Abstract
Chronic tic disorders, including Tourette’s syndrome (TS), are neuropsychiatric disorders characterized by the childhood onset of motor and/or vocal tics. Youth with TS often experience disturbances in social functioning, which can negatively impact functioning and overall quality of life. We summarize the existing knowledge about social deficits in youth with TS, while highlighting the various ways that these deficits present in comorbid developmental disorders (i.e., autism spectrum disorders) as well as in other TS-related phenomenology impacting social functioning (i.e., comorbid psychiatric conditions, tic severity, and peer victimization). Further, we discuss how interventions for TS should aim to address not only tic severity, but also the multifaceted reasons for social deficits within this population. We conclude with a discussion of clinical implications and future directions for clinical intervention and research.
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Introduction
Tourette’s syndrome (TS) is a neuropsychiatric disorder characterized by the childhood onset of multiple motor tics and at least one vocal tic for duration of at least 1 year [1]. TS impacts approximately 1–10 in 1000 children [2–4] and is commonly associated with other psychiatric disorders including attention deficit hyperactivity disorder (ADHD) [5–7], obsessive-compulsive disorder (OCD) [6], mood disturbances [8, 9], disruptive behaviors [10], and learning disorders [11]. In addition, youth with TS often experience peer victimization [12, 13•], self-concept deficits [14•], and interpersonal difficulties [15, 16•], particularly those with comorbid autism spectrum disorders (ASD) [17, 18]. The compounding burden of these co-occurring conditions is often reported as more problematic than the tics themselves [16•, 19, 20].
Over the last few decades, researchers have increasingly examined the prevalence, development, maintenance, and treatment of social deficits among youth with TS. Broadly, social deficits are considered maladaptive behaviors that can include difficulty identifying social cues, difficulty with social engagement (or motivation), social communication, limited insight into other’s feelings and intentions, and/or restricted or bizarre interests [21]. Dysfunction in these social domains can impact a child’s ability to function in multiple settings (home and school) and can contribute to decreases in overall quality of life [16•]. Improving our understanding of the clinical characteristics and biological underpinnings of social deficits in youth with TS may help inform evidenced-based intervention strategies that will not only improve tic symptoms but also address these social deficits, bolstering improved quality of life and social acceptability of the disorder. This paper will review the literature as it pertains to the manifestation of social deficits in children and adolescents with TS through comorbid developmental disorders (i.e., ASD) and through other TS-related phenomenology and/or environmental factors that impact social functioning (i.e., tic severity, peer victimization, co-occurring psychopathology).
TS and Autism Spectrum Disorders (ASD)
In recent years, there has been an increasing interest in the clinical characteristics and biological underpinnings of TS and common co-occurring psychopathology, including ASD. Although there is no enough evidence to support a unified theory, recent research has focused on both genetic and neuropathological etiologies of TS and ASD. ASDs are neurodevelopmental disorders characterized by the presence of impaired social interaction and communication, typically accompanied by restricted interests and/or stereotyped behaviors. A recent epidemiological study estimated the global prevalence of ASD to be between 1 and 2 % [22]. To date, numerous reports have examined the relationship between ASD and TS [17, 18, 23–29], including several population-based studies identifying a significant relationship between TS and ASD above and beyond what would be expected by chance [17, 30, 31]. However, highly variable rates of comorbidity between tic disorders and ASD have been reported, ranging from 2.9 to 30.0 % [6, 9, 16•, 30–32]. This range of incidence rates may be attributed to variable clinical samples (e.g., severity of psychopathology, cognitive abilities) and/or differences in research methodology (e.g., utilization of treatment-seeking clinical samples versus population-based samples).
