (Lord et al. 2000) and the ADI-R

(Lord et al. 1994), and measures of intellectual ability

(IQ).and behaviour. All information was used by the senior

authors to derive a clinical consensus diagnosis of ASD

(childhood autism and other ASDs; Baird et al. 2006) based

on ICD-10 (World Health Organization (WHO) 1993)

1 A Statement of Special Educational Needs is a legal document

issued by the local educational authority when children require

significant additional support in school due to any learning and/or

behavioural problems. 2 The cut-offs of 15 and 22 are recommended by Rutter et al. (2003),

and an additional cut-point of \8 was applied, based on the distribution of SCQ scores within the sample.

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research criteria. The total number of ICD-10 autism

symptoms was recorded. A panel of international experts

reviewed a proportion of cases and agreement on diagnosis

was high (see Baird et al. 2006 for details). Cases not

meeting criteria for a diagnosis of ASD were categorized as

SEN. These children had educational needs and a variety of

other developmental/medical diagnoses.

Measures

ADI-R the ADI-R has three items relevant to sensory

responsivity; ‘unusual sensory interests’, ‘undue sensitivity

to noise’, and ‘abnormal idiosyncratic response to specific

sensory stimuli’. Scored as current or having ever been

present; 0 (nil), 1 (present but with little or no impact, 2

(definite with impact), and 3 (for two items indicating

severe impact).

The Sensory Profile (SPr) (Dunn 1999). Parents com-

pleted the SSP (Dunn 1999), a commonly used question-

naire measure of abnormal responses to sensory stimuli,

reported to have good discriminate validity for children

(McIntosh et al. 1999a). The parent or carer rates the

child’s typical responses to sensory stimuli across 38 items

on a five point scale from ‘never = 5’ responds in this

ASD Autism Spectrum Disorder; SCQ Social Communication Questionnaire; SEN Special Educational Needs; SSP Short Sensory Profile

56, 946 births in total population (July 1, 1990 to Dec 31 1991)

1515 with SEN but no local ASD diagnosis 37 with local ASD diagnosis but no SEN 218 with local ASD diagnosis and SEN

1770 screened with the SCQ

1035 completed SCQ and opted in for further assessment

363 selected for in-depth assessment Local diagnosis SCQ<8 SCQ 8-14 SCQ 15-21 SCQ>21 Total No Selected 94 36 31 61 222

Participated 62 16 19 46 143 Yes Selected 9 14 29 89 141

Participated 3 9 26 74 112

255 seen for assessment (Consensus diagnosis: 97 no ASD (SEN), 158 ASD)

66 opt-outs 30 uncontactable 12 did not attend

173 SSPs fully completed 15 SSPs pro-rated

188 SSPs for analysis

72 SEN 116 ASD

Fig. 1 SNAP sampling methodology

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manner to ‘always = 1’. The time period is not specified

but the present tense phrasing implies current behaviour.

The total score indicates overall sensory dysfunction

(lower scores reflecting greater sensory dysfunction), and

seven subscales reflect dysfunction in the following

domains; tactile sensitivity, taste/smell sensitivity, move-

ment sensitivity, under-responsive/seeks sensation, audi-

tory filtering, low energy/weak, and visual/auditory

sensitivity. Missing values were prorated as an average for

the subscale if \10 % of items were missing for that subscale and no more than 10 % of items missing across all

subscales. Cut-off scores for typical performance, probable

difference and definite difference can be calculated for the

total as well as each subscale. Construct validity and cut-

off scores have been derived from a North American

sample exploring the relationship of the SSP to physio-

logical responses in skin conductance in typical children

and a clinical sample of children identified with sensory

modulation difficulties (McIntosh et al. 1999a, b).

To conform to DSM-5 criteria, hyper-reactivity was

defined as scoring within the definite difference range on

SSP domains (tactile sensitivity, taste/smell sensitivity,

movement sensitivity or visual/auditory sensitivity) or a

score of 2 or 3 on the ADI-R items describing undue

sensitivity to noise or idiosyncratic negative responses to

sensory stimuli (using current codes). Hypo-reactivity was

defined as definite difference in the auditory filtering

domain of the SSP and an ‘always’ or ‘frequently’ response

to ‘Doesn’t seem to notice when face or hands are messy’,

or ‘Leaves clothing twisted on body’ items (both from the

under-responsive/seeks sensation domain) of the SSP.

Sensory interests were defined as a score of 1 or 2 on the

ADI-R item ‘unusual sensory interests’ (current code

used).

