The effectiveness of habit reversal therapy in the treatment of Tourette syndrome and other chronic tic disorders: a systematic review

Neeladri Duttaa,b health-related quality of life across the lifespan (Hassan Andrea E. Cavanna, MD, PhDa,b,c and Cavanna, 2012) and require active treatment inter- vention (Eddy et al., 2011, Cavanna et al., 2008). a College of Medical and Dental Sciences, The European clinical guidelines for TS and other tic dis- University of Birmingham, United Kingdom orders state that the typical antipsychotics haloperidol b The Michael Trimble Neuropsychiatry Research and pimozide are the most effective medications for tic Group, Department of Neuropsychiatry, management (Roessner et al., 2011). Although there is BSMHFT and University of Birmingham, strong evidence in favor of pharmacological interven- United Kingdom tion, it is also acknowledged that there are drawbacks to c Sobell Department of Motor Neuroscience this approach. For example, the currently available and Movement Disorders, Institute of Neurology, UCL, agents are rarely able to eradicate tics completely. Fur- London, United Kingdom thermore, antidopaminergic medications are commonly associated with unwanted effects, including weight gain, Correspondence to: Andrea E. Cavanna sedation, extrapyramidal effects and dyskinesia. A de- E-mail: [email protected] cline in the use of neuroleptics, due to patients being un- able to tolerate their frequent and often severe adverse Summary effects, was recently reported (Roessner et al., 2011). Psychosocial management of TS and tic disorders, in Tourette syndrome (TS) is a neurodevelopmental disor- combination with pharmacological interventions (Frank der characterized by multiple tics, which can require and Cavanna, 2013), has long been considered. Behav- active intervention. It is recognized that behavioral ioral therapies are the psychological interventions most techniques, especially habit reversal therapy (HRT), commonly used, with habit reversal therapy (HRT) con- can offer an effective alternative or complement to sidered one of the most efficacious strategies. HRT is al- pharmacotherapy in this setting. We conducted a sys- so the most researched of all behavioral therapies for tematic literature review to evaluate the efficacy of HRT TS, having first been mentioned in 1973 as a method of in TS and other chronic tic disorders (CTDs). Our suppressing nervous tics (Azrin and Nunn, 1973). Since search was restricted to randomized controlled trials then, strong evidence has accumulated on the useful- that used standardized diagnostic and outcome meas- ness, in tic disorders, of HRT combined with response ures to compare the efficacy of HRT against a control prevention (ERP), whilst studies on other behavioral in- treatment. We identified five relevant studies, which in- terventions have given inconsistent findings (Frank and cluded 353 patients. Significant post-treatment reduc- Cavanna, 2013). tions in tic severity scores (range: 18.3%-37.5%) were Habit reversal therapy consists of several components, seen in the HRT groups across all studies. Current evi- including awareness training with self-monitoring, relax- dence suggests that HRT can significantly reduce tic severity in both adults and children with TS and other ation training and competing response training (Azrin CTDs. Further head-to-head studies are needed to com- and Peterson, 1988). Regardless of the way in which pare the efficacy of HRT with other behavioral interven- HRT is administered (e.g. alone or as part of treatment tions for tic management. packages such as Comprehensive Behavioral Interven- tion for Tics, CBIT), awareness training and competing KEY WORDS: behavioral therapy, habit reversal, tics, Tourette syn- response training are widely accepted to be the two key drome, treatment components of this intervention (Azrin and Nunn, 1973; Woods and Miltenberger, 1995). Arguably, HRT offers an effective non-pharmacological method of suppress- Introduction ing tics, without causing unwanted effects such as those associated with pharmacotherapy. Tourette syndrome (TS) is a neurodevelopmental disor- The majority of studies on HRT have involved only small der characterized by the presence, for over a year, of numbers of patients, and in several cases just one indi- multiple motor tics and at least one vocal or phonic tic vidual (Woods et al., 2007). Only a few studies have re- (Cavanna et al., 2009). Tics are defined as repetitive, in- cruited large cohorts of participants and randomized voluntary, non-rhythmic, sudden movements or vocal- subjects to two different treatment options. The aim of izations that can involve discrete muscle groups and of- this systematic literature review was to analyze these ten present between the ages of four and six years randomized studies of HRT in order to accurately evalu- (Woods et al., 2007; Robertson and Cavanna, 2008), ate its efficacy and to provide an up-to-date and reliable with a male:female ratio of approximately 4:1 (Cavanna evidence base on the effect of HRT on tic suppression et al., 2009). It has been shown that tics can affect in TS and other chronic tic disorders (CTDs).

