Research in Developmental Disabilities 104 (2020) 103702

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Research in Developmental Disabilities

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Motor delay - An early and more common "red flag" in girls rather
T
than boys with autism spectrum disorder
Lidia V. Gabisa,b,*, Odelia Leon Attiaa, Ronit Roth-Hananiac, Jennifer Foss-Feigd
a
Weinberg Developmental Center, Safra Children’s Hospital, Tel Hashomer, Israel
b
Sackler School of Medicine at Tel Aviv University, Israel
c
The Academic College of Tel-Aviv Yaffo, Israel
d
Seaver Autism Center for Research and Treatment, Department of Psychiatry, Icahn School of Medicine at Mount Sinai, United States

A R T IC LE I N F O ABS TRA CT

Keywords: Background: Autism and intellectual disability may coincide and be preceded by global devel-
Autism opmental delay or by motor delay.
ASD Hypothesis: Motor delay in the context of global developmental delay is an initial "red flag” for
Global developmental delay ASD, with added risk in girls.
motor delay
Objective: To assess early developmental milestones in girls with ASD as compared to diagnosed
boys, considering prematurity risk.
Method: Developmental milestones in a cohort of 467 children with ASD - diagnosed at mean age
of 3.4 years (SD = 2.2) - were analyzed according to gender and prematurity risk.
Results: 111 girls (24 %), 356 boys (76 %), presented with motor milestones acquisition grossly
within the normal range. However, there was a shift towards acquisition of walking being at the
later end of the norm range, with this shift being more prominent in girls. 60 % of girls and 47 %
of boys with ASD had motor delay and 49 % of girls and 36 % of boys had global developmental
delay. The extent of the delays was greater in the prematurity subgroup.
Conclusion: Global delay of early milestones occurred in half of children with ASD and in 60 % of
girls with ASD. Delayed acquisition of independent walking is relatively more common in girls
subsequently diagnosed with ASD.

1. What this paper adds?

Acquisition of motor milestones in most children with ASD occurs grossly within the normal range. However, there is a shift
towards delayed acquisition of walking within the normal range for those subsequently diagnosed with ASD, with this shift being
more prominent in girls, with 60 % of girls and 47 % of boys with motor delay and 49 % of girls and 36 % of boys with global
developmental delay. In the 20 % of the cohort who were born prematurely, motor and global developmental delays were even more
significant. Within the prematurity subgroup, motor and global developmental delays were relatively more common in girls. Our
results demonstrate that delays in gross and fine motor skills may accompany language, communication, and social skills deficits in
children with ASD. This presentation is particularly common in girls with ASD. Late attainment of walking should be a worrisome
sign, especially in girls born premature, and should prompt an expanded evaluation for autism related signs and symptoms.

⁎
Corresponding author at: Weinberg Developmental Center, Sheba Medical Center, Tel Hashomer, Israel.
E-mail addresses: Lidia.Gabis@sheba.gov.il (L.V. Gabis), odelialeon@gmail.com (O.L. Attia), roniti1968@gmail.com (R. Roth-Hanania),
jennifer.foss-feig@mssm.edu (J. Foss-Feig).

https://doi.org/10.1016/j.ridd.2020.103702
Received 15 January 2020; Received in revised form 19 May 2020; Accepted 19 May 2020
Available online 20 June 2020
0891-4222/ © 2020 Elsevier Ltd. All rights reserved.
L.V. Gabis, et al. Research in Developmental Disabilities 104 (2020) 103702

ASD diagnosis should be considered when children are referred for a developmental evaluation due to parental concern regarding
particularly motor but also any other developmental delays. More emphasis should be put on evaluation of minor delays and in
examination of toddler girls.

