Youths with ADHD with and without tic disorders: Comorbid psychopathology, executive function and social adjustment

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Abstract

Attention deficit/hyperactivity disorder (ADHD) and tic disorders (TD) commonly co-occur. Clarifying the psychiatric comorbidities, executive functions and social adjustment difficulties in children and adolescents of ADHD with and without TD is informative to understand the developmental psychopathology and to identify their specific clinical needs. This matched case-control study compared three groups (n = 40 each) of youths aged between 8 and 16 years: ADHD with co-occurring TD (ADHD + TD), ADHD without TD (ADHD  TD) and typically developing community controls. Both ADHD groups had more co-occurring oppositional defiant disorder than the control group, and the presence of TD was associated with more anxiety disorders. TD did not impose additional executive function impairments or social adjustment difficulties on ADHD. Interestingly, for youths with ADHD, the presence of TD was associated with less interpersonal difficulties at school, compared to those without TD. The potential various directions of effects from co-occurring TD should be carefully evaluated and investigated for youths with ADHD.

Highlights

► We investigated tic disorders and attention deficit/hyperactivity disorder (ADHD). ► We compared psychopathologies, executive functions (EF) and social adjustment. ► The presence of tic disorders in ADHD was associated with more anxiety disorders. ► Tic disorders add no more EF impairments and social difficulties on ADHD.

Introduction

Attention-deficit/hyperactivity disorder (ADHD) is a common developmental neuropsychiatric disorder of childhood, with a world-wide pool prevalence of 5.29% (Polanczyk, de Lima, Horta, Biederman, & Rohde, 2007) and a prevalence rate of 7.5% in the Taiwanese child and adolescent population (Gau, Chong, Chen, & Cheng, 2005). ADHD is characterized by early-onset functionally impairing attention deficits, hyperactivity and impulsivity. Commonly occurring together with ADHD, tic disorder (TD) is also an early-onset neuropsychiatric condition, characterized by episodic motor or/and vocal tics. According to the presentation and course of symptoms, it is further classified into Tourette's disorder, chronic tic disorder, transient tic disorder and tic disorder, not otherwise specified. Tourette's disorder shows persistent motor tics and at least one kind of vocal tics persisting for more than one year, with a symptom-free period less than three consecutive months. Chronic tic disorder, a milder form of Tourette's disorder (Leckman et al., 1998), is defined by either motor and/or vocal tics lasting more than one year. Transient tic disorder is defined as having motor and/or vocal tics with a duration of at least four weeks but less than one year. The prevalence is around 5–23% for all tic disorders (Khalifa and von Knorring, 2003, Kurlan et al., 2001, Wang and Kuo, 2003) and 0.6–3.8% for Tourette's disorder (Hornsey et al., 2001, Khalifa and von Knorring, 2003, Wang and Kuo, 2003).

ADHD and TD commonly co-occur. Children with ADHD have high rate (8–14%) of concurrent TD (Biederman et al., 2005) and around 35–50% of children with TD also meet the diagnosis of ADHD (Freeman, 2007, Kurlan et al., 2002, Wang and Kuo, 2003). The high co-occurrence of these two disorders has raised significant clinical attention (Carter et al., 2000, Erenberg, 2005, Khalifa and von Knorring, 2003, Kurlan et al., 2002, Nijmeijer et al., 2008). Although many studies have tried to clarify the overlap of these two disorders with regard to psychopathological, psychophysiological (Rothenberger et al., 2000, Yordanova et al., 1996, Yordanova et al., 1997) and neuropsychological (Brand et al., 2002, Harris et al., 1995, Roessner et al., 2007a, Sherman et al., 1998, Shin et al., 2001) aspects, the pathophysiological mechanism underlying this comorbidity is still unclear (Roessner, Becker, Banaschewski, & Rothenberger, 2007b).

Nevertheless, the relationship between comorbid psychopathology and social function in the two disorders are rather commonly acknowledged. ADHD, with or without Tourette's disorder, is associated with higher rates of other psychopathology than Tourette's disorder-alone (Brand et al., 2002, Carter et al., 2000, Sukhodolsky et al., 2003). Furthermore, ADHD is associated with disruptive behaviors, but TD (including Tourette's disorder) is with anxious or depressive symptoms (Freeman, 2007, Roessner et al., 2007b, Spencer et al., 2001). Children with Tourette's disorder co-occurring with ADHD present worse psychosocial outcome than with those without (Carter et al., 2000, Spencer et al., 1998). Interestingly, co-occurring Tourette's disorder has little impact on the psychosocial outcomes of children with ADHD (Spencer et al., 1999). Taken together, it seems that ADHD contributes most to the social and behavioral impairments for children with co-occurring ADHD and TD (Robertson, 2006).