Functional Neurology 2013; 28(1): 7-12 7 N. Dutta et al.

Methods tailed above. After eliminating results which had escaped the initial removal of duplicates, eight studies remained For this systematic literature review, the healthcare which were then assessed more closely for their eligibil- databases PubMed and PsycINFO were searched fol- ity to be included in the present review. Only studies that lowing the methodology outlined in the Prisma guide- used a standardized method for the diagnosis of tic dis- lines (Moher et al., 2009) (Fig. 1). First, using PubMed, orders, such as the DSM-IV-TR criteria, could be includ- relevant search terms were entered (“Tourette*”, “tic*”) ed. Eligible studies also used a standardized outcome using the “Map to Thesaurus” tool. The subject headings measure to quantify the efficacy of treatment, with the “Tourette syndrome” OR “Tics” OR “Tic disorders” AND Yale Global Tic Severity Scale (YGTSS) being the pre- “habit revers*” OR “comprehensive behav*” were en- ferred choice. Ideally, studies included would be blinded tered, screening titles and abstracts of papers written in to those rating the effectiveness of treatment and an in- English. This search produced a list of 36 papers. The tention-to-treat (ITT) analysis would be implemented, process was then repeated for the PsycINFO database, however these were not strict criteria for inclusion. and this second search yielded 79 results. The results of A further three studies were eventually excluded: an ear- the two literature searches were analyzed and dupli- ly study by Azrin et al. (1980) because the patients were cates were removed. This left 112 results, which were not selected according to specific criteria for the diagno- then screened for inclusion in the present systematic lit- sis of TS or other tic disorders, and two others (Azrin erature review. Only original studies looking at the effec- and Peterson, 1990; O’Connor et al., 2001) because tiveness of HRT in the treatment of TS and other CTDs, they did not compare HRT with a control treatment op- in children or adults, could be included. With regard to tion, instead using a waiting list as the control group. study paradigms, we focused on the best level of evi- This left five studies which met all the criteria for inclu- dence, i.e. randomized controlled trials involving HRT. sion in our systematic literature review. The majority of the papers mentioning HRT did not de- scribe studies specifically focusing on this technique (n=87) and were therefore excluded; others were ex- Results cluded because they reported small case studies carried out on fewer than thirty patients (n=5), or presented sin- Table I sets out the main findings of the five relevant gle case studies (n=7). Judging by their abstracts, thir- studies identified by our search. teen papers appeared to meet the search criteria de- Three of these studies (Wilhelm et al., 2003; Deckers-

Records identified through database searching (n = 115)

Records after duplicates removed Records excluded as not (n = 112)

Idenficaon relevant to HRT (n = 87)

Records excluded as Records screened small case-studies (n = 112) (n = 5)

Records excluded as single case-studies

Screening (n = 7)

Full-text articles

assessed for eligibility (n = 13)

Studies excluded because of unspecified diagnosis (n = 1) Studies included after

further removal of duplicates (n = 8) Eligibility Studies excluded because of lack of control treatment group (n = 2)