2. Introduction

Individuals diagnosed with autism spectrum disorder (ASD) are an etiologically heterogeneous group (Happé, Ronald, & Plomin,
2006). Nevertheless, these individuals share common characteristics that are clinically expressed via impairments in social devel-
opment, verbal and non-verbal communication (including both acquisition and utilization), play, and interests (Bradley, Caldwell, &
Underwoord, 2014). ASD is a brain-based developmental disorder and, in many cases, it is genetically determined (Mandy, Charman,
Gilmour, & Skuse, 2011; Tick, Bolton, Happé, Rutter, & Rijsdijk, 2016). Many of the genetic etiologies of ASD, including Fragile X
syndrome, Rett syndrome and Phelan McDermid syndrome, share intellectual impairment preceded by global developmental delay
(De Rubeis et al., 2018; Dykens et al., 1989; Kau, Meyer, & Kaufmann, 2002; Marschik et al., 2018; Zingerevich et al., 2009).
Early motor delay and long-term motor impairment are characteristic features of individuals diagnosed with syndromic forms of
ASD. Fragile X syndrome, for example, includes significant motor impairment as well as global delay, occurring alongside language
and communication delays (Gabis, Baruch, Jokel, & Raz, 2011; Zingerevich et al., 2009). Rett syndrome is characterized by global
developmental delay and regression, with specific impairments in motor functioning for both upper and lower limbs (Marschik et al.,
2018). Individuals with non-genetic etiologies of ASD, such as prematurity (Mahoney, Minter, Burch, & Stapel-Wax, 2013), may also
present with primary global developmental delay, particularly in early developmental milestones achievement, as well as specific
developmental delays in attaining motor milestones. Prematurity has been considered a major risk factor for ASD. Consequently,
thorough examination of communication milestones has been emphasized in developmental follow-ups of premature infants
(Limperopoulos, 2009; Mahoney, Minter, Burch, & Stapel-Wax, 2013). The incidence of an identifiable cause of ASD depends on the
extent of the genetic workup with reports of an identifiable cause in 20–80 % of cases and the incidence of prematurity increasing the
probability of ASD diagnosis by about fourfold (Leavey, Zwaigenbaum, Heavner, & Burstyn, 2013; Rylaarsdam & Guemez-Gamboa,
2019).
Children who are later diagnosed with ASD may show impaired early motor performance compared to non-ASD children with an
older sibling diagnosed with ASD and to typical developing children. In addition, girls had significantly lower scores than boys on the
reach-to-grasp movement (Sacrey et al., 2015). Chinello, Di Gangi, and Valenza (2018) evaluated the association between 12- to 17-
month-olds’ persistence of primitive reflexes (grasping, rooting and sucking), their motor repertoire in terms of interactions with
objects and people, and their parents’ autistic traits as measured by the Autism-Spectrum Quotient questionnaire. They found that
primitive reflexes decreased with infants’ increasing age; however, regardless of infants’ age, the persistence of their primitive
reflexes was related to their reduced motor repertoire. We presume that this pattern is enhanced in prematurity, since persistence of
primitive reflexes and abnormal general movements are common in high risk infants (Sohn, Ahn, & Lee, 2011).
Although differences in motor development are not considered a primary diagnostic category for ASD, researchers interested in
autism are increasingly considering the importance of motor dysfunction in children with ASD in applying the diagnosis (Jansiewicz
et al., 2006). Many studies have pointed to the correlation between autism symptoms and motor scores (Dziuk et al., 2007; Kopp,
Beckung, & Gillberg, 2010; Ming, Brimacombe, & Wagner, 2007; Mostofsky, Burgess, & Gidley Larson, 2007; Piek & Dyck, 2004),
suggesting that motor deficits may have a significant impact on the core characteristics of autism. For instance, Flanagan and
colleagues’ prospective longitudinal study with high risk infants linked poor postural control (specifically in pull-to-sit) at age six
months to ASD at 36 months (Flanagan, Landa, Bhat, & Bauman, 2012). Motor skills at six months may predict ASD status at 24–36
months, and ASD may be associated with poorer infant motor skills (LeBarton & Landa, 2019).
Despite strong evidence for motor delay and impairment in several etiologically diverse groups of individuals with ASD, in
idiopathic ASD, motor dysfunction is not considered a core diagnostic feature (Armstrong, 2001). Instead, early identification of ASD
relies primarily on lack of or delay in the acquisition of communication and social skills alongside repetitive behaviors and atypical
sensory responses (NIMH, 2010). Although motor mannerisms are included as one example of possible repetitive behavior that
comprises an ASD diagnosis, the early "red flags" for ASD do not include specific motor deficits or delays. And yet, during the first 18
months, parental concern regarding motor delays are often the primary reason for referral to a developmental evaluation (Guinchat
et al., 2012). Parental concerns in regards to motor delays were more significant in retrospect in high risk infants (older sibling
diagnosed with ASD), as compared to low risk at both six and fifteen months of age (Sacrey et al., 2015). In a prospective study
examining a cohort of infants, motor development was not a significant predictor of ASD; however, the assessments were performed
using a developmental cognitive test, the Mullen Scales for Early Learning, in which the motor exam is limited to very few items, as
the authors state in their study limitations (Landa & Garrett-Mayer, 2006). A recent review emphasizes the need for standardized
tools to asses motor function in ASD (Wilson, Enticott, & Rinehart, 2018). Indeed, the observation that a child is not walking like his
siblings or peers is a very realistic reason for parents to request a developmental evaluation. However, for many children, the
underlying cause of late walking may not relate to a primary motor disability.
Researchers interested in autism are increasingly considering motor dysfunction in children with ASD as an important diagnostic
marker across ages (Lloyd, MacDonald, & Lord, 2013). Specific attention is given to the impact of motor dysfunction on behavior
(Mache & Todd, 2016), the contribution of motor skills to neuropsychiatric function (Mari, Castiello, Marks, Marraffa, & Prior, 2003),
and the need for targeted treatment addressing motor concerns (Baranek, 2002). The prevalence of atypical motor development in
children with ASD has been highlighted in a number of studies (Green et al., 2002; Kalberg et al., 2006; Lane, Harpster, & Heathcock,
2012; Miyahara et al., 1997; Sumner, Leonard, & Hill, 2016). The prevalence of motor deficits in ASD include: hypotonia (51 %),

