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RESEARCH ARTICLE

Classification of Children With Autism Spectrum Disorder by Sensory


Subtype: A Case for Sensory-Based Phenotypes
Alison E. Lane, Cynthia A. Molloy, and Somer L. Bishop

This study examines whether sensory differences can be used to classify meaningful subgroups of children with autism
spectrum disorder (ASD). Caregivers of children with ASD aged 2–10 years (n = 228) completed the Short Sensory Profile.
Model-based cluster analysis was used to extract sensory subtypes. The relationship of these subtypes to age, gender,
autism symptom severity, and nonverbal intelligence quotient (IQ) was further explored. Four distinct sensory subtypes
were identified: (a) sensory adaptive; (b) taste smell sensitive; (c) postural inattentive; and (d) generalized sensory
difference. The sensory subtypes differ from each other on two dimensions: (a) the severity of reported sensory differences;
and (b) the focus of differences across auditory, taste, smell, vestibular and proprioceptive domains. Examination of the
clinical features of each subtype reveals two possible mechanisms of sensory disturbance in autism: (a) sensory hyper-
reactivity; and (b) difficulties with multisensory processing. Further, the sensory subtypes are not well explained by other
variables such as age, gender, IQ, and autism symptom severity. We conclude that classification of children using sensory
differences offers a promising method by which to identify phenotypes in ASD. Sensory-based phenotypes may be useful
in identifying behavioral features responsive to specific interventions thereby improving intervention effectiveness.
Further validation of the sensory-based phenotypes by establishing neural and physiological correlates is recommended.
Autism Res 2014, 7: 322–333. © 2014 International Society for Autism Research, Wiley Periodicals, Inc.

Keywords: sensory; autism; phenotypes; subtypes; children; classification; model-based cluster analysis; Short Sensory Profile

Introduction higher levels of sensory hyperreactivity predicted higher


levels of repetitive behaviors in ASD, and sensory seeking
Previous studies have reported that many children with was associated with ritualistic/need for sameness behav-
autism spectrum disorder (ASD) exhibit behaviors and iors. Others have observed significant associations
emotional responses associated with sensory differences, between sensory hyperreactivity and social communica-
such as sensory hyperreactivity (e.g., covering ears to loud, tion, social motivation, and performance of social activi-
unexpected sounds), sensory hypo-reactivity (e.g., failure ties [Hilton et al., 2007; Reynolds, Bendixen, Lawrence, &
to react to painful stimuli), and sensory seeking (e.g., Lane, 2011]. In Lane et al. [2010], maladaptive behaviors
licking or smelling objects) [Baker, Lane, Angley, & Young, and communication competence varied depending on
2008; Baranek, Boyd, Poe, David, & Watson, 2007; Rogers sensory subtype in autistic disorder.
& Ozonoff, 2005; Tomchek & Dunn, 2007]. These differ- Findings such as these support the hypothesis that
ences are unrelated to sensory loss (i.e., hearing loss, visual close examination of sensory differences may elucidate
impairment, etc.) and are significantly more prevalent in behavioral subgroups or phenotypes of children with
children with ASD than in typically developing children ASD. A phenotype is the classification of disorder based
[Ben-Sasson et al., 2009]. Individuals with ASD and their on specific physical and behavioral characteristics that
families report that sensory differences contribute signifi- are considered relevant to its further understanding or
cantly to caregiver burden and social isolation [Koenig & management [Center for the Study of Language and
Kinnealey, 2008]. Moreover, sensory differences have been Information, Stanford University, 2013]. Phenotyping
included in the DSM-5 diagnostic criteria for ASD efforts in complex neurodevelopmental disorders such as
[American Psychiatric Association, 2013]. Recently, asso- ASD are considered critical to the identification of sub-
ciations have been made between patterns of sensory groups of children who are similar to each other behav-
difference and the core deficits of ASD [Boyd et al., 2010; iorally and who may, therefore, share etiological
Hilton, Graver, & LaVesser, 2007; Lane, Young, Baker, & similarities and/or respond similarly to intervention
Angley, 2010]. Specifically, Boyd et al. [2010] reported that [Gottesman & Gould, 2003].

From the School of Health Sciences, University of Newcastle, Callaghan, New South Wales, Australia (A.E.L.); Harrison Community Network, Harrison,
Ohio (C.A.M.); Center for Autism and the Developing Brian (CADB), Weill Cornell Medical College, White Plains, New York (S.L.B.)
Received May 22, 2013; accepted for publication January 24, 2014
Address for correspondence and reprints: Alison E. Lane, School of Health Sciences, University of Newcastle, University Drive, Callaghan, NSW 2308,
Australia. E-mail: alison.lane@newcastle.edu.au
Published online 17 March 2014 in Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/aur.1368
© 2014 International Society for Autism Research, Wiley Periodicals, Inc.