Studies included in systematic literature review (n = 5) Included

Figure 1 - PRISMA flow diagram for the inclusion and exclusion of studies

8 Functional Neurology 2013; 28(1): 7-12 Habit reversal therapy for tic disorders

bach et al., 2006; Wilhelm et al., 2012) only included term data, patients followed up after undergoing HRT ap- adults (aged 18 years or older), while one study (Pia- peared to experience continued reduction of tic severity. centini et al., 2010) focused solely on the effect of HRT in children (under 18 years). All of the studies included both males and females. A total of 353 patients were in- Discussion cluded in this review, of whom 326 met formal diagnos- tic criteria for TS (92.4%) and 244 were males (69.1%). The aim of this literature review was to provide an up-to- The number of patients included in each study ranged date source of evidence-based information on the effica- from 30 to 126, with a mean of 70.6 participants per cy of HRT in the treatment of TS and other CTDs, con- study. Three studies included patients with a specific di- sidering the results of suitable randomized controlled tri- agnosis of TS only, whereas the largest two studies in- als. Our main finding was that HRT can significantly re- cluded patients with both TS and other CTDs. Four stud- duce tic severity in both adults and children with TS and ies compared the efficacy of HRT with that of supportive other CTDs, which is in line with the results of the first psychotherapy, and one compared HRT with ERP. The randomized trial of HRT in the treatment of tic disorders YGTSS was used to measure tic severity in all of the in- (Azrin et al., 1980) and of subsequent small case stud- cluded studies. ies (Woods et al., 2007). The specific elements of the HRT intervention varied The male:female ratio of the patients identified in this re- across the five studies (Table II): Verdellen et al. (2004) view supports previous evidence that TS is about four focused on competing response and awareness training times more common in males than in females (Azrin and only, whilst Piacentini et al. (2010) and Wilhelm et al. Nunn, 1973). The studies by Wilhelm et al. (2003, 2012), (2012) implemented the most comprehensive treatment Deckersbach et al. (2006), and Piacentini et al. (2010) all protocols. compared HRT with supportive psychotherapy. Each of Table III (over) highlights the key findings of the studies these studies found that HRT was much more effective included in this review. In all five studies, HRT was at reducing tic severity, producing a mean reduction of shown to substantially reduce tic severity. 32.3% (range -25.8% to -37.5%). This contrasts with the Most of the studies included follow-up data ranging from absent or limited reduction in symptoms observed with 3 to 10 months in order to assess whether the findings supportive psychotherapy, which averaged 7.0% (range were maintained over time. Table IV (over) shows the +1.1% to -14.2%). The study by Verdellen et al. (2004) YGTSS scores recorded at follow-up in the reviewed compared HRT with ERP and found that both therapies studies. As shown by all the studies that provided long- significantly improved symptoms in patients with TS.

Table I - Large randomized controlled trials of habit reversal therapy for tic disorders.

Study No. of No. (%) Diagnosis Adults/ Mean age Comparator Outcome patients of males Children (SD) years group measure

Wilhelm et al. 2003 32 16 TS Adults 36.2 SP YGTSS (50.0%) (12.7) Verdellen et al. 2004 43 34 TS Both 20.6 ERP YGTSS (79.1%) (12.1) Deckersbach et al. 2006 30 17 TS Adults 35.1 SP YGTSS (56.7%) (12.2) Piacentini et al. 2010 126 99 TS/CTD Children 11.7 SP YGTSS (78.6%) (2.3) Wilhelm et al. 2012 122 78 TS/CTD Both 31.6 SP YGTSS (63.9%) (13.7)

Abbreviations: TS=Tourette syndrome; CTD=chronic tic disorder; SP=supportive psychotherapy; ERP=exposure with response pre- vention; YGTSS=Yale Global Tic Severity Scale

Table II - Components of habit reversal therapy used in the randomized controlled trials.

Study Competing Awareness Relaxation Function-based response training training training interventions

Wilhelm et al. 2003 ✓✓✓✓ Verdellen et al. 2004 ✓✓ Deckersbach et al. 2006 ✓✓✓✓ Piacentini et al. 2010 ✓✓✓✓ Wilhelm et al. 2012 ✓✓✓✓

Functional Neurology 2013; 28(1): 7-12 9 N. Dutta et al.

However, in this study (Verdellen et al., 2004), HRT did ising short-term results, its long-term findings were less not appear to reduce tic severity to the same extent as in convincing. In the study by Verdellen et al. (2004), over- the other four studies reviewed in the present article. In all follow-up rates at three months were relatively low: addition, the proportion of patients who showed a >30% only 59% of the patients from the HRT group and 57% reduction in tic severity was 58% in the ERP group, of those from the ERP group. Of these, 12 patients (8 in which was substantially greater than the 28% found by the HRT group and 4 in the ERP group) did not complete Wilhelm et al. (2003) in the HRT group. the follow-up. Most importantly, due to the crossover de- Although all the reviewed studies met our strict inclusion sign of the study in the post-treatment phase, 25 of the criteria, we nevertheless identified a number of method- follow-up patients (68%) subsequently received the op- ological limitations. In particular, the follow-up protocols posite treatment to the initial one they were assigned to. presented problems in all the studies. Wilhelm et al. This made it impossible to extrapolate any information (2003) carried out follow-up assessments at 10 months, about the long-term efficacy of either treatment, and to which is the longest time of all the reviewed studies. see how they compared over this time period. In this They found that a significant improvement in tic severity study, as well as in the ones by Piacentini et al. (2010) was still apparent in the HRT group at 10 months, al- and Deckersbach et al. (2006), a significant number of though the mean YGTSS scores had risen since the patients initially assessed were subsequently lost to fol- treatment intervention. Conversely, mean YGTSS low-up, which introduced a bias in the evaluation of fol- scores in the supportive psychotherapy group had fall- low-up tic severity scores. Moreover, in the study by Pi- en. As a result, the post-treatment difference between acentini et al. (2010), only selected patients deemed to YGTSS scores in the HRT and supportive psychothera- be “positive responders” to treatment, i.e. patients who py groups was no longer significant at the final follow- had improved significantly with the initial treatment inter- up. For this reason, even though this study gave prom- vention, were given booster sessions at three-month in-