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L.V. Gabis, et al. Research in Developmental Disabilities 104 (2020) 103702

motor apraxia (34 %), historical intermittent toe-walking (19 %) and gross motor delay (9%) (Ming et al., 2007). It is estimated that
50%–73% of children with ASD had significant early motor delays compared to same-age, typically-developing peers (Berkeley,
Zittel, Pitney, & Nichols, 2001; Manjiviona & Prior, 1995; Mari et al., 2003; Mayes & Calhoun, 2003). The high percentage found in
those studies represents a different era of ASD incidence and genetic evaluation, as such syndromes with overt motor difficulties- such
as Rett Syndrome or Fragile X- may have been included and influenced the high incidence. Newer studies point to more subtle motor
differences, but still emphasize it in the context of ASD: in one study, a retrospective examination of home videotapes of infants later
diagnosed with ASD yielded clear differences in the early development of motor skills in comparison to a group of typically de-
veloping infants (Esposito, Venuti, Maestro, & Muratori, 2009). The primary finding of the latter study was that infants who would
later be diagnosed with ASD exhibited an early asymmetry in their motor development (Esposito et al., 2009). A recent study found
that infant motor skill predicts later expressive language and autism spectrum disorder diagnosis (LeBarton & Landa, 2019). And, a
longitudinal study of motor development in 3- to 6-month-old high risk infants (infant siblings of children diagnosed with ASD)
reported that 70 % of high-risk infants with early motor delays subsequently exhibited communication delays (Bhat, Galloway, &
Landa, 2012). Finally, parents who had higher levels of subclinical autistic traits (as measured in the Autism Spectrum Quotient
questionnaire) tended to have infants who displayed more persistent primitive reflexes than parents with lower levels of subclinical
autistic traits (Chinello et al., 2018).
The presence of language or communication delays along with motor delays may confer a diagnosis of global developmental delay
(GDD), which is defined by delay in two or more areas of development of two or more standard deviations below age norms.
However, we suggest that delays in these two areas may also denote an ASD diagnosis that might be overlooked once a GDD diagnosis
is applied, given that at present, motor delays are not commonly considered central to ASD diagnosis. As the early diagnosis of GDD is
commonly associated with later intellectual disability, children presenting with a combination of language and motor delays and who
are diagnosed with GDD may miss the opportunity to receive early ASD-focused interventions that may have been indicated if the
correct ASD diagnosis had been applied.
In a study exploring early motor delays, young children with ASD were compared to children with GDD and to children with
typical development (Esposito & Venuti, 2009). Some degree of motor dysfunction was reported across both clinical groups, with
delays in both gross and fine motor skills. Both children with GDD and those with ASD showed greater impairment in motor de-
velopment compared to children with general developmental concerns (Esposito & Venuti, 2009). However, despite the fact that
language/communication impairments and motor delays coexist in ASD, the diagnosis only emphasizes the former.
The focus on motor impairments as features related to motor disability or global developmental delay and not to ASD is further
demonstrated in premature babies. Standard practice calls for a motor examination during the developmental follow up for pre-
mature infants. However, this developmental follow-up does not include evaluation of early markers of ASD such that these "red
flags" are commonly overlooked. This happens despite ASD being of growing prevalence among infants born premature
(Limperopoulos, 2009; Mahoney et al., 2013a).