322 Autism Research 7: 322–333, 2014 INSAR


Phenotyping efforts in ASD have considered features described as: (a) mild sensory differences with a focus in
such as face processing abilities, sensitivity to social auditory filtering and seeking difficulties; (b) moderate
reward, motor imitation, memory, executive function, sensory differences with extreme difficulties in taste/
language ability, and restricted and repetitive behaviors smell sensitivity; and (c) moderate–severe sensory differ-
[Bishop et al., 2013; Dawson et al., 2002; Lord, Leventhal, ences in all sensory domains. Classification of children
& Cook, 2001]. Barriers to the utility of these features as with ASD using the sensory subtypes proposed by Lane
a means of ASD phenotyping include that many are dif- and colleagues allows for more systematic examination of
ficult to measure reliably in children younger than 3 years behavioral and symptom profiles. Preliminary work sug-
of age and in some individuals with severe autism symp- gests that children with ASD whose sensory differences
toms or cognitive impairments. Further, differences in are characterized by extreme taste and smell sensitivity
language function and sensitivity to social reward, once appear to have more severe communication impairments
emerging sufficiently to allow reliable observation, may and are pickier eaters [Lane, et al., in press; Lane et al.,
not be useful in the early identification of ASD. A system- 2010]. Further, children experiencing the highest fre-
atic investigation of sensory-based phenotypes in ASD, quency of sensory differences display more maladaptive
however, is indicated given the frequency of reported behavior [Lane et al., 2010].
difficulties in this area and preliminary indicators of Methodological issues, however, limit this preliminary
strong links between sensory differences and specific work. First, detailed examinations of systematic variance
symptom and behavioral profiles [Boyd et al., 2010; Lane in behavior and symptoms require large sample sizes for
et al., 2010]. Additionally, sensory differences, as one conclusive findings. Second, only one study to date has
aspect of a temperament profile, may be observable in included representation across the full spectrum of ASD.
early infancy prior to the time when clinically significant This limits conclusions being made about the role of
ASD symptoms are recognized [Baranek, 1999; Clifford autism symptom severity and IQ in the expression of
et al., 2013]. sensory differences. Third, studies to date have mea-
Previous studies have explored sensory differences sured sensory differences at differing time points in the
within subgroups of children with ASD further strength- care path of the participants. Some participants were
ening the case for the development of sensory-based ASD newly diagnosed, while others had received several
phenotypes. In a study by Liss, Saulnier, Fein, and years of intervention. It is possible, therefore, that some
Kinsbourne [2006], sensory hyperreactivity was found to of the variance in sensory differences reported previ-
be a discriminating characteristic of individuals with ously in ASD samples is related more to intervention
ASD, over-focused attention, exceptional memory, and experience rather than to features inherent to the
perseverative behavior. Further, Ausderau et al. [2013], disorder.
report that autism severity and developmental function- This study proposes to examine further the case for
ing varied on the basis of sensory differences. Specifically, sensory-based phenotypes in ASD by answering the fol-
increased sensory differences were associated with lowing questions:
increased autism severity and lower IQ. In work by Lane
1. What are the sensory subtypes in a large sample of
and colleagues, distinct sensory subtypes within ASD
children at the time of their ASD diagnosis? How do
have been identified. First, Lane and colleagues [2010]
these subtypes compare to those reported in previous
identified a triad of sensory subtypes in children with
sensory subtype investigations?
autistic disorder (n = 54), aged 3–8 years using the Short
2. What is the relationship between sensory subtype, age,
Sensory Profile [SSP; McIntosh, Miller, & Shyu, 1999a]. A
gender, autism symptom severity, and IQ?
novel analysis technique, model-based cluster analysis,
was applied to examine trends in the presentation of This study addresses the limitations of previous enqui-
sensory differences. Subtypes were distinguishable from ries by: (a) analyzing data from a large sample of children
each other on the basis of the frequency of reported with ASD; (b) establishing sensory differences at the point
differences in attending to relevant auditory stimuli in of diagnosis; and (c) examining sensory difference along-
the context of a busy background, hypo-reactivity and side comprehensive behavioral and diagnostic data col-
sensory seeking (low, medium, and high frequency of lected using a standard protocol. Based on the previous
symptoms), and the sensory modalities most affected. literature, we hypothesized that at the time of diagnosis,
Response to taste, smell, movement, and proprioceptive children with an ASD would exhibit sensory differences
sensation varied most between the three subtypes [Lane that vary in severity, and are characterized by focal diffi-
et al., 2010]. Lane, Dennis, and Geraghty [2011] repli- culties in auditory filtering, hypo-reactivity, sensory
cated and refined these findings in an independent seeking, taste/smell sensitivity, and vestibular and pro-
sample of 30 children with autistic disorder and pervasive prioceptive processing. Further, these differences will
developmental disorder—not otherwise specified. These conform to a subtype structure similar to that reported in
authors concluded that sensory subtypes were best Lane et al. [2010, 2011]. In relation to the second study

