Background
Autism spectrum disorder (ASD) is primarily characterized by persistent impairment of reciprocal social communication and interactions, as well as restricted, repetitive patterns of behavior, interests, or activities (RRB). The term
spectrum reflects the fact that the manifestations of ASD greatly vary according to the severity, functioning level, and chronological age [
1]. Since ASD affects a wide range of developmental domains, including motor coordination and repetitive motor behaviors, it is a lifelong chronic neurodevelopmental disorder that affects daily functions. In addition to the core symptoms involving social communication and repetitive behaviors, individuals with ASD often present various comorbidities. Approximately 70% and 40% of individuals with ASD have at least one and two or more comorbid disorders, respectively [
1]. Examples of common comorbidities in individuals with ASD include major depressive disorder, bipolar disorder, phobias, obsessive–compulsive disorder (OCD), anxiety disorder, attention deficit hyperactivity disorder (ADHD), and psychosis [
2]. A recent meta-analysis indicated that the overall pooled estimated prevalence of ADHD and anxiety disorders was 28% and 20%, respectively [
3].
Additionally, motor disturbances are prevalent among individuals with ASD, including gross motor coordination, fine motor coordination, motor stereotypies, postural impairment, and imitation and praxis. However, the exact mechanisms underlying these disturbances remain unclear [
4]. Tics are a common motor disturbance among individuals with ASD. The severity of tic symptoms can be attenuated through several treatment strategies, including pharmacotherapy. However, the prevalence and clinical characteristics of tics in individuals with ASD remain relatively unclear compared with those of other mental disorders [
5,
6]. The estimated prevalence of tics among individuals with ASD ranges from 22 to 34% depending on the sample population and administered assessment tools [
5‐
7]. Approximately 3–20% and 3–11% of children with Tourette disorder and ASD have comorbid ASD and Tourette disorder, respectively [
7‐
9]. Additionally, a recent study that used video-based assessment for tic evaluations by well-trained movement experts rather than the commonly used questionnaires confirmed that tics might be relatively common among young individuals with severe ASD who present heterogeneous repetitive behaviors [
10]. The wide range of the reported prevalence rates of tics could be mainly attributed to the absence of standardized screening tools and the inclusion of small sample sizes.
The core clinical characteristics of comorbid disorders, including tic disorder, in individuals with ASD remain unclear. Few studies have explored the clinical characteristics of ASD in individuals with Tourette disorder. A study reported that social communication deficits in patients with Tourette disorder could reflect ASD [
11]. Moreover, the developmental history of individuals with tics suggested that the observed social deficits could be attributed to ASD [
11]. Co-occurrence of early-onset Tourette disorder with ASD may be a prognostic marker for positive outcomes of general developmental achievement and autistic features, which could be mediated by high Intelligence Quotient (IQ) scores in children with comorbid tics [
12‐
14]. Accordingly, it is important to investigate the relationship between comorbid tic disorders and high IQ. Additionally, it is important to elucidate the characteristics of baseline functioning, as well as core and comorbid symptoms of ASD, in individuals with comorbid tic and Tourette disorder.
The primary aim of this study is to investigate the frequency of comorbid tic disorders in individuals with ASD in our sample using standardized assessment methods. Secondly, we aimed to explore differences in ASD symptom severity, other comorbidities, such as OCD symptoms and externalizing/internalizing behaviors, and baseline functioning through verbal/non-verbal IQ or adaptive behaviors. The hypotheses of this study are as follows: (1) clinical characteristics, including core ASD symptoms, internalizing/externalizing problems, and obsession/compulsion, are significantly higher among individuals with ASD and tics than in those without tics; (2) the severity of tic symptoms is significantly correlated with various clinical scores; (3) a high IQ score (IQ ≥ 70) is more common among individuals with ASD and comorbid tics than in individuals with ASD without tics.
Discussion
In our study, the prevalence of tic symptoms in individuals with ASD (18.4%) was higher than that in the general population (0.77–2.99%) [
35]. Further, the prevalence of tic symptoms in individuals with ASD (18.4%) was higher than the reported prevalence of Tourette disorder in individuals with ASD (3–11%) [
7‐
9]. The previously reported prevalence of tics among individuals with ASD ranges from 22 to 34% [
6,
7]. The wide range of the reported prevalence rates of tics could be mainly attributed to the absence of standardized screening tools and the inclusion of small sample sizes. Therefore, the findings should be interpreted with caution. Based on the findings of previous studies [
6,
36,
37], chronic motor tics are more common than chronic vocal tics in various groups; moreover, the prevalence of comorbid vocal and motor tics is higher or similar to that of only chronic motor tics. Consistent with findings of previous studies, the co-occurrence of motor and vocal tics was the most frequent, while the occurrence of only vocal tics was the least frequent.