3. Gender differences

According to a recent systematic review and meta-analysis, ASD is three times more prevalent in boys than girls (Loomes, Hull, &
Mandy, 2017). As such, studies examining and emphasizing examination of motor development in "infants" predominantly emphasize
motor development in boys with ASD (Harris, 2017). As a result, little is known about the prevalence of motor delays or deficits in
girls with ASD. Understanding the presentation of ASD symptoms among affected females has become a key focus of funded research
over the past several years. Sex differences in developmental profiles, particularly in communication skills, between girls and boys
with ASD, were reported in previous studies (Dean et al., 2014; Øien et al., 2018) and there is evidence that somewhat better early
social skills may render a definite diagnosis in girls at a slightly older age than boys. If deficits in social skills are less apparent in
younger girls with ASD in comparison to same age boys and are difficult to use as early predictors of ASD, perhaps other markers,
such as motor deficits, should be carefully considered and emphasized in girls being referred for a developmental evaluation.
The present study examined motor functioning in young children referred to a specialized child development center with sus-
pected communication disorder (ASD). The study quantified motor delays among these clinically-referred children who were ulti-
mately diagnosed with ASD. A particular focus of the study was the examine the nature of motor skill delays and deficits among girls
with ASD in particular. This gender differentiation towards a "red flag" for females may be significant in view of the fact that young
girls with ASD receive lower (better) scores, and occasionally may be missed by standardized measures examining communication. In
a recent study examining sex differences in toddlers, females with ASD had higher failure rates on the M-CHAT than males with ASD,
meaning that it is more likely that current screening methods miss girls subsequently diagnosed with ASD (Øien et al., 2017).
We hypothesized that motor delay and global developmental delay would be prominent across young children with ASD, but
would be more prevalent in girls subsequently diagnosed with ASD than in same aged boys. This assumption is based on the emerging
motor phenotype in autism, and the paucity of girls in those studies. Since girls with a milder phenotype are missed by standardized
tools, girls included in studies often show a higher ASD severity and may have comorbid intellectual disability that may be preceded
by motor and global delays (Howe et al., 2015). If our hypotheses are confirmed, identifying prominent motor delays or deficits
among young girls ultimately diagnosed with ASD could promote earlier diagnosis and pave the path for early intervention adapted
to their primary developmental needs.