INSAR Lane et al./Sensory phenotypes in autism 323


question, we hypothesize that: more frequent sensory from the site database by facility staff, blind to the objec-
differences will be related to increased autism symptom tives of the study. Prepared data were then forwarded to
severity; lower developmental functioning (assessed by the first author for analysis (described below). Appropri-
age and IQ) will be related to increased sensory differ- ate approvals for the study were gained from the relevant
ences; and no sensory differences will be apparent Institutional Review Boards.
between males and females. All participants were administered diagnostic and other
measures by trained clinicians using approved ATN pro-
tocols. This multidisciplinary assessment included inde-
Methods pendent evaluations by a developmental pediatrician,
Participants child psychologist, and speech-language pathologist. Fol-
lowing this assessment, a diagnosis of ASD was made by
Participants for this study were individuals presenting to
the developmental pediatrician. All data included in this
a major, Midwestern US autism specialist center for diag-
study were collected at or close to the time of diagnosis.
nostic assessment of ASD between 2008 and 2010. Par-
The ATN protocol requires that all assessments be com-
ticipants were included in the study if: (a) they were
pleted within 9 months of each other.
ultimately diagnosed with an ASD by the evaluation
team; and (b) they completed the comprehensive battery Instrumentation
of diagnostic evaluations provided by the center. All par-
ticipants were aged between 2–10 years, which aligns Instruments used to evaluate the key study variables are
with the recommended age range for the primary described below.
measure of sensory differences (discussed below) and pre- 1. Autism symptom severity was calculated using the Cali-
vious studies investigating sensory subtypes. A total of brated Severity Score (CSS) from the Autism Diagnosis
228 participants met the above criteria and were included Observation Schedule [ADOS; Lord et al., 2000]. The
in the study. Table 1 provides a description of the partici- ADOS is a well-established, standardized diagnostic
pant characteristics. tool for ASD. Four different modules of the ADOS are
available for use depending on the expressive language
Procedure and Design skills of the child. In this study modules 1–3 only were
used (module 1: n = 108; module 2: n = 64; module 3:
This study involved the secondary analysis of data col- n = 52). Module 1 is intended for children who are
lected at the specialist center. The center is a member of preverbal or with very limited language abilities (i.e.,
the Autism Treatment Network (ATN) and follows a no more than single words or short phrases), module 2
nationally derived consensus protocol for the evaluation is intended for children who use flexible phrase
and management of children with ASDs (http:// speech, and module 3 is intended for children who use
www.autismspeaks.org/science/programs/atn/index.php complex sentences, which are defined as sentences
#ATN). Data used in this study were sourced from a data- with two or more clauses.
base maintained by the center. De-identified data pertain- 2. Nonverbal IQ (NVIQ) was used to estimate each child’s
ing to the variables of interest in this study were extracted cognitive ability. NVIQ has been found to be more

Table 1. Participant Characteristics

n Mean Standard deviation Range

All participants age (months) 228 60.71 26.86 24–130


Male age 203 60 26.15 24–130
Female age 25 66.44 32.01 26–130
Nonverbal IQ 174 72.43 23.08 21–132
ADOS CSS 224 6.84 1.82 2–10
SSP 228
Tactile 226 26.91 5.58 10–35
Taste/smell sensitivity 226 12.47 5.69 4–20
Movement sensitivity 228 12.69 2.99 3–15
Under-responsive/Seeks sensation 226 21.25 6.39 7–35
Auditory filtering 228 17.19 5.04 6–30
Low energy weak 228 24.94 6.69 6–30
Visual/Auditory aensitivity 223 17.47 4.79 5–25
SSP overall 223 132.89 25.04 52–179

ADOS CSS, Autism Diagnostic Observation Schedule Calibrated Severity Score; SSP, Short Sensory Profile.