Initial Case Reports and Case Series
The association between ASD and tic disorders was initially described in single case reports [33–37], including several describing the development of tics following withdrawal from long-term neuroleptics [38–41]. It is unclear, however, whether the neuroleptic medication use produced TS-like symptoms, or inadvertently masked tics that would have already been in existence. These early reports were followed by several case series presenting an elevated concurrence of ASD and TS [29, 42–45], as well as examples of tic development positively impacting autistic symptoms in several young children (mostly males) [24]. Collectively, these early reports spurred a growing interest and discussion in regards to the potential genetic overlap between the two disorders.
Larger Studies
A consistent limitation in studies reporting overlap between ASD and TS has been capturing large cohorts of TS and/or ASD subjects. In 1999, Baron-Cohen and colleagues identified 8.1 % of 37 school-aged children with autism presenting with comorbid TS [32]. Later, Canitano et al. [18] evaluated a clinical sample of 105 children with ASD, observing 22 % with a tic disorder (11 % with TS and 11 % with chronic motor tics) [18]. These findings suggested that the rate of comorbidity was higher than what would have been expected by chance; however, in both reports, the small sample size limited the generalizability of findings. Recently, the Tourette Syndrome International Consortium was initiated to more accurately describe the comorbidity patterns of TS using a large cohort of individuals. Using these data, Burd et al. [30] observed that 4.6 % of the 7288 participants with TS presented with a comorbid pervasive development disorder (PDD), providing significant support that TS increases the risk for PDD (including ASDs) 13-fold [30]. Further, the presence of TS and comorbid PDD significantly increased the risk of additional comorbid psychopathology (not including PDD), with nearly 98 % presenting with one or more comorbidity versus 13.2 % in the group with TS only [30]. These findings suggest that patients with TS and PDD/ASD may present with a more complex diagnostic picture, likely demanding more comprehensive and intensive managed care.
Familial and Genetic Findings
Several studies have identified a positive family history of TS and/or ASD in individuals presenting with both disorders concurrently [18, 29, 30]. In a clinical sample of 105 youth with ASD, Canitano et al. [18] observed a positive family history for tic disorders in 59.5 % of youth presenting with ASD and comorbid TS [18]. Burd et al. [30] also identified an association between neuropsychiatric symptoms (including TS and ASD) and a deletion involving exons 4, 5, and 6 of the gene neuroligin 4 (NLGN4) in a family study [30]. To further delineate potential genetic associations between TS and ASD, Fernandez et al. [46•] examined gene copy number variants (CNVs) in individuals with TS (n = 460) compared to control subjects (n = 1131). While no significant increases in the number of de novo or transmitted rare CNVs were identified in TS subjects compared to controls, gene mapping within rare CNVs in TS subjects showed significant overlap with CNVs previously identified in individuals with ASD [7, 46•]. Taken together, these findings reinforce the idea of a common pathogenetic mechanism and shared genetic risk between the two disorders [7].
Neuropathological Similarities
Given the growing evidence suggesting an etiological overlap between TS and ASD, this relationship has been investigated by several researchers via psychopathological, neuropsychological, brain imaging, genetic, and clinical studies. A recent review by Kern et al. [47] observed several neuropsychological similarities between TS, ASD, and ADHD, highlighting that these disorders may be part of a broader neurodevelopmental illness spectrum (termed abnormal connectivity spectrum disorder [ACSD]), resulting from neural processes that cause long-range underconnectivity and short-range overconnectivity. These connectivity abnormalities may be related to neurotoxicity, neuroinflammation, excitotoxicity, sustained microglial activation, proinflammatory cytokines, toxic exposure, and oxidative stress [47]. Evidence also suggests that the severity of connectivity deficits is associated with symptom severity in TS, ASD, and ADHD [48]. Collectively, these data further support the hypothesis that these disorders, though separate, may share common risk factors or possibly etiology.