Table III - Difference in tic severity before and after habit reversal therapy and control treatment in the randomized controlled trials.

YGTSS Study Treatment group Pre-treatment Post-treatment % change

Wilhelm et al. 2003 Habit reversal 30.5 19.8 -35.1 Supportive psychotherapy 26.6 26.9 1.1 Verdellen et al. 2004 Habit reversal 24.1 19.7 -18.3 Exposure with response prevention 26.2 17.6 -32.8 Deckersbach et al. 2006 Habit reversal 29.3 18.3 -37.5 Supportive psychotherapy 27.7 26.8 -3.2 Piacentini et al. 2010 Habit reversal 24.7 17.1 -30.8 Supportive psychotherapy 24.6 21.1 -14.2 Wilhelm et al. 2012 Habit reversal 24.0 17.8 -25.8 Supportive psychotherapy 21.8 19.3 -11.5

Abbreviations: YGTSS=Yale Global Tic Severity Scale.

Table IV - Tic severity at follow-up after habit reversal therapy or control treatment in the randomized controlled trials.

Study YGTSS score Follow-up (no. of patients) Treatment group (no. of patients) Pre- Post- 3 6 10 % change Tx Tx months months months since pre-Tx Wilhelm et al. 2003 HR (16) 30.5 19.8 21 (10) -31.1 SP (13) 26.6 26.9 23.8 (11) -10.5 Verdellen et al. 2004 HR (22) 24.1 19.7 13.5 (13) -44.0 ERP (21) 26.2 17.6 14 (12) -46.6 Deckersbach et al. 2006 HR (15) 29.3 18.3 18.4 (8) -37.2 SP (15) 27.7 26.8 26.6 (10) -4.0 Piacentini et al. 2010 HR (61) 24.7 17.1 13.9 (28) 13.3 (23) -46.2 SP (65) 24.6 21.1 9.9 (12) 10.4 (8) -57.7 Wilhelm et al. 2012 HR (63) 24.0 17.8 SP (59) 21.8 19.3

Abbreviations: YGTSS=Yale Global Tic Severity Scale; Pre-Tx=pre-treatment; Post-Tx=post-treatment; HR=habit reversal; SP=sup- portive psychotherapy; ERP=exposure with response prevention.