324 Lane et al./Sensory phenotypes in autism INSAR


stable than verbal IQ (VIQ) in children with ASD Table 2. Example Short Sensory Profile Items
[Begovac, Begovac, Majic, & Vidovic, 2009] and is less
SSP domain Example items
confounded with language ability. NVIQ was calculated
in two ways depending on the test that was adminis- Tactile sensitivity Item 4: Reacts emotionally or aggressively to
tered. Younger children or children with significant touch
cognitive impairments were administered the Mullen Item 7: Rubs or scratches out a spot that has been
touched
Scales of Early Learning [MSEL; Mullen, 1995]. The
Taste/Smell Item 8: Avoids certain tastes or food smells that
MSEL is a standardized assessment of development and sensitivity are typically part of children’s diets
provides scores for gross motor, fine motor, visual Item 10: Will only eat certain tastes
reception (nonverbal problem solving), receptive lan- Movement Item 13: Fears falling or heights
guage, and expressive language. The MSEL does not sensitivity Item 14: Dislikes activities where head is upside
down (for example, somersaults, roughhousing)
yield separate NVIQ scores, so it was necessary to cal-
Under-responsive/ Item 18: Touches people and objects
culate a nonverbal ratio IQ (also called a deviation IQ). Seeks sensation Item 19: Doesn’t seem to notice when face or
This was done by dividing the child’s nonverbal mental hands are messy
age by his/her chronological age and multiplying by Auditory filtering Item 22: Is distracted or has trouble functioning if
100 [see Bishop, Guthrie, Coffing, & Lord, 2011]. there is a lot of noise around
Item 26: Doesn’t respond when name is called but
you know the child’s hearing is OK
Older children, who were cognitively capable of doing
Low energy/Weak Item 29: Tires easily, especially when standing or
so, completed the Stanford Binet 5th Edition [SB5; Roid, holding particular body position
2003]. The SB5 is designed for individuals aged 2–85+ Item 32: Props to support self (even during
years and yields separate NVIQ and VIQ scores. For activity)
children who received the SB5, a standard NVIQ score Visual/Auditory Item 34: Responds negatively to unexpected or
sensitivity loud noises
was used.
Item 38: Is bothered by bright lights after others
Complete NVIQ data were available for 174 partici- have adapted to the light
pants in our sample. Table 1 details the mean NVIQ
scores for the sample. Participants without available
NVIQ data were generally determined by the evaluating
Analysis
psychologist to be unable to participate in or complete
reliable IQ testing. Statistical analyses were conducted using the Statistical
Package for the Social Sciences (SPSS v 19.0, New York,
3. Sensory differences were assessed in our sample using New York, USA) and R (v 2.15, Vienna, Austria). Descrip-
the Short Sensory Profile (SSP). The SSP is a 38-item tive statistics for all key variables were generated for the
parent questionnaire designed to measure behaviors sample. Model-based cluster analysis [mclust: Zhong &
associated with differences in the modulation of Ghosh, 2003] was applied to SSP scores to identify
everyday, environmental sensory stimuli in children sensory subtypes and address study question 1. Standard-
aged 3–10 years [McIntosh et al., 1999a]. Scores are ized z-scores from the seven SSP sensory domains (Miller
derived for seven domains: (a) tactile; (b) taste/smell; & Schoen, personal communication) were submitted to
(c) movement; (d) visual/auditory sensitivity; (e) this analysis replicating the method used in previous
under-responsive/seeks sensation; (f) auditory filter- studies [Lane et al., 2010, 2011].
ing; and (g) low energy/weak, and for overall sensory Z-scores correspond to the number of standard devia-
modulation function. Example items for each of the tions above or below the normative mean. Based on the
seven domains are listed in Table 2. Scores on each SSP interpretation guide, z-scores at or above −1 are clas-
SSP domain are then compared to normative data sified as “Typical Performance.” Z-scores that fall between
from 1,200 typically developing children. Higher −1 and −2 are classified as “Probable Difference.” In the
scores relate to more typical performance, whereas case where an individual scores within the “Probable
lower scores indicate that either a probable or definite Difference” range, supporting observations from other
difference in sensory function is likely. Internal con- sources, e.g., parent or teacher comments, clinical obser-
sistency of overall and subdomain sections of the SSP vations, are used to determine if this sensory area is
has been reported as ranging between r = 0.70–0.90 impacting on functional performance. Z-scores that fall
along with acceptable discriminative validity (>95% below −2 are considered to indicate “Definite Difference,”
in differentiating children with and without sensory and these sensory areas are likely to be functionally lim-
impairments) [McIntosh et al., 1999a; McIntosh, iting [McIntosh et al., 1999a]. Further, the Sensory Pro-
Miller, Shyu, & Hagerman, 1999b]. The SSP and its cessing Disorder research consortium uses the following
parent measure, the Sensory Profile, are used exten- guidelines to identify clinical cases: Total SSP score
sively in clinical practice. > = −3.0 OR two or more SSP domains > = −2.5 OR one SSP

INSAR Lane et al./Sensory phenotypes in autism 325


domain > = −4.0 (Miller & Schoen, personal communica-
tion). We adopted the guidelines from both the SSP
manual and the Sensory Processing Disorder research
consortium to guide our interpretation of sensory
subtypes.
Model-based cluster analysis compares the fit to the
data of a number of possible models using the Bayesian
Information Criteria (BIC) to determine the best model
[Zhong & Ghosh, 2003]. A high BIC indicates that an
optimal trade-off between the fit of the model to the data
and the complexity of the model (i.e., numbers of clusters
or numbers of parameters) has been achieved. Use of the
BIC allows simultaneous comparison of a number of dif-
ferent cluster models that have differing complexity. This
clustering technique has the advantage over traditional
hierarchical methods that only consider proximity of
scores to each other but not the complexity of the model.
One-way analysis of variance (ANOVA) with Tukey post-
hoc analyses was used to determine the sensory differ-
Figure 1. Bayesian Information Criteria values for each Gaussian
ences between clusters.
model (each represented by a different icon) considered in the
After classification of each child into a sensory subtype, analysis. Each Gaussian model used in this analysis is identified in
one-way ANOVA was used to examine differences in age, the figure legend by a combination of the letters E, V, and I. The
autism symptom severity, and NVIQ between sensory sequence of the letters indicates specific variance and geometric
subtypes (study question 2). Differences in gender features of each model. For a detailed description of this method-
between subtypes were determined using chi-square ology, please see Fraley and Raftery [2007].
analysis.
40.2%) displays clinically significant differences in taste/
smell sensitivity but typical function in low energy weak;
Results
cluster 3 (n = 23, 10.3%) displays typical function in
taste/smell sensitivity but clinically significant difference
Table 1 reports the descriptive results for key variables of
in low energy weak; and cluster 4 (n = 29, 12.1%) is char-
interest in this study. Chronological age was calculated
acterized by clinically significant differences in both
from the date of SSP administration. As NVIQ data were
taste/smell sensitivity and low energy weak.
not available for all participants, one-way ANOVA was
One-way ANOVAs with Tukey post-hoc analyses further
used to compare participants with (n = 174) and without
clarified the differences in SSP domain scores between
(n = 54) NVIQ scores on age, gender, and sensory subtype
clusters (Table 3). First, all clusters display some differ-
membership to examine equivalence between the groups.
ences from typical in the domains of auditory filtering
No significant differences were found between groups
and under-responsive/seeks sensation. These differences
(age: P = 0.43; gender: P = 0.59; subtype: P = 0.11).
are mild in cluster 1, moderate in clusters 2 and 3, and
severe in cluster 4. Second, cluster 1 displays no differ-
Sensory Subtypes in ASD ences in any other domain. Third, cluster 2 displays an
extreme score in the area of taste/smell sensitivity, and
A four cluster solution was determined to be the most
cluster 3 displays an extreme score in low energy weak.
parsimonious and interpretable after inspection of the
Fourth, cluster 4 displays differences in all domains and is
BIC values and consideration of five, six, seven, and eight
the only cluster to show atypical movement sensitivity.
cluster solutions. Figure 1 shows a comparison of the
On the basis of these results, we propose that each
BICs for each model considered in the analysis. As can be
cluster corresponds to a distinct sensory subtype in ASD.
seen, the value of the BIC peaks at four components
The subtypes are characterized as follows:
(clusters). The four cluster solution is presented in
Figure 2. Visual inspection indicated that these clusters 1. Sensory adaptive (Cluster 1)—typical function in five
are most clearly distinguishable when viewing the of the seven sensory domains; mild elevation in audi-
scatterplot of taste/smell sensitivity against low energy tory filtering and under-responsive/seeks sensation;
weak scores. In the cluster solution for our sample, cluster participants classified in this cluster do not meet the
1 (n = 84, 37.5%) displays typical function on both taste/ criteria for clinical cases of sensory processing disorder
smell sensitivity and low energy weak; cluster 2 (n = 92, as described in the “Analysis” section and, therefore,