In children with ADHD, TD, and ADHD plus TD, the neuropsychological functions, rather than the motor symptoms, contribute most to their functional impairments (Cohen et al., 1992, Dykens et al., 1990). Tourette's disorder is characterized by impairments in visuomotor integration (Schultz et al., 1998), sustained attention (Harris et al., 1995, Sherman et al., 1998, Shucard et al., 1997), inhibition (Channon et al., 2003a, Muller et al., 2003), reaction time and verbal fluency (Schuerholz, Baumgardner, Singer, Reiss, & Denckla, 1996) and real-life problem-solving (Channon, Crawford, Vakili, & Robertson, 2003). Nevertheless, these studies seldom controlled for comorbid conditions (Shin et al., 2001). The deficits are often associated with comorbid ADHD, which typically presents deficits in inhibition, sustained attention, self-control, time perception and other executive functions (Barkley, 1997, Berlin et al., 2003, Coffey et al., 2004, Gau and Shang, 2010, Hwang et al., 2010, Nigg, 2005). Studies accounting for the presence of ADHD often report no differences on general intelligent ability between children with and without TD (Roessner et al., 2007a). In a few studies investigating executive functions, ADHD is suggested to be the main impairing factor on neuropsychological performance for children with concurrent ADHD and Tourette's disorder (Banaschewski, Neale, Rothenberger, & Roessner, 2007). Paradoxically, some studies reported a better performance of children with ADHD co-occurring with Tourette's disorder than those with ADHD alone, indicating plausible protective or compensatory mechanisms (Greimel et al., 2008, Sherman et al., 1998). Studies are required to disentangle the relationship between these two disorders in terms of executive functions.

Most studies to date investigated the relationship between ADHD and Tourette's disorder (and/or chronic tic disorder), but rarely included transient tic disorder. However, transient tic disorder is even more prevalent and commonly associated with ADHD (Khalifa & von Knorring, 2005). In addition, two community-based studies showed that children with tic symptoms had similar psychopathology as those with Tourette's disorder (Gadow et al., 2002, Kurlan et al., 2002). Investigating how TD in general (i.e., including transient tic disorder, chronic tic disorder and Tourette's disorder altogether) has an impact on ADHD better reflects the actual clinical complexity of ADHD and provides more ecologically valid inferences. Therefore, this study aims to compare children and adolescents with ADHD with and without co-occurring TD on aspects of comorbid psychopathology, executive functions and social adjustments. Based on findings reviewed earlier, we hypothesized that (1) for comorbid psychopathology, children and adolescents with ADHD and co-occurring TD (ADHD + TD group) are more likely to have comorbid anxiety disorders than those without TD (ADHD  TD group); furthermore, both ADHD + TD and ADHD  TD groups have more disruptive behaviors than the control group; and (2) the ADHD + TD group has similar or better executive function and social adjustment compared to ADHD  TD group, and both ADHD +/− TD groups have poorer executive and social functions than the control group.

Section snippets

Participants

Participants included three age-, sex- and IQ-matched groups of children and adolescents aged between 8 and 16. The ADHD + TD group included 40 participants diagnosed with both ADHD and TD at the child neurology and child psychiatry clinics of the National Taiwan University Hospital. The ADHD  TD group included 40 participants diagnosed with ADHD alone, at the child psychiatry clinic of the same hospital. The control group included 40 typically developing participants without either TD or ADHD,

Sample characteristics

Table 1 summarizes the demographic characteristics of the ADHD + TD, ADHD  TD and the control groups. The three groups were well matched in terms of chronological age, sex and IQ. There were no group differences in parental age, educational level and occupation for the whole sample and for the subsample with complete SAICA data either (data not shown). There was no significant difference in the number of inattentive symptoms assessed by the CK-SADS-E between the ADHD + TD and ADHD  TD groups, but the

Discussion

This study discovered interesting similarities and differences between ADHD youths with and without co-occurring TD. Consistent with our prediction, ADHD itself was associated with more disruptive behavioral disorders, and co-occurring TD brought in a higher association with anxiety disorders. Neuropsychologically, ADHD youths with or without TD both showed faster movement in 5-choice reaction and poor spatial working memory. Similar to previous reports (Channon et al., 2003a, Roessner et al.,

Conclusions

TD (including transient/chronic tic disorders and Tourette's disorder) does not add additional executive dysfunctions or social adjustment problems to youths with ADHD, yet the presence of TD is associated with higher co-occurrence of anxiety disorders and less interpersonal relationship difficulties at school. The finer differential patterns of comorbidity, executive functions and social adjustment between ADHD youths with and without TD may imply partially divergent developmental

Acknowledgements

This study was supported by grants from National Health Research Institute (NHRI-EX98-9407PC) and National Taiwan University Hospital, Taipei, Taiwan (NTUH96-S558).

References (76)

  • D.G. Sukhodolsky et al.