Notably, the FSIQ was positively correlated with tic severity, which could be attributed to the fact that tics might be easier to differentiate in children with higher IQ scores. The presence of tics in individuals with early-life ASD may be a positive prognostic factor [
13], with this relationship being mediated by the generally higher IQ levels in these individuals [
38]. In our study, individuals without intellectual disability showed a higher rate of comorbid tics than individuals with intellectual disability. However, the exact mechanism or causal relationships of IQ with tic symptoms in individuals with ASD remains unclear; therefore, further research is warranted. Our findings are inconsistent with the general notion that patients with tic disorders without ASD have a lower IQ than the general population [
39,
40]. Contrastingly, our findings are consistent with a previous report that tics and Tourette’s syndrome are extremely common in individuals with autism, especially those with a high IQ [
41]. Further, our findings suggest that comorbid ASD should be suspected in patients with both chronic tic symptoms and social deficits, as well as a normal IQ. Contrastingly, regarding adaptive behaviors, the standardized VABS-2 score was higher in the ASD only group than in the ASD with tics group.
We observed significant between-group differences in all core and comorbid symptoms of ASD, with the ASD with tics group showing higher scores. Furthermore, tic severity showed a significant positive correlation with several clinical variables. These findings could be attributed to the fact that tic symptoms are considered as RRB symptoms on various scales measuring ASD core symptoms. Furthermore, due to mediating factors such as social deficits, the severity of ASD core symptoms could be worse than that of ASD alone [
42]. Notably, the ASD with tics group tended to have more past and current mannerisms detected using ADI-R subscales than the ASD only group, which could be mediated by RRB symptoms in individuals with ASD. However, there was no significant between-group difference. Therefore, further studies are warranted to elucidate the relationships between motor disturbances. Additionally, prospective studies on the trajectory of tics and mannerisms in individuals from an early age are warranted. Moreover, cognitive deficits in executive functioning and attention may impact ASD core symptoms. Regarding comorbid conditions, individuals with both tics and ASD showed multiple behavioral and emotional comorbidities, which may have synergistic effects on each other. Future studies are warranted to investigate mediating factors the relationship between tic symptoms and social difficulties.
The strengths of this study include the use of a large-scale sample recruited from a single center and the use of standardized tests. To our knowledge, this is the first study to compare comorbid conditions between patients with ASD with and without tics. This study has a few limitations. First, there may be a possible confounding effect of age, which we adjusted for using Quade’s rank of covariance. Second, we did not consider previous medications. However, we analyzed current medications according to specific psychiatric medication groups (See Additional file
1: Table S1, Additional file
2: Table S2, Additional file
3: Table S3 for more details). Third, we only used the parent-reported YGTSS to assess the severity of tics; however, it has shown good discriminative ability [
43]. Moreover, the YGTSS could have a limited ability in discriminating tic symptoms from ASD stereotypes and compulsive behavior in OCD. However, we observed a significant correlation between the parent-reported “present tics” and positive YGTSS scores. Additionally, there was a low proportion of participants with a positive YGTSS score and mannerisms or rituals on the ADI-R. Therefore, it is unlikely that parents misinterpreted tics as compulsive behaviors or mannerisms. Fourth, this was a retrospective study, which is limited by the time-sensitive nature of the data. Fifth, our findings could have been influenced by the presence of other comorbidities; however, we analyzed several other comorbidities, including OCD, internalizing symptoms, and externalizing symptoms. Taken together, individuals with comorbid ASD and tics may be more clinically susceptible because they are usually accompanied by other comorbidities. Therefore, professionals should identify and manage individuals with comorbid ASD and tics. Finally, we did not consider the history and severity of tics since they were only assessed using the YGTSS.
Conclusions
A high IQ (≥ 70) was significantly associated with tic disorders in individuals with ASD. Moreover, the severity of ASD core and comorbid symptoms was significantly associated with tic symptoms. Our findings suggest that comorbid tic disorders are more common in children with ASD than in the general population. Therefore, close surveillance for comorbid tic disorders in individuals with ASD, especially those without intellectual disabilities, is important.
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