326 Lane et al./Sensory phenotypes in autism INSAR


it is considered unlikely that the sensory diffe- 4. Generalized sensory difference (Cluster 4)—all
rences observed are strongly impacting functional sensory domains are affected including movement
performance. sensitivity.
2. Taste/Smell sensitive (Cluster 2)—extreme taste/smell
sensitivity and clinically significant concerns in audi-
Sensory Subtypes and Age, Gender, Autism Symptom
tory filtering and under-responsive/seeks sensation; no Severity, and NVIQ
differences noted in domains assessing movement and
proprioceptive function. Table 4 reports age, gender, autism symptom severity (as
3. Postural inattentive (Cluster 3)—extreme score in low measured by the ADOS CSS), and NVIQ data by sensory
energy weak and clinically significant concerns in audi- subtype. As can be seen, no differences emerged between
tory filtering and under-responsive/seeks sensation. sensory subtypes on the basis of gender or autism
symptom severity.
Statistically significant differences were observed,
however, between subtypes on the basis of age and NVIQ.
Post-hoc analyses clarified these differences. In terms
of age, subtype taste/smell sensitive was significantly
younger than subtype postural inattentive. There were no

Table 4. Age, Gender, nonverbal IQ and Autism Symptom


Severity by Sensory Subtype

NVIQ (SE) ADOS CSS (SD)


Subtype Age (SE) Gender (n = 174) (n = 224)

SA 4.93 Male = 77 75.71 6.79


Cluster 1 (0.22) Female = 7 (2.90) (1.63)
(n = 84)
TSS 4.70* Male = 78 65.61* 6.92
Cluster 2 (0.23) Female = 14 (2.37) (1.97)
(n = 92)
PI 6.02* Male = 20 80.32* 7.0
Cluster 3 (0.54) Female = 3 (5.40) (1.57)
(n = 23)
GSD 5.79 Male = 28 78.23 6.59
Cluster 4 (0.46) Female = 1 (5.90) (2.10)
(n = 29)
Figure 2. Model-based cluster solution on sensory features—“0”
Statistic F = 3.42 χ2 = 4.08 F = 4.00 F = .31
represents the normative mean for performance (i.e., typical per-
df = 3, 224 df = 3,170 df = 3,220
formance) on the sensory domain. Values above and below “0” P value 0.02 0.25 0.009 0.82
indicate the number of standard deviations from the normative
mean. Values above 0 and between 0 and −1 indicate no sensory SA, sensory adaptive; TSS, taste/smell sensitive; PI, postural inatten-
impairment; between −1 and −2 indicate mild sensory impairment; tive; GSD, Generalized Sensory Difference; ADOS CSS, Autism Diagnostic
below −2 indicate clinically significant sensory impairment. Each Observation Schedule Calibrated Severity Score; SD, standard deviation; SE,
icon represents a single case. standard error.

Table 3. Mean Short Sensory Profile Z-Scores by Cluster

Cluster (n) Tactile (SD) Taste smell (SD) Movement (SD) Under seeks (SD) Aud filter (SD) Low energy weak (SD) Visual aud sens (SD)

1 (84) −0.84 0.99 −0.29 −1.74 −1.96 −0.13 −0.58


(1.38) (1.15) (1.27) (1.93) (1.6) (0.71) (1.4)
2 (92) −1.97 −4.10 −0.61 −2.77 −2.78 −0.43 −1.23
(1.78) (1.32) (1.44) (1.99) (1.63) (0.99) (1.5)
3 (23) −1.59 0.76 −0.65 −2.88 −2.78 −4.32 −1.36
(1.34) (1.2) (1.22) (2.22) (1.26) (1.23) (1.24)
4 (29) −3.34 −4.48 −1.86 −4.16 −3.76 −5.49 2.56
(2.27) (1.11) (1.86) (2.01) (1.6) (1.47) (1.82)
P value 0.001 0.001 0.001 0.001 0.001 0.001 0.001

Under seeks, under-responsive/seeks sensation; Aud filter, auditory filtering; Visual aud sens, visual auditory sensitivity.