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4. Method

4.1. Participants

The present study is a retrospective review of records focusing on the early developmental milestones of 467 children diagnosed
with ASD, based on DSM-IV-TR or DSM-5 criteria (American Psychiatric Association, 2013; DSM-IV, 2000), at a specialized, hospital-
based clinic for child development in Israel. The current cohort included 111 Girls (24 %) and 356 Boys (76 %), reflecting a sex
distribution representative of the broader ASD population. Age of initial diagnosis was in the range of 1.1–12.7 years (mean age 3.4
years, SD = 2.2).
About eighty percent of the cohort was referred to our center (the largest national developmental center) due to concerns re-
garding autism. About twenty percent of the cohort were children followed from birth at our prematurity clinic who subsequently
received a diagnosis of ASD. Thus, the prematurity follow up sample was not biased towards an ASD diagnosis.

4.2. Procedure & measures

The study was approved by the hospital's IRB as part of a larger study predicting developmental disability type and intellectual
disability level in children with global developmental delay (Helsinki approval 8458-11-SMC). The Autism Diagnostic Observation
Schedule - ADOS (Lord et al., 2000) was used to confirm diagnoses in cases that were not clear. Children also underwent a neuro-
developmental evaluation. A Developmental Quotient (DQ) score was obtained for each child based on the Denver Developmental
Screening Test (DDST II; (Frankenburg & Dodds, 1967) and the Clinical Adaptive Test/Clinical Linguistic and Auditory Milestone
Scale (CAT/CLAMS); (Hoon, Pulsifer, Gopalan, Palmer, & Capute, 1993). In addition to the ASD diagnosis and neurodevelopmental
evaluation, the developmental quotient (DQ) was calculated by the pediatric neurologist. In addition, as part of their clinical eva-
luation, all participants underwent a standardized developmental test and 45 % of the participants underwent a cognitive test
performed by a developmental psychologist. Specific instruments selected for developmental or cognitive testing were dependent on
the child's age and functioning level. For young children, instruments used included the Bayley II scales (Matula, Gyurke, & Aylward,
1997) and Mullen Scales for Early Learning (Mullen, 1995) as developmental tests. For children older than three years, a cognitive
test was performed, such as the Stanford-Binet Fourth Edition (Thorndike, Hagen, & Sattler, 1986) Wechsler Preschool and Primary
Scale for Intelligence – Third Edition (Wechsler, 2002), Wechsler Intelligence Scale for Children – Revised (Wechsler, 1974), Leiter-R
(Roid & Miller, 1997) or Kaufman Brief Intelligence Test (K-BIT; (Hildman, Friedberg, & Wright, 1993).

5. Plan of data analysis

5.1. Data extraction

Our primary independent variables including motor delay score and GDD score were based on DQ (Developmental Quotient)
scores obtained from measures of attained milestones in each area. DQ is routinely calculated by the pediatric neurologist during the
evaluation and calculated as- developmental age divided by chorological age (corrected for prematurity below age two years) and
multiplied by 100. If developmental age fits the chronological age the DQ is 100. The mean and standard deviation of DQ are similar
to those of intellectual functioning distribution as measured by standardized tests, namely: 100, and 15 respectively. A significant
developmental delay in one area is defined by DQ below 70 (two standard deviations below the mean). For example, for a child
achieving independent walking at 24 months, the calculated gross motor DQ would be 75, defined relative to a normative milestone
of 18 months, and therefore not considered a delay for categorical analysis. Walking at 26 months, on the other hand, would result in
a motor DQ of 69 and a delay classification in the motor domain. Age of acquisition of walking (in months) was also considered as a
continuous variable for some analyses.
GDD was defined as delay of more than 2 SD (i.e., DQ < 70) in two or more areas of development using the developmental scales
mentioned above. Specific DQ for each of the four domains (i.e., gross motor, fine motor, language and social) was calculated. Since a
combined delay of language and social development are reported in children with ASD (Cleland, Gibbon, Peppé, O’Hare, &
Rutherford, 2010; Noterdaeme, Wriedt, & Höhne, 2010), we defined GDD as a different combination of any other two areas or more -
gross motor, concurrent with language & communication, fine motor or social delays (Shevell et al., 2003). Data regarding devel-
opmental achievement in all four domains was obtained from parental reports regarding their children's milestones attainment,
which was present in medical records and available for all participants. The data was recorded by the pediatric neurologist at the
initial evaluation of each child and included milestones in all areas until the occurrence of the evaluation. The report on current
developmental milestones was validated by neurodevelopmental examination during the initial evaluation and prior milestones were
reported by the parents. Subsequent evolution of milestones was examined and recorded on follow-up visits. Since infants born
prematurely were referred by the hospital from discharge, their milestones were validated during each visit from the first months
after birth.