IQ was measured using the Wechsler Intelligence Scale

for Children (WISC-III, Wechsler 1991; the current version

at the time of the study) or Raven’s Standard (SPM) or

Coloured Progressive Matrices (CPM) (Raven et al.

1990a, b) depending on the child’s ability. Where WISC

full scale IQs were not available, imputed full-scale IQs

were obtained using the regression relationship of full scale

IQ to SPM/CPM IQ (N = 12). For the five cases where no

direct cognitive testing was possible, all had Vineland

Adaptive Behaviour composite scores (Sparrow et al.

1984) below 20 and these cases were assigned an IQ score

of 19 to reflect their profound level of intellectual

disability. 3

Severity of ASD was measured by ADI-R (4–5 and

current) and ADOS total scores, as well as an overall ICD-

10 symptom count based on all available information (with

symptom counts ranging 0–12). For each of these mea-

sures, total scores as well as domain scores for social

impairment, communication impairment, and restrictive,

repetitive and stereotyped behaviours (RRSB) were cal-

culated. Behaviour problems were measured by the parent

and teacher versions of the Strengths and Difficulties

Questionnaire (SDQ) (Goodman 1997), which asks par-

ents/teachers to rate 25 behaviours as not true (0), some-

what true (1) or certainly true (2). These ratings can be

used to generate a total difficulties score, as well as sub-

scales for emotional symptoms, conduct problem, hyper-

activity, peer problems, and prosocial behaviours. The

SDQ is widely used as a brief screening instrument for

psychiatric problems and its psychometric properties have

been established in several samples, including the UK (e.g.

Goodman et al. 2000).

Data Analysis

Chi squared analyses and Fisher’s exact tests were used to

compare the proportions of children, with and without

ASD, with a hypersensitivity or a hyposensitivity or a

sensory interest consistent with DSM-5 criteria. Within the

ASD group, linear regression was used to examine the

relationship between sensory dysfunction (indicated by

lower SSP total scores) and other child characteristics, IQ,

age, autism symptoms (domain scores from the ICD-10

symptom count, ADOS and ADI-R), and behaviour and

emotions (SDQ subscale scores). Analyses were carried out

using Stata 11 (StataCorp 2009).

Results

From a sample of 255 children, a total of 210 SSPs were

returned. Of these, 173 were fully completed and prorated

scores were calculated for a further 15 resulting in a total of

188 SSPs available for analysis (see Fig. 1). Of the 188,

116 children received a consensus diagnosis of ASD. The

diagnoses of the remaining 72 children (categorised as

SEN) included: 39 intellectual disability, 11 hyperkinetic

or conduct disorder, 10 language impairment, 4 hearing

impairment, 5 physical disability or medical condition, 2

chromosome disorders and 1 with no current clinical

diagnosis. Sample characteristics, mean SSP total and

domain scores are presented in Table 1. The SEN group

was slightly older than the ASD group [t (186) = 8.85,

p \ .001] but the groups did not differ in terms of IQ [t (186) = 0.92, p = 0.36].

3 As these children scored at floor (composite standard score \ 20)

on the Vineland Adaptive Behaviour Scale, these cases were assigned

a proxy IQ score of one point below this, consistent with previous

papers.

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The proportions of SEN and ASD children reported to

have sensory behaviours on the ADI-R, and those scoring

within the definite difference range for each of the SSP

domains are shown in Table 2. Ninety-two percent (107) of

the ASD group compared with 67 % (48) of the SEN group

had either a hypersensitivity, hyposensitivity or a sensory

interest [v2 (1, N = 188) = 20.1, p \ .001]. Compared to the SEN group more children with ASD

scored within the definite difference range on at least one

hyper-reactive domain on the SSP [v2 (1, N = 188) = 29.7, p \ .001] and also for two hyper-reactive domains [v2 (1, N = 188) = 27.1, p \ .001]. Hyper-reactivity to the sensory environment was more common among the

ASD group compared to the SEN group for tactile, taste/

smell and visual/auditory sensitivity (all p \ .05); for movement sensitivity, the difference in rates did not quite

reach significance [v2 (1, N = 188) = 3.84, p = .05]. Definite/marked oversensitivity to noise (ADI item, current

coding of 2 or 3) was also more common in the ASD group,

compared to the SEN group (Fisher’s exact: N = 188,

p \ .001). However rates of idiosyncratic negative responses to specific sensory stimuli causing intrusion

(ADI item coding of 2 or 3) did not differ significantly

(Fisher’s exact: N = 188, p = .295).