INSAR Lane et al./Sensory phenotypes in autism 327


2. Taste smell sensitive—characterized by extreme taste
and smell sensitivity alongside moderate-level con-
cerns in auditory filtering and under-responsive/seeks
sensation.
3. Postural inattentive (new)—characterized by extreme
difficulties in postural processing alongside moderate-
level concerns in auditory filtering and under-
responsive/seeks sensation.
4. Generalized sensory difference—experiences signifi-
cant difficulties across all areas of sensory difference.

In general, the subtypes differ from each other on the


basis of the severity of differences in auditory filtering
and under-responsive seeks sensation and in the focus of
differences in areas of taste/smell sensitivity and low
energy weak.
Of note is the large proportion (37.5%) of the sample
that met criteria for the subtype, sensory adaptive. This
Figure 3. Mean nonverbal IQ scores by sensory subtype. finding is in contrast to previous studies that have esti-
mated the prevalence of sensory differences in ASD as
high as 92% [Tomchek & Dunn, 2007]. Sampling strategy
significant differences in age between sensory adaptive,
differences between studies may explain this result. Our
postural inattentive, and generalized sensory difference.
study was based on a representative referral sample (all
In terms of NVIQ, subtype taste/smell sensitive was sig-
those presenting for diagnosis of ASD) rather than a con-
nificantly lower than subtype postural inattentive. No
venience sample. Estimates of the prevalence of sensory
other significant differences between subtypes were
differences in ASD may have been inadvertently inflated
observed for NVIQ. Figure 3 displays mean NVIQ scores
in previous studies by recruitment practices. Parents of
and standard error for each subtype.
children with ASD and significant sensory differences
may have been over-represented in studies where the
research aims were focused on sensory issues. A further
Discussion
difference between our study and previous investigations
is that sensory differences were assessed for all partici-
The purpose of our study was to examine further the case
pants at or close to the time of diagnosis. While some
for sensory-based phenotypes in ASD by (a) identifying
children with ASD receive general developmental inter-
sensory subtypes in a large sample of children with ASD
vention prior to diagnosis, it can be inferred that the
and (b) establishing the relationship between these sub-
findings of the current study represent baseline sensory
types and age, gender, NVIQ, and autism symptom sever-
differences prior to implementation of autism-specific
ity. Exploration of these questions in a large sample of
intervention strategies. The finding suggests that many
children with ASD was indicated given promising pre-
children with ASD do not experience functionally limit-
liminary results in other studies.
ing sensory differences at diagnosis and, therefore, may
Partial replication and further refinement of the sub-
not benefit from sensory-based therapies. Subsequently,
types reported by Lane et al. [2010, 2011] is evident in this
this finding lends support to the utility of sensory differ-
study. Previously, three general sensory subtypes have
ences as a means of distinguishing clinically meaningful
been described including: (a) mild sensory difference with
subgroups or phenotypes within ASD. Moreover, classifi-
a focus in auditory filtering and seeking difficulties; (b)
cation of children presenting for diagnosis of ASD using
moderate sensory difference with extreme difficulties in
sensory subtypes will also assist in diagnosis using the
taste/smell sensitivity; and (c) moderate–severe sensory
DSM-5. Sensory differences are now listed as one possible
difference in all sensory domains [Lane et al., 2010, 2011].
manifestation of stereotypic and repetitive behaviors in
In the current study, we identified the same three general
the DSM-5 criteria. Establishing the sensory subtype of
subtypes and revealed a new, fourth subtype. The four
the child during the diagnostic evaluation provides an
sensory subtypes in this study are:
efficient means of identifying whether this sub-criteria
1. Sensory adaptive—predominantly typical sensory has been met.
function with mildly elevated scores in auditory filter- Further, examination of the nature of the behavioral
ing and under-responsive seeks sensation that are and sensory differences expressed in each subtype reveals
unlikely to be functionally limiting. two possible mechanisms of sensory disturbance in