5.2. Statistical analyses

In order to examine the association between sex and motor as well as other delays noted in children with ASD, chi-Square tests
were used for dichotomized variables (i.e., delayed, within-normal-limits). Group differences in age of acquisition of walking (in

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Table 1
Demographic information by gender.
Variable Boys (n = 356) Girls (n = 111)

M (SD) M (SD)
Birth week 38.27 (3.09) 38.29 (3.31)
Birth weight 3173 (742) 2981 (632)
Age of initial diagnosis 3.55 (2.17) 3.01 (2.42)
N (N%) N (N%)
High-risk pregnancies 94 (26.4 %) 27 (24.3 %)
Prematurity 73 (20.5 %) 21 (18.9 %)
Genetic disorder 8 (2.2 %) 11 (9.9 %)
Intellectual disability 67 (18.8 %) 34 (30.6 %)

months) as a function of biological sex were analyzed using a t-test for independent samples. For differences in prematurity ASD
group a two-way analysis of variance was conducted. All statistical analyses were conducted using SPSS version 21.

6. Results

6.1. Perinatal course

Birth week was in the range of 23–42 weeks (mean 32 weeks, SD = 3). Birth weight was in the range of 775–4929 gr (mean
3129 g, SD = 722). Twenty-six percent of the cohort (22 % of boys; 6% of girls) were the result of high-risk pregnancies and 20 %
were born preterm (77.7 % boys and 22.3 % girls). Perinatal history was unknown in 8% of the cohort (e.g., because the child had
been brought in for the evaluation by an adopting parent or foster family). Demographic information by gender is described in
Table 1.
In the present study 45 % of the children underwent cognitive assessment and 48 % of these children were diagnosed with various
levels of intellectual disability. In 5% a genetic syndrome was identified, mainly Fragile X (n = 8) and Rett syndromes (n = 3).
For the 467 children diagnosed with ASD, the age of initial diagnosis was in the range of 1.1–12.7 years (mean 3.4 years,
SD = 2.2). There was no significant difference in age of diagnosis between boys (mean 3.5 years, SD = 2.2) and girls (mean 3 years,
SD = 2.4), t(90) = 0.97, p > 0.05.

6.2. Motor delays

In our overall sample, definite gross motor delays were found in 38 % of the children (49.5 % of the girls and 36 % of the boys).
The average age of independent walking acquisition was 17.9 months in girls and 16 months in boys t(330) = 2.43, p < 0.05.
Fifteen percent of the children acquired independent walking at significantly delayed age (19–60 months). The upper typical age
limit used is 18 months, however, most children attain walking before 16 months and children that do not walk at this age are usually
referred for physiotherapy evaluation. Girls with ASD were more likely to have a motor delay than boys diagnosed with ASD,
χ2(1) = 6.56, p < 0.01. Girls with ASD were more likely to have a GDD than boys diagnosed with ASD, χ2(1) = 5.87, p < 0.05.
There was no significant difference in cognitive delay, social interaction delay and language delay between boys and girls, p > 0.05.
Parental concerns regarding their child's development in general, began at a mean age of 20 months (SD = 12.23, range 2–101
months). There was no significant difference in children's age with respect to parental concerns regarding possible developmental
delay between boys (mean 20.72 months, SD = 12.9) and girls (mean 17.2 months, SD = 8.7), t(178) = 1.54, p > 0.05.