Similarities in Symptomology
Beyond potential etiological similarities, phenotypic overlap exists between TS and ASD. First, there is a significant male predominance in both disorders (approximately 60–80 %) [2, 49]. Second, these disorders have many overlapping clinical symptoms, including social deficits, speech abnormalities (e.g., echolalia or palilalia), sensory abnormalities, obsessive-compulsive symptoms, and repetitive motor behaviors [47, 50]. However, there are also significant differences between the two disorders. For example, speech abnormalities such as coprolalia may present in TS but are not characteristic of ASD symptomology. In TS, disordered movements present as motor and vocal tics (i.e., repetitive, sudden, brief, irregular, involuntary) while ASD patients often present with stereotypies (i.e., repetitive, ritualistic, rhythmical, purposeful). Further, rigidity and resistance to change, common features of ASD, are somewhat distinct from the classic obsessive symptoms that frequently co-occur with TS [51]. Specific differences between tics and stereotypies can usually be differentiated by a thorough and comprehensive clinical evaluation, providing an accurate differential diagnosis [52]. A comparison of TS and ASD characteristics is presented in Table 1.
Factors Impacting the Development of Social Deficits in TS
Social skills deficits and/or interference has been identified in youth with chronic tic disorders even in the absence of ASD [2, 15, 16•, 19, 53–55]. Freeman et al. [19] examined 3500 youth with TS as part of an international population-based study, with 20 % reporting deficits in social skills. Similarly, Kadesjo and Gillberg [17] reported that almost two thirds of their school-aged TS sample (N = 58) had major social interaction problems (e.g., described as being without a friend or had “empathy problems”), with only 14 % described as having no major problems interacting with their peers [17].
Carter et al. [15] found that youth with TS and comorbid ADHD had significantly more social adaptation problems (as well as externalizing and internalizing behavior problems) than unaffected control subjects or youth with TS alone. Further, obsessive-compulsive symptom severity and disturbances in family functioning were significantly associated with deficits in social, behavioral, and emotional functioning among youth with TS, while increased tic symptom severity was not [15]. This finding was consistent with three reports [16•, 54, 56], but in contrast to several others identifying a positive association between increased tic severity and deficits in social/emotional functioning [57, 58]. This discrepancy may be attributed to differences in sample characteristics (e.g., inclusion of youth with more severe oppositional behaviors [57]) or analytic methodology (e.g., findings dependent on medication status [58]).
Similarly, Sukhodolsky et al. [10] identified a significant relationship between the presence of TS and deficits in social functioning (e.g., having fewer friends, being rejected by peers, not meeting the demands of everyday life) when compared to control subjects. Youth with comorbid ADHD did not significantly differ from youth without ADHD in these domains; however, both groups were significantly different from the control group. Further, the presence of disruptive behaviors (e.g., parent-reported aggression and delinquency) was associated with increased social deficits and family dysfunction [10]. These findings are consistent with previous studies reporting that aggressive behavior has the most detrimental effect on peer relationship difficulties in non-TS school-aged youth [59] and in youth with ADHD [60]. Storch et al. [19] examined the impact of TS on youth using a parent-report measure of functional impairment. In general, tic-related impairment in a least one domain (school, home, social activities) was reported by 70 % of parents, with 42 % reporting at least one significant problem interacting socially (e.g., problems making friends [21 %] or being around strangers [15 %]) [19]. In an Internet-based survey conducted by Conelea et al. [54], parents and youth with TS reported significant social interference due to symptoms, which was positively associated with tic severity and the presence of psychiatric comorbidities [54].
More recently, McGuire et al. [16•] found that youth with TS or chronic tic disorders (N = 99) had increased social deficits (e.g., difficulties picking up social cues, interpreting social cues, engagement in reciprocal social behavior) compared to normative samples, with 19 % of TS youth exhibiting severe social deficits. Although the presence of ADHD (without comorbid OCD) and/or increased tic severity was not directly associated with social deficits, a positive relationship was identified between increased social impairment and the severity of inattention, hyperactivity, and oppositionality [16•]. Similarly, Ghanizadeh and Mosallaei [6] observed a significant proportion of TS youth with comorbid disruptive behavioral disorders exhibiting greater parent-reported social problems compared to youth without these co-occurring behaviors [6]. These data are consistent with existing literature describing significant social impairment in youth with ADHD and/or commonly comorbid disruptive behavior (with or without TS) [61]. Taken together, these findings highlight the increased prevalence of social deficits among individuals with TS and highlight the impact of comorbid psychiatric diagnoses (particularly ADHD), disruptive behaviors, and/or increased tic severity on social functioning.