Regarding hyposensitivity, a greater proportion of the

ASD group compared to the SEN group, scored within the

definite difference on the SSP auditory filtering subscale

[70 vs 49 %, v2 (1, N = 188) = 8.46, p \ .05]. The SEN

and ASD groups showed similar proportions of children

who always/frequently ‘[doesn’t] seem to notice when face

or hands are messy’ [v2 (1, N = 188) = .92, p = .34, see Table 3]. However, the proportion of children who always/

frequently ‘leaves clothing twisted on body’ was signifi-

cantly higher in the ASD group [v2 (1, N = 188) = 13.3, p \ .001].

More children in the ASD than SEN group were

reported to have unusual sensory interests both by current

[v2 (1, N = 188) = 23.2, p \ .001] and historical [v2 (1, N = 188) = 36.4, p \ .001] ADI-R score (coding 1 or 2).

Within the ASD group, a lower SSP total (indicating

greater sensory dysfunction) was associated with higher

SDQ total score, accounted for by the emotional subscale

on parent report [b = -2.54, t (101) = -2.96, p = .004] and with repetitive, restricted and stereotyped behaviour as

recorded on the ICD-10 symptom count [b = -5.49, t (101) = -2.18, p = .03];but not with ICD-10 social or

communication impairment scores (p = .36 and p = .46,

respectively) (See Table 4). Sensory dysfunction was not

associated with IQ, age, or the remaining SDQ subscales

(all p [ .12). Repeated regressions using the different measures of autism severity, ADI-R and ADOS scores,

yielded the same results, i.e. autism severity and SDQ total

were associated with sensory behaviours, while IQ was not.

A similar pattern was found when the regression analysis

was repeated using teacher SDQ totals in place of parent

SDQ totals.

Table 1 Sample characteristics and mean SSP scores

SEN (N = 72) ASD (N = 116) T test/Chi square/Fisher’s exact

Sample characteristics

Age in years (SD, range) 12.7 (0.87, 10.1–14) 11.6 (0.87, 10–13.8) p \ .001 IQ (SD, range) 77.0 (20.5, 31–131) 73.9 (23.0, 19–136) p = .359

Ethnicity 94 % white 95 % white p = .909

Parental education 39 % with A-levels 47 % with A-levels p = .287

Gender 82 % male 87 % male p = .337

ADI-R 4–5 total (SD) 12.0 (8.87) 43.2 (11.0) p \ .001 ADOS-G total (SD) 3.99 (2.92) 12.5 (6.39) p \ .001 ICD-10 symptom count (SD) 1.38 (1.17) 7.97 (2.47) p \ .001

SSP scores

SSP total [mean (SD)] 153.7 (24.1) 131.0 (24.3) p \ .001 SSP domain scores [mean (SD)]: tactile sensitivity 30.4 (4.45) 26.4 (5.68) p \ .001 Taste sensitivity 16.8 (4.58) 13.5 (5.51) p \ .001 Movement sensitivity 13.0 (2.64) 11.89 (3.30) p \ .014 Underresponsive/seeks sensation 26.2 (7.54) 21.4 (6.20) p \ .001 Auditory filtering 20.2 (5.25) 16.8 (4.85) p \ .001 Low energy/weak 25.6 (5.98) 23.4 (7.12) p = .029

Visual/auditory 21.4 (3.71) 17.6 (5.22) p \ .001

A-Levels Advanced Level General Certificate of Education equivalent to Secondary or High School leaving qualification, ADI-R Autism

Diagnostic Interview-Revised, ADOS-G Autism Diagnostic Observation Scale-Generic, SSP Short Sensory Profile

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Discussion

In this well characterised cohort, sensory interests or hyper

or hypo reactivity to sensory input were reported in the

majority (92 %) of children with ASD but were also

reported in 67 % with SEN but without ASD. A definite

difference in total SSP score was found in 66 % of the

ASD group and 32 % of the SEN group. Both

groups showed a higher frequency than in a group of

typically developing children without functional/clinical

Table 2 Frequency and percentage of definite sensory symptoms among the SEN and ASD groups

SEN

(N = 72)

ASD

(N = 116)

Chi-Sqaure/

Fisher’s exact

ADI-R items

Sensory interests (current) 1 or 2 shown regularly—score

1 [n (%)]

11 (15 %) 49 (42 %) p \ .001

Marked with impact—score 2

[n (%)]