328 Lane et al./Sensory phenotypes in autism INSAR


autism: (a) sensory hyperreactivity (taste smell sensitive elevated scores in these domains. It is possible that behav-
and generalized sensory difference); and (b) difficulties iors associated with hypo-reactivity are ubiquitous across
with multisensory processing (postural inattentive and individuals with ASD while presenting at different levels
generalized sensory difference). This schema incorporates of severity from mild, and not affecting function, to
and streamlines the current nosology of sensory differ- severe and functionally limiting. Close examination of
ence expressed as: sensory modulation disorder (hyperre- the items included on these domains of the SSP and their
activity, hypo-reactivity, and seeking), sensory-based relationship to the core symptoms of ASD may give
movement disorder, and sensory discrimination disorder insights into the underlying processes of the disorder. It
[Ausderau et al., 2013; Miller, Anzalone, Lane, Cermak, & is notable that both subtypes associated with sensory
Osten, 2007]. Individuals with ASD and sensory hyperre- hyperreactivity, taste/smell sensitive, and generalized
activity may be observed to display behaviors consistent sensory difference also displayed moderate–severe differ-
with intolerance and sensitivity to specific sensory stress- ences in hypo-reactivity. Two possible hypotheses for this
ors. For example, in our subtypes, children were reported finding are that: (a) a more general impairment of sensory
by their parents to exhibit heightened responses to select reactivity that includes both hyper- or hypo-reactive fea-
tastes and smells (taste smell sensitive and generalized tures is implicated in ASD or (b) that individuals with
sensory difference) and movement, tactile, visual, and sensory hyperreactivity engage in behaviors that mimic
auditory stimuli (generalized sensory difference). Simi- hypo-reactivity (i.e., withdrawal, failure to respond) as a
larly, individuals with ASD may also display behaviors means of managing an over-stimulating environment.
associated with difficulties with multisensory integration Alternatively, it is possible that the items included in the
or the simultaneous processing of multiple sensory SSP were insufficiently sensitive to true hypo-reactivity.
modalities or differing elements of a single modality (e.g., Future investigations focused on hypo-reactivity in ASD
pitch and loudness of an auditory stimulus). In our sub- should consider the best methods for identifying these
types, postural, coordination, and auditory filtering diffi- differences in children and explore their relationship to
culties may well have a base in impaired multisensory features of hyperreactivity.
integration. Impairment in the concurrent processing of The second major finding from our study is that, in
visual, proprioceptive, and vestibular sensory stimuli is general, sensory differences are not well explained by
likely to impact the maintenance of body position and variables such as age, NVIQ and autism symptom sever-
the production of coordinated movements such as reach- ity as measured by the ADOS CSS. This finding is in
ing [Izawa et al., 2012; Sober & Sabes, 2003]. Similarly, contrast to those of Ausderau et al. 2013 who reported
difficulties in identifying salient auditory stimuli within that autism symptom severity (measured using the
the context of multiple auditory and other sensory inputs Social Responsiveness Scale) was differentially impacted
(e.g., such as in a classroom) could lead to behaviors such by frequency of sensory differences. An important dif-
as those described in the auditory filtering domain of the ference between the current study and that by Ausderau
SSP. Additional support for these hypotheses is found et al. is in the methods used. In our study, we used
within the neurophysiological literature where observa- cluster analysis to identify groups of similar cases based
tions of differences in sympathetic nervous system on sensory differences, whereas Ausderau and colleagues
activation (sensory hyperreactivity) and multisensory were focused on detailing similarities between item scores
processing are commonly reported [Hirstein, Iversen, & on a measure of sensory differences. This disparity in the
Ramachandran, 2001; Marco, Hinkley, Hill, & Nagarajan, approaches of the two studies likely explains the differ-
2011]. Further validation of our proposed theory of ent results. Leekam, Nieto, Libby, Wing, and Gould
mechanisms of sensory disturbance in ASD with neuro- [2007] also reported age and IQ effects in their study of
physiological data is indicated. sensory differences of individuals with ASD aged 32
Additional study is also required into the role of months–38 years. Specifically, age was related to sensory
sensory hypo-reactivity in ASD. Individuals with ASD differences in oral and kinesthetic domains (differences
(especially young children) are commonly described as decreased with increasing age), younger children with
experiencing behaviors consistent with high tolerance or lower IQ were more likely to exhibit sensory differences
insensitivity to sensory stressors [Baranek, David, Poe, across sensory modalities and individuals with higher IQ
Stone, & Watson, 2006; Ben-Sasson et al., 2009]. A spe- showed fewer visual differences. Kern et al. [2006] also
cific subtype characterized by sensory hypo-reactivity, reported a decrease in sensory differences (particularly in
however, did not emerge in this study. Items related hyperreactivity) with increasing age in a sample aged
to hypo-reactivity on the SSP are found in under- 3–56 years. A direct comparison of the findings of these
responsive/seeks sensation and auditory filtering. Sensory studies with the current study is difficult, however, due
differences of significance in these areas were noted in to the contrasting age groups included in each study.
all subtypes except sensory adaptive, although parents Our study examined a narrow age range of 2–10 years
of children classified in this subtype, endorsed mildly only. It is possible that changes in sensory differences