Peer Relationship Problems in TS
In addition to the social deficits often reported in samples of youth with TS, a few reports have also shed light on the peer relationship problems that these youth often experience. Previous findings suggest that youth with TS are viewed as more socially withdrawn and less popular than their peers [56, 62], have difficulty getting along with their classmates [63], and experience increased bullying or victimization by their peers compared to youth with other chronic health conditions (type 1 diabetes) or healthy controls [12, 13•, 64]. Evidence also suggests that peer victimization experienced by youth with TS is positively associated with increased tic symptom severity, strength of premonitory urge, loneliness, internalizing symptoms (e.g., anxiety and/or depression), explosive outbursts, and deficits in quality of life [12, 13•]. Peer victimization was also identified as a mediator between tic symptom severity and loneliness [12], suggesting that victimized youth may perceive negative peer evaluations as veridical information about themselves which can negatively shape their self-concept and foster greater internalizing distress [14•, 65, 66].
Social Deficits in Adults with TS
Although TS symptoms tend to decrease or remit once a child reaches late adolescence, a considerable portion of individuals exhibit tics into adulthood [67]. Previous research suggests that social deficits in youth with TS may carry over into adulthood as well [68–70]. In a survey-based assessment of social functioning in individuals with TS, Champion, Fulton, and Shady [69] found that almost half of the adults within their total sample (N = 210) reported significant problems with dating as a result of their TS symptoms. This finding is consistent with an earlier study reporting low marriage rates in adults with TS [70]. Further, Shady et al. [68] found that adults with TS reported significant interpersonal problems in the workplace, including experiencing ridicule by coworkers and/or employers about their tics, low job satisfaction, and discrimination in the workplace [68]. More recently, Conelea et al. [71] conducted an Internet-based survey of 1216 adults with TS to assess the impact of tics on functioning, finding that a significant portion of the sample reported avoidance of social situations and/or experienced discrimination due to their tics. Further, from the adults employed within the last 12 months of the study (n = 461), a significant portion of the sample avoided pursuing a job promotion (12 %) or avoided a job interview (11.9 %) because of their tics, both of which positively correlated with tic severity [71]. Evidence suggests that women may also be at greater risk for tic-related social impairment and avoidance of social/group activities compared to men, independent of tic severity [72].
Evidence-Based Interventions for Improving Social Functioning in TS
Although substantial evidence exists for pharmacological and behavioral interventions for tics [73], there is a paucity of research evaluating the effectiveness of augmenting (or modifying) interventions to address social deficits within this population. Youth with tics may benefit from social skills training to improve peer relationships and/or effectively respond to teasing or rejection [74]. Educating youth and parents about the greater social and emotional risks associated with their condition and monitoring family functioning (e.g., stress related to chronic condition) in combination with evidenced-based pharmacologic and/or behavioral treatments may also be beneficial. Careful assessment should be done to examine tic-related impairment on an individual basis, rather than assuming that all youth with TS have similar problems [19].