2 (3 %) 13 (11 %) p = .051

Any-score 1 or 2 [n (%)] 13 (18 %) 62 (53 %) p \ .001 Sensory interests (ever): 1 or 2 shown regularly score 1

[n (%)]

11 (15 %) 49 (42 %) p \ .001

Marked with impact—score 2

[n (%)]

3 (4 %) 26 (23 %) p = .001

Any—score 1 or 2 [n (%)] 14 (20 %) 75 (65 %) p \ .001 Sensitivity to noise (current): Slight—score 1 [n (%)] 9 (13 %) 31 (27 %) p = .027

Definite—score 2 [n (%)] 2 (3 %) 28 (24 %) p \ .001 Marked with impact—score 3

[n (%)]

1 (1 %) 6 (5 %) p = .254

Any—score 1–3 [n (%)] 12 (17 %) 65 (56 %) P \ .001 Sensitivity to noise (ever): Slight—score 1 [n (%)] 8 (11 %) 32 (28 %) p = .008

Definite—score 2 [n (%)] 7 (10 %) 40 (34 %) p \ .001 Marked with impact—score 3

[n (%)]

1 (1 %) 12 (10 %) p = .020

Any—score 1–3 [n (%)] 16 (23 %) 84 (72 %) p \ .001 Abnormal idiosyncratic negative response to specific

sensory stimuli (current):

Mild reaction—score 1 [n (%)] 5 (7 %) 23 (20 %) p = .020

Causes some intrusion—score

2 [n (%)]

4 (6 %) 11 (9 %) p = .415

Substantial intrusion—score 3

[n (%)]

0 (-) 2 (2 %) p = .525

Any—score 1–3 [n (%)] 9 (13 %) 36 (31 %) p = .005

Abnormal idiosyncratic negative response to specific

sensory stimuli (ever):

Mild reaction—Score 1 [n

(%)]

7 (10 %) 26 (22 %) p = .030

Causes some intrusion—score

2 [n (%)]

4 (6 %) 14 (12 %) p = .202

Substantial intrusion—score 3

[n (%)]

0 (-) 3 (3 %) p = .287

Any—score 1–3 [n (%)] 11 (15 %) 43 (37 %) p = .001

SSP domains

SSP total Definite difference [n (%)] 23 (32 %) 76 (66 %) p \ .001 Taste/smell sensitivity Definite difference [n (%)] 9 (13 %) 41 (35 %) p = .001

Movement sensitivity Definite difference [n (%)] 12 (17 %) 34 (29 %) p = .050

Under-responsive/seeks sensation Definite difference [n (%)] 23 (32 %) 72 (76 %) p \ .001 Auditory filtering Definite difference [n (%)] 35 (49 %) 81 (70 %) p = .004

Low energy/weak Definite difference [n (%)] 20 (28 %) 42 (36 %) p = .232

Visual/auditory sensitivity Definite difference [n (%)] 3 (4 %) 37 (32 %) p \ .001

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Table 3 Frequency and percentage of children who always or frequently displayed behaviours on the Short Sensory Profile

SEN

(N = 72)

ASD

(N = 116)

Chi-sqaure/Fisher’s

exact

Tactile sensitivity

1. Expresses distress during grooming 5 (7 %) 39 (34 %) p \ .001 2. Prefers long-sleeved clothing even when it is warm or short sleeves when it is

cold

8 (11 %) 20 (17 %) p = .296

3. Avoids going barefoot, especially in grass or sand 4 (6 %) 18 (16 %) p = .060

4. Reacts emotionally or aggressively to touch 5 (7 %) 15 (13 %) p = .231

5. Withdraws from splashing water 4 (6 %) 18 (16 %) p = .060

6. Has difficulty standing in line or close to other people 7 (10 %) 41 (35 %) p \ .001 7. Rubs or scratches out a spot that has been touched 5 (7 %) 12 (10 %) p = .602

Taste/smell sensitivity

8. Avoids certain tastes or food smells that are typically part of children’s diets 7 (10 %) 40 (34 %) p \ .001 9. Will only eat certain tastes 9 (13 %) 37 (32 %) p = .003