    Disruptive behavior in children with Tourette's syndrome: Association with ADHD comorbidity, tic severity, and functional impairment

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2003)
  • H.S. Wang et al.

    Tourette's syndrome in Taiwan: An epidemiological study of tic disorders in an elementary school at Taipei County

    Brain and Development

    (2003)
  • J. Yordanova et al.

    Coexistence of tics and hyperactivity in children: No additive at the psychophysiological level

    International Journal of Psychophysiology

    (1996)
  • J. Yordanova et al.

    Frontocortical activity in children with comorbidity of tic disorder and attention-deficit hyperactivity disorder

    Biological Psychiatry

    (1997)
  • T. Banaschewski et al.

    Comorbidity of tic disorders & ADHD

    European Child & Adolescent Psychiatry

    (2007)
  • R.A. Barkley

    Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD

    Psychological Bulletin

    (1997)
  • Y. Benjamini et al.

    Controlling the false discovery rate: A practical and powerful approach to multiple testing

    Journal of the Royal Statistical Society

    (1995)
  • L. Berlin et al.

    Relations between inhibition, executive functioning, and ADHD symptoms: A longitudinal study from age 5 to 8(1/2) years

    Child Neuropsychology

    (2003)
  • J. Biederman et al.

    Absence of gender effects on attention deficit hyperactivity disorder: Findings in nonreferred subjects

    The American Journal of Psychiatry

    (2005)
  • N. Brand et al.

    Brief report: Cognitive functioning in children with Tourette's syndrome with and without comorbid ADHD

    Journal of Pediatric Psychology

    (2002)
  • A.S. Carter et al.

    Social and emotional adjustment in children affected with Gilles de la Tourette's syndrome: Associations with ADHD and family functioning Attention Deficit Hyperactivity Disorder

    Journal of Child Psychology and Psychiatry

    (2000)
  • F.X. Castellanos et al.

    Neuroscience of attention-deficit/hyperactivity disorder: The search for endophenotypes

    Nature Reviews Neuroscience

    (2002)
  • S. Channon et al.

    Real-life-type problem solving in Tourette syndrome

    Cognitive and Behavioral Neurology

    (2003)
  • S. Channon et al.

    Executive function, memory, and learning in Tourette's Syndrome

    Neuropsychology

    (2003)
  • B.J. Coffey et al.

    Reexamining Tic persistence and Tic-associated impairment in Tourette's Disorder: Findings from a naturalistic follow-up study

    The Journal Nervous and Mental Disease

    (2004)
  • D.J. Cohen et al.

    Tourette syndrome. Extending basic research to clinical care

    Advances in Neurology

    (1992)
  • D.E. Comings et al.

    A controlled study of Tourette syndrome. III. Phobias and panic attacks

    American Journal of Human Genetics

    (1987)
  • M. Danckaerts et al.

    The quality of life of children with attention deficit/hyperactivity disorder: A systematic review

    European Child & Adolescent Psychiatry

    (2010)
  • E. Dykens et al.

    Intellectual, academic, and adaptive functioning of Tourette syndrome children with and without attention deficit disorder

    Journal of Abnormal Child Psychology

    (1990)
  • C.M. Eddy et al.

    Clinical correlates of quality of life in Tourette syndrome

    Movement Disorders

    (2011)
  • R.D. Freeman

    Tic disorders and ADHD: Answers from a world-wide clinical dataset on Tourette syndrome

    European Child & Adolescent Psychiatry

    (2007)
  • K.D. Gadow et al.

    Tics and psychiatric comorbidity in children and adolescents

    Developmental Medicine and Child Neurology

    (2002)
  • S.S. Gau et al.

    Sleep problems and disorders among adolescents with persistent and subthreshold attention-deficit/hyperactivity disorders

    Sleep

    (2009)
  • S.S. Gau et al.

    A 3-year panel study of mental disorders among adolescents in Taiwan

    The American Journal of Psychiatry

    (2005)
  • S.S. Gau et al.

    Executive functions as endophenotypes in ADHD: Evidence from the Cambridge Neuropsychological Test Battery (CANTAB)

    Journal of Child Psychology and Psychiatry

    (2010)
  • S.S. Gau et al.

    An open-label, randomized, active-controlled equivalent trial of osmotic release oral system methylphenidate in children with attention-deficit/hyperactivity disorder in Taiwan

    Journal of Child and Adolescent Psychopharmacology

    (2006)
  • E. Greimel et al.

    Attentional functions in children and adolescents with attention-deficit/hyperactivity disorder with and without comorbid tic disorder

    Journal of Neural Transmission

    (2008)
  • E.L. Harris et al.

    Executive function in children with Tourette syndrome and/or attention deficit hyperactivity disorder

    Journal of the International Neuropsychological Society

    (1995)
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