INSAR Lane et al./Sensory phenotypes in autism 329


attributable to age and IQ are not readily observed hypo-reactivity in early childhood is a defining feature of
during this time period but rather are more significant ASD vs. other developmental disabilities [Baranek et al.,
when considering development from early childhood to 2006; Ben-Sasson et al., 2007]. We argue that, taken
adulthood. together, the results of this study and previous reports
Our findings contribute important information to support the hypothesis that atypical sensory reactivity
efforts to identify precise and reliable features for ASD (hyper- and/or hypo-reactivity) may be a discriminating
phenotyping. Sensory subtypes appear to provide one feature useful in the early identification of ASD in young
means of classifying individuals with ASD in a way that children. It also supports the hypothesis that impairment
may suggest indicators for response to intervention. For in general sensory reactivity, as suggested earlier, is indi-
example, understanding the sensory subtype of a newly cated in ASD. One proposition worthy of consideration is
diagnosed individual will clarify whether presenting that all infants who go on to be diagnosed with ASD
problem behaviors are likely to be responsive to a experience a fundamental impairment in sensory reac-
sensory-based desensitization protocol (taste/smell sensi- tivity but that sensory subtype is not determined until
tive and generalized sensory difference); an approach closer to diagnosis. Impairments in sensory reactivity in
addressing multisensory processing impairment (postural infancy may manifest in differing behavioral and tem-
inattentive and generalized sensory difference) or non- perament profiles that are highly susceptible to develop-
sensory-based interventions (sensory adaptive). mental, environmental and other factors. The interplay
Further, the sensory subtype schema may allow practi- of these factors in early childhood may then shape the
tioners to make predictions with regard to the presenta- emergence of a specific sensory subtype at the time of
tion and progression of functional difficulties in the diagnosis. For example, management of a hyperreactive
newly diagnosed individual. For example, the age differ- infant with risk factors for ASD by promoting self-
ence observed in our sample between taste/smell sensi- soothing and self-regulation strategies may reduce hyper-
tive and other subtypes suggests that individuals in this reactivity resulting in a profile consistent with sensory
particular subtype may present for diagnosis earlier adaptive or postural inattentive at the time of diagnosis.
because of the severity of behaviors associated with Alternatively, protection of a hyperreactive infant from
sensory hyperreactivity. These children would also be sensory stressors (e.g., managing the environment to
predicted to experience protracted difficulties with eating prevent unexpected sounds; only offering preferred
diverse and novel foods [Lane et al., in press]. Subse- foods, etc.) may result in the persistence of a hyperreac-
quently, they may benefit from early and intensive eating tive profile consistent with taste/smell sensitive or gen-
therapy to prevent secondary health concerns (vis a vis, eralized sensory difference. Further, neurodevelopmental
dietary insufficiency) and ease daily caregiver burden. processes initiated as a means of coping with nonfunc-
Additionally, previous research has linked sensory hyper- tional hyperreactivity may result in a hypo-reactive
reactivity with increased anxiety, gastrointestinal distur- profile (e.g., withdrawal) in a young child. Alternatively,
bance, and repetitive behavior in children with ASD, failure to stimulate a hypo-reactive infant may result in
suggesting that these children may require specific thera- the delays in the development of critical sensory dis-
pies to address these functional limitations [Boyd et al., crimination and perceptual skills necessary for multisen-
2010; Mazurek et al., 2013]. In contrast, children identi- sory processing and the performance of more complex
fied as meeting criteria for postural inattentive and behaviors such as motor coordination and social com-
generalized sensory difference may be predicted to expe- munication. Systematic study of these and related
rience difficulties in attention and motor skills. These hypotheses is required before definitive conclusions can
individuals would likely benefit from additional motor be drawn. In particular, careful assessment and monitor-
testing to assess the impact of multisensory processing ing of sensory differences in infants and toddlers with
difficulties on this system and on other autism symp- risk factors for ASD is required to fully understand the
toms. In fact, the postural inattentive and generalized emergence of sensory subtypes at diagnosis.
sensory difference subtypes, together, may constitute an
additional motor phenotype. In summary, establishing Limitations
the sensory subtype of a child with ASD at the time of
diagnosis may assist in planning for targeted and indi- Interpretations of the findings of our study are limited by
vidualized intervention protocols, which maximize like- the reliance on a parent-report tool to classify sensory
lihood of positive outcomes for individuals and their difference in ASD. Parent-report tools are, however, the
families. most common method used in practice to identify
Our finding regarding the younger age of presentation sensory difficulties in children with ASD and as such,
of taste/smell sensitive indicative of sensory hyperreac- provide valuable insight into the impact of sensory dif-
tivity may appear to be at odds with aspects of the ferences on the daily life context of the individual. Future
previous literature. Some reports have proposed that studies should augment data from parent-report tools

330 Lane et al./Sensory phenotypes in autism INSAR


with a systematic clinician-directed observational proto- ATN. Further support came from a cooperative agreement
col of children’s sensory-related behaviors. (UA3 MC 11054) from the U.S. Department of Health and
Further investigation of the relationship between NVIQ Human Services, Health Resources and Services Adminis-
and sensory subtypes is also indicated, as we were not tration, Maternal and Child Health Research Program, to
able to evaluate IQ performance in all participants in this the Massachusetts General Hospital. The AS ATN includes
study. Difficulties establishing a reliable IQ in children these members: Cincinnati Children’s Hospital Medical
with ASD are common. We adopted a number of strate- Center, Patricia Manning-Courtney, MD. The views
gies to optimize our assessments of this area. No signifi- expressed in this publication do not necessarily reflect the
cant differences between those with and without NVIQ views of the Autism Speaks, Inc.
data were observed in our data set leading us to conclude Other acknowledgments: Dr. Bishop received support
that our reduced data set for IQ analyses was representa- from R01HD065277. Simon Dennis, Terri Mitchell, Carrie
tive of the total group. Nevertheless, our findings should Thomas, Chelsea Hetrick, Kerry Dalton, Kelly Tanner,
be confirmed in other samples. Brittany Hand, Andrew Persch, Marisa Capogreco
The authors have no conflicts of interest to declare.

Summary and Future Research


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