10. Limits self to particular food textures/temperatures 7 (10 %) 34 (29 %) p = .002

11. Picky eater, especially regarding food textures 14 (19 %) 41 (35 %) p = .020

Movement sensitivity

12. Becomes anxious or distressed when feet leave the ground 1 (1 %) 9 (8 %) p = .092

13. Fears falling or heights 4 (6 %) 22 (19 %) p = .009

14. Dislikes activities where head is upside down 12 (17 %) 24 (21 %) p = .496

Underresponsive/seeks sensation

15. Enjoys strange noises/seeks to make noise for noise’s sake 11 (15 %) 45 (39 %) p = .001

16. Seeks all kinds of movement and this interferes with daily routines 24 (33 %) 58 (50 %) p = .025

17. Becomes overly excitable during movement activity 13 (18 %) 39 (34 %) p = .020

18. Touches people and objects 15 (21 %) 46 (40 %) p = .007

19. Doesn’t seem to notice when face or hands are messy 20 (28 %) 40 (34 %) p = .338

20. Jumps from one activity to another so that it interferes with play 15 (21 %) 39 (34 %) p = .060

21. Leaves clothing twisted on body 10 (14 %) 46 (40 %) p \ .001 Auditory filtering

22. Is distracted or has trouble functioning if there is a lot of noise around 32 (44 %) 75 (67 %) p = .007

23. Appears to not hear what you say 21 (29 %) 63 (54 %) p = .001

24. Can’t work with background noise 6 (8 %) 25 (22 %) p = .025

25. Has trouble completing tasks when the radio is on 12 (17 %) 33 (28 %) p = .066

26. Doesn’t respond when name is called but you know the child’s hearing is ok 10 (14 %) 39 (34 %) p = .003

27. Has difficulty paying attention 30 (42 %) 70 (60 %) p = .013

Low energy/weak

28. Seems to have weak muscles 7 (10 %) 25 (22 %) p = .045

29. Tires easily, especially when standing or holding particular body position 12 (17 %) 25 (22 %) p = .413

30. Has weak grip 7 (10 %) 17 (15 %) p = .375

31. Can’t lift heavy objects 8 (11 %) 25 (22 %) p = .078

32. Props to support self 8 (11 %) 16 (14 %) p = .592

33. Poor endurance/tires easily 10 (14 %) 27 (24 %) p = .089

Visual auditory sensitivity

34. Responds negatively to unexpected or loud noises 3 (4 %) 43 (37 %) p \ .001 35. Holds hands over ears to protect ears from sound 7 (10 %) 47 (41 %) p \ .001 36. Is bothered by bright lights after others have adapted to the light 2 (3 %) 19 (16 %) p = .004

37. Watches everyone when they move around the room 16 (22 %) 24 (21 %) p = .803

38. Covers eyes or squints to protect eyes from light 3 (4 %) 21 (18 %) p = .006

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impairments (albeit aged 3–6 years) who were reported as

having a probable (13 %) or definite (3 %) difference in

total SSP scores (Tomchek and Dunn 2007). Multiple

hyper-sensitivities (i.e. tactile, taste/smell, and noise) were

much more common in ASD than in the SEN group, as was

severity of hypersensitivity and impact particularly from

noise as shown on ADI score. Sensory interests were more

common in the ASD than SEN group.

Our findings support the inclusion of atypical sensory

responsivity to the environment in the DSM-5 diagnostic

criteria but emphasise that such behaviours are not unique

to ASD; one feature does not make a diagnosis, other

features remain essential. The findings are also supportive

of the hypothesis that sensory symptoms are a non-specific

indicator of brain functional network difference in devel-

opmental psychopathology (Levit-Binnun et al. 2013).

The association of atypical sensory behaviours with

restricted, repetitive and stereotyped behaviours, but not

IQ, are consistent with those of Boyd et al. (2010), Mandy

et al. (2012), Dar et al. (2012) and Wigham et al. (2015)

but inconsistent with Lane et al. (2014) who found hyper-

sensitivity and generalised reactivity to differ by age and

IQ but not ASD severity (as measured by the ADOS

whereas we included history from the ADI-R and ADOS).

We did not explore sensory subtypes but other studies have

found individual sensory subtypes e.g. tactile responsive-

ness patterns in ASD, to be only weakly (or not at all)

correlated with repetitive behaviours and extent of social

impairment (Foss-Feig et al. 2012). Some aspects of

atypical sensory behaviours, e.g. sensory interests, in ASD

may be an expression of positive absorption in a detail of

the environment similar to other restricted and repetitive

behaviours.

Our finding of an association between atypical sensory

behaviours and increased emotional symptoms in ASD is

consistent with the literature showing a potential link

between sensory symptoms and anxiety (Lane et al. 2012)

and depression (Bitsika et al. 2016) although the direction

of effect is not known. Further research is required for a

better understanding of the inter-relationship between aut-

ism, comorbidities and sensory symptoms and, how these

may change over time (Chen et al. 2009; McCormick et al.