Peer-Focused Interventions
Recently, researchers have investigated TS intervention strategies that aim to improve the social acceptability of the disorder, including self-disclosure of diagnosis and/or educational outreach via video-based delivery. To date, there have been at least five studies evaluating these interventions. First, Woods [75] randomly assigned subjects to a group that either received an educational video about TS or no video; then, all subjects watched an hour long video of an actor portraying a person with TS. Their findings indicated that subjects who watched the educational video were more likely to positively rate the actor in regards to social acceptability than those that did not watch the video [75]. In a follow-up study, Woods and Marcks [76] compared groups receiving either an educational video about TS, a similar video about depression, or no video. Only subjects receiving the TS-specific video demonstrated increased acceptability of TS, indicating that this increase was not solely an effect of educational videos about mental health challenges [76]. Third, Marcks et al. [37] found that the preventative self-disclosure (compared to nondisclosure) of TS symptoms significantly reduced negative perceptions of an individual with TS, regardless of gender or age. Fourth, Holtz and Tessman [77] found that compared to a control group, youth exposed to a video-based educational tool exhibited significant changes in knowledge, positive attitudes, and behavioral intentions toward their peers with TS [77]. More recently, the effect of either generic TS educational videos or personally delivered self-disclosure on participant’s perceptions of individuals with TS was compared. Although both conditions rated their knowledge about tics significantly higher than those who did not watch any video, those who viewed the actor personally self-disclose their symptoms had higher ratings of social acceptability than those in the generic TS education video [78]. Taken together, these findings suggest that increasing TS awareness, especially when information is personally self-disclosed by those with TS, can significantly improve the social acceptability of individuals with TS.
Conclusions
Existing research suggests an increased prevalence of comorbid ASD and/or disturbances in social functioning and peer victimization among individuals with TS. While the precise nature of these relationships is uncertain, both genetic factors and co-occurring psychopathology have been implicated in the etiology and/or maintenance of these difficulties. Over the last few decades, researchers have identified several factors that may contribute to these social disturbances, highlighting the negative impact of comorbid psychiatric diagnoses (particularly ADHD), disruptive behaviors, and/or increased tic severity. Evidence also suggests that peer victimization experienced by youth with TS is associated with increased tic symptom severity, strength of premonitory urge, loneliness, internalizing symptoms (e.g., anxiety and/or depression), explosive outbursts, and deficits in quality of life. Although several studies postulate that reducing these disabling aspects of symptom presentations beyond tics will reduce the overall burden of TS, most are cross-sectional or preliminary in nature. As such, interventions for TS should aim to address not only tic severity, but also the multifaceted reasons for social deficits within this population.
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Camille E. Hanks and P. Jane Mutch declare that they have no conflict of interest.
Adam B. Lewin reports other from Children’s Tumor Foundation, University of Central Oklahoma, Springer, Rogers Hospital, TSA, APA Division 53, and Oxford; personal fees from Prophase; and grants from All Childrens Hospital and IOCDF.
Eric A. Storch reports grants from National Institute of Health, Agency for Healthcare Research and Quality, Ortho-McNeil Janssen Scientific Affairs, Fulbright scholar program, All Children’s Hospital Research Foundation, and International OCD Foundation; and book royalties from Wiley, Lawrence Erlbaum, Springer publishers, and American Psychological Association.
Tanya K. Murphy reports grants from AstraZeneca Pharmaceuticals, Auspex Pharmaceuticals, Sunovion Pharmaceuticals, Psyadon Pharmaceuticals, Pfizer, Inc., Neurocrine Biosciences, Hoffmann-La Roche Ltd., Shire Pharmaceuticals, Centers for Disease Control, National Institute of Mental Health, Massachusetts General Hospital, Otsuka Pharmaceuticals, and PANDAS Network; and personal fees from International OCD Foundation, Tourette Syndrome Association, and Grand Rounds/Continuing Medical.
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This article is part of the Topical Collection on Tourette’s Syndrome
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Hanks, C.E., Lewin, A.B., Mutch, P.J. et al. Social Deficits and Autism Spectrum Disorders in Tourette’s Syndrome. Curr Dev Disord Rep 2, 285–292 (2015). https://doi.org/10.1007/s40474-015-0060-8
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DOI: https://doi.org/10.1007/s40474-015-0060-8