6.3. "Idiopathic" ASD

When the sample was limited to 314 children without known background of cerebral palsy, prematurity, or genetic syndromes,
33.7 % (120) of this group had motor delays. Girls with ASD were still likely to have a motor delay than boys with ASD, 42.7 % and
31 % respectively, (χ2(1) = 3.84, p = 0.05). Based on parental reports of milestone trajectory, definite motor delays were reported in
38 % of children and GDD was reported in 50 % of the cohort. The gender gap was significant for both with motor delay in 49.5 % of
girls and 36 % of boys. GDD was also more prevalent in girls (60.4 %) than in boys (47.2 %) (see Fig. 1).
In a sample limited to 94 children with prematurity, there were 73 boys (77.7 %) and 21 girls (22.3 %). GDD was found in 69.1 %
of the premature children later diagnosed with ASD (46 boys - 48.9 % and 19 girls -20.2 %), and motor delay was present in 54.3 % of
the children (in 36 boys - 38.3 % and 15 girls 16 %). Within the prematurity ASD group, girls attained walking later than boys (mean
18.79 months, SD = 6.5 and mean 17.39 months, SD = 4.8 respectively) but the difference did not reach significance, F
(1,309) = .02, p > 0.05, η2 = .008.
In both domains of GDD and motor delay there was a significant difference between premature and term born ASD children: for
GDD (χ2(1) = 16.10, p < 0.001) and for motor delay (χ2(1) = 8.48, p < 0.05) with a significantly higher age of attaining in-
dependent walking in premature ASD children (mean 17.7 months, SD = 5.2) than in term ASD children (mean 16 months, SD = 6), t
(311) = 2.02, p < 0.05 (see Table 2, Fig. 2).

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L.V. Gabis, et al. Research in Developmental Disabilities 104 (2020) 103702

Fig. 1. Developmental delay prevalence (%) by gender (N = 467).

Table 2
:Developmental delay at diagnosis by Prematurity.
Domain Prematurity (n = 94) Term (n = 318) χ2

Global Delay 65 (69.1 %) 145 (45.6 %) 16.1***

Gross Motor Delay 51 (54.3 %) 119 (37.4 %) 8.48**
Social Interaction Delay 70 (98 %) 209 (95 %) 1.75
Language delay 78 (83 %) 235 (73.9 %) 3.28

** p < 0.01.
*** p < 0.001.

Fig. 2. Average age of acquisition of walking (in months) by gender and prematurity (N = 313).

Additional analysis performed while excluding outliers, +-2 STD, 7 children were dropped out due to advanced age of diagnosis.
This had no effect on the significance of all the results.

7. Discussion

In this study, we harnessed a large sample of young children diagnosed with ASD to show that on average, acquisition of motor
milestones in most children with ASD occur grossly within the normal range. However, there is a shift towards acquisition of walking
being at the later end of the norm range, with this shift being more prominent in girls. About 38 % of girls with ASD in our sample had
overt motor delay. GDD of early milestones occurred in half of children with ASD and in 60 % of girls with ASD. A general population
study with infants and young toddlers (without gender differentiation), identified poor motor development related to increased
presence of ASD symptoms (Kovaniemi et al., 2018).
Setoh and colleagues believe that there are at least two possibilities. In the first possible scenario, motor impairments and ASD
traits form a single cluster of symptoms unique to a subgroup of individuals with autism. A second possible scenario is that motor
differences are the first warning signs of vulnerability often associated with atypical development (Setoh, Marschik, Einspieler, &
Esposito, 2017). However, as mentioned, using ASD screening methods without including screening for motor delays, more girls may