2015). Anecdotally, many sensory symptoms persist into

adult life and continue to have a significant impact on

individuals.

Assessing sensory behaviours is limited by the current

methods available, usually through questionnaires com-

pleted by parent or carers or individuals themselves rather

than objective measures (Tavassoli et al. 2016). The SSP

has been widely used clinically and in research studies but

for some items the face validity as a ‘sensory’ behaviour is

unclear e.g. ‘Has a weak grasp’. Some clinically important

items are not recorded in the SSP, for example lack of

response to pain and lack of awareness of temperature,

which are hypo-responsivities frequently commented on by

parents. Thus, for this study we used complete SSP

domains for hypersensitivity but for hyposensitivity, one

domain and two items met face validity as representing

Table 4 Multiple regression results for Short Sensory Profile

Total Scores and features of

Autism and behavioural factors

as report on the parent SDQ

Coefficient t 95 % CI p

Full scales

F(6108) = 6.50, p \ .001, R2 = .224 IQ .150 1.58 -.038, .337 .117

ADOS age years -.235 -0.10 -4.92, 4.45 .921

ICD 10 total -.066 -0.06 -2.34, 2.20 .954

ADI-R total -.709 -3.42 -1.12, -.298 .001

ADOS G total .370 0.90 -.448, 1.19 .372

SDQ total -1.58 -3.79 -2.40, -.752 \.001 Subscales

F(10,101) = 3.41, p \ .001, R2 = .253 ICD 10_social 2.20 0.91 -2.57, 6.96 .362

ICD 10 communication -1.87 -0.74 -6.83, 3.10 .458

ICD 10 repetitive -5.50 -2.18 -10.5, -.510 .031

SDQ emotional -2.54 -2.96 -4.24, -.834 .004

SDQ conduct -1.18 -1.21 -3/12, .750 .228

SDQ peer relations -1.70 -1.45 -4.03, .621 .149

SDQ hyperactivity -.038 -0.04 -2.09, 2.01 .971

SDQ pro-social -.043 -0.05 -1.87, 1.79 .963

CI confidence interval; Rfsiq Raven’s full scale IQ; ADOS Autistic Diagnostic Observation Scale-Generic;

ICD International Classification of Diseases; SDQ Strengths and Difficulties Questionnaire

3604 J Autism Dev Disord (2016) 46:3597–3606

123

under-responsiveness to sensory stimuli. This aspect of

behaviour may therefore have been underestimated.

Strengths of the study are a well characterised sample, the

use of a recognised sensory questionnaire and a comparison

group who have special educational needs and are a group

in which ASD is often considered as a differential

diagnosis.

In summary, the inclusion of hyper-or hypo respon-

sivity or sensory interests within the ASD diagnostic cri-

teria of DSM-5 is supported. However, comparison of

children with ASD to those with SEN affirms the finding

that young people with other developmental disorders may

also demonstrate altered sensory responsivity. In ASD

altered sensory function was associated with emotional

problems and restricted repetitive behaviours. It remains to

be seen if the profile of sensory responsivities differs

between neurodevelopmental disorders, how these may

differentially impact on function and participation and how

these may change over time.

Acknowledgments We are grateful to the children and families and the clinical teams in South Thames, whose participation and collab-

oration made the study possible.

Funding This study was funded by the Wellcome Trust and the Department of Health (Grant Number 039/0026).

Author Contributions All of the individuals listed as authors on this manuscript contributed to the study design, data collection and or data

analysis along with manuscript preparation. All authors have read the

manuscript and agreed to its submission for publication. All authors

meet the appropriate authorship criteria, nobody who qualifies for

authorship has been omitted, all contributors and funding sources

have been properly acknowledged, and authors and contributors have

approved the acknowledgement of their contributions.

Compliance with Ethical Standards

Conflict of interest Dr Green declares that she has no conflict of interest. Dr Chandler declares that she has no conflict of interest. Prof

Charman declares that he has no conflict of interest. Prof Simonoff

declares that she has no conflict of interest. Prof Baird declares that

she has no conflict of interest.

Ethical Approval All procedures performed in studies involving human participants were in accordance with the ethical standards of

the institutional and/or national research committee and with the 1964

Helsinki declaration and its later amendments or comparable ethical

standards.

Informed Consent Informed consent was obtained from all parents for their and their child’s participation in the study.

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