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be missed as toddlers than boys (Øien et al., 2017). Based on our study we suggest that more girls may belong to the cluster of ASD
with comorbid motor impairments.
Since the upper end of the typical age range for independent walking is given as 18 months, while earlier than current diagnosis of
ASD, it is not really "early" given that many interventions have been started earlier in this population (Oono, Honey, & McConachie,
2013). As such, awareness to even earlier motor milestones than walking- such as rolling over or sitting- may be warranted to provide
even and earlier opportunity for intervention.
This cluster of developmental delays is even more accentuated in ASD children with a history of prematurity. In our cohort, GDD
and motor delay occurred more frequently in premature girls with ASD, whose mean age of attaining independent walking is outside
the upper end of the normal limits.
Regarding developmental milestones of language and social-interaction we did not find significant differences between the
preterm and term group in those two domains. Since the prematurity cohort was followed prospectively, we did expect differences in
language and/or social interaction, in terms of age of diagnosis or presentation. We assume that other deficits relating to prematurity
such as vision, hearing and medical issues may have obscured the ASD milestones, or the prematurity age correction may have caused
an artifact in the assessment. This cohort was not large enough to clarify this pitfall and we are planning a larger study to address ASD
differences between preterm and term children with ASD.
In young children, when motor delays are present alongside language or communication delays, a diagnosis of GDD is often given.
However, we show here that motor delays are also quite common in children with ASD. Therefore, the additional presence of motor
delays alongside language or social ones in young children, ought to direct clinicians more towards an ASD diagnosis. Indeed, our
results show that in our sample, nearly 60 % of children met criteria for both ASD and DD. Failing to diagnose ASD in children with
motor delays who meet criteria for DD likely results in missed opportunities to apply ASD-specific early intervention.
A significant limitation of our study is that the developmental milestones until the initial evaluation was based on parental report.
Though, during the initial evaluation, the occurring milestones were validated and DQ was calculated by the pediatric neurologist. It
is possible that the report on earlier milestones but motor skills examined close the skills achievement were more accurate. All
children in Israel undergo subsequent developmental assessments from birth (attached to their immunization schedule) and parents
are in general aware of specific milestone achievements. To elucidate the accuracy of parental reports a large prospective study
including all milestones should be performed.
Considering the pitfalls, we can recommend that consideration of an ASD diagnosis should be accounted for when children are
referred to a developmental evaluation, due to parental concern regarding particularly motor but also other developmental delays,
and even more emphasis should be put on the examination of toddler girls. To this end, development of useful and hands-on tools to
be utilized for an early diagnosis of ASD during the first years of life is of paramount importance.
The ongoing attempts for an early diagnosis of ASD are somewhat hindered and complicated by the heterogeneous etiologies and
symptom presentations associated with ASD. Though consensus holds that early diagnosis of ASD is significant in conferring access to
implementation of early intervention, there is a long temporal gap between when parents first raise concerns and when a formal
diagnosis is eventually given, especially in girls (Lidia V. Gabis et al., 2018). For the primary care physician, there is an urgent need
for easy-to-perform screening tools and clearer evidence regarding salient warning markers, "red-flags" of ASD in the younger ages.

8. Conclusions

Our results demonstrate that delays in gross and fine motor skills may accompany language, communication, and social skills
deficits in children with ASD. This presentation is particularly common in girls with ASD. As such, when an infant girl presents with
mild motor skill delay, a thorough evaluation of all other developmental areas should be performed and an autism screener should be
administered. Nevertheless, when using ASD screening tools such as Q-CHAT, M-CHAT etc., a motor screening tool should be added.
Increased awareness and more thorough evaluation for ASD should also be emphasized in the follow-up of premature infants un-
dergoing developmental screening, particularly in those showing motor delay. Late attainment of walking should be a worrisome sign
in girls born premature and should prompt an expanded evaluation for autism related signs and symptoms.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

CRediT authorship contribution statement

Lidia V. Gabis: Conceptualization, Methodology, Validation, Writing - original draft, Writing - review & editing, Supervision.
Odelia Leon Attia: Formal analysis, Investigation, Data curation, Writing - review & editing. Ronit Roth-Hanania: Writing - review
& editing. Jennifer Foss-Feig: Writing - review & editing.

Declaration of Competing Interest

All authors read and approved the final manuscript and do not have any conflict of interest with regards to this study.

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L.V. Gabis, et al. Research in Developmental Disabilities 104 (2020) 103702

Acknowledgment

Ms. Romi Oren-Schwartz for final preparation of the manuscript.

Appendix A. Supplementary data

Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.ridd.2020.
103702.

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