10 Functional Neurology 2013; 28(1): 7-12 Habit reversal therapy for tic disorders

tervals. A greater proportion of patients from the HRT Wilhelm et al. (2012), and 14% in the study by Verdellen group were evaluated as positive responders compared et al. (2004). Deckersbach et al. (2006) reported only with the supportive psychotherapy group, resulting in a figures for comorbid obsessive-compulsive disorder, possible bias in follow-up tic severity scores. which was present in 30.0% of patients, whilst Wilhelm The study by Wilhelm et al. (2012) used a similar para- et al. (2003) did not report rates of comorbid diagnoses. digm to that of Piacentini et al. (2010) in order to inves- This systematic review provides an up-to-date summary tigate the efficacy of HRT as part of a tailored compre- of the existing scientific evidence for the use of HRT in hensive intervention (CBIT). Again, only participants the treatment of tics in TS and other CTDs. However, showing positive results were invited for follow-up as- there are some intrinsic limitations to our literature re- sessments. The reliability of the follow-up data was re- view strategy. For example, relevant information might duced by the fact that of the 24 participants invited, on- have been missed by choosing to use selective inclu- ly 15 were available for assessment. Additionally, the sion criteria for the reviewed studies. Moreover, there authors rated clinical improvement at 6-month follow-up emerged significant differences between the studies in using the Clinical Global Impression-Improvement Scale covariate variables, such as gender and age. Although rather than the YGTSS, thus limiting the accuracy and such differences are acknowledged in this review, ad- generalizability of the findings. justment for these variables was not performed. Further- A further set of problems with the examined literature re- more, other potential confounders, such as socio-eco- lates to the blinding procedure and ITT analysis. In the nomic status, ethnic origin, etc., were not considered. study by Wilhelm et al. (2003), the interviewers who rat- The overall results of our systematic literature review re- ed the YGTSS were not blinded to which treatment inforce the conclusions of the recently published Euro- group the patients were in. Moreover, although patients pean clinical guidelines on behavioral and psychosocial who dropped out before the eighth session of their treat- treatments for TS and other CTDs (Verdellen et al., ment (two in the HRT group, one in the supportive psy- 2011), which suggest that HRT is an effective treatment chotherapy group) were excluded from the analysis, option for reducing tic severity in both adults and chil- those who dropped out after this point (one in the HRT dren. This supports the clinicians’ perception that HRT group, two in the supportive psychotherapy group) were should be considered as a first-line behavioral treatment included. In the more recent study by Wilhelm et al. for obtaining tic suppression in patients of all ages (2012), tic severity was assessed by a blinded inde- (Verdellen et al., 2011). However, currently there are on- pendent clinician and conventional ITT analysis was ly a few specialists who are trained and experienced performed. In the study by Deckersbach et al. (2006), enough to administer HRT sessions (Piacentini et al., the YGTSS ratings, the clinical diagnoses and the treat- 2010). More teaching and training in this technique are ment interventions for the patients were all performed by required in order to expand its application to the treat- the same author. Therefore, it is likely that this study ment of tics throughout healthcare systems (Woods et was not assessor-blinded. Moreover, in this study two of al., 2007). Existing evidence would justify a more wide- the initial 32 patients dropped out. Data from these two spread diffusion of HRT, which in turn would allow fur- patients were not included in the analysis. However, ther research on larger and clinically diverse cohorts of when the analysis was repeated using an ITT paradigm, patients. incorporating the two drop-out patients, there was no This review has highlighted some potential areas for fur- change in the significance of the results. In contrast to ther research. Verdellen et al. (2004) noted statistically these articles, the studies by Verdellen et al. (2004) and significant reductions in tic severity in patients treated Piacentini et al. (2010) were both assessor-blinded and with ERP. The use of this behavioral therapy is support- used an ITT analysis, thus increasing the reliability and ed by relatively little research in TS populations. Future validity of their findings. studies should investigate the efficacy of ERP in larger Treatment protocols varied widely across the reviewed samples of patients with TS and other CTDs, in order to studies. Although all had a treatment group allocated to allow reliable comparisons with HRT. More research in- HRT, the specific elements incorporated into the treat- to whether behavioral therapies could represent a valid ment intervention and the frequency with which it was complement or alternative to pharmacological interven- administered differed between the studies. For example, tion for tic management is also required. Some patients the protocols adopted by Piacentini et al. (2010) and in the reviewed studies were taking medication whilst Wilhelm et al. (2012) included eight HRT sessions, undergoing the behavioral interventions, and others whereas the protocols of the other studies included ten were not. Research comparing tic severity in patients re- (Verdellen et al., 2004) or fourteen (Wilhelm et al., 2003; ceiving first-choice antidopaminergic medication versus Deckersbach et al., 2006) sessions. Likewise, although those receiving HRT could shed more light on the real the five studies used competing response and aware- efficacy of HRT compared with drug therapy. Quality of ness training as part of the HRT procedure, the other life should also be taken into consideration, in addition components of the HRT intervention were not consistent to tic severity. By replacing pharmacotherapy with HRT, across all the studies. Finally, outcome data may have adverse effects may be reduced and quality of life im- been affected by the different rates of psychiatric disor- proved. Even if tic severity scores remain higher in pa- ders across the studies: comorbid attention deficit and tients undergoing HRT compared with those on medica- hyperactivity disorder was reported in 30.2% of patients tions, patients who experience severe side effects from in the study by Verdellen et al. (2004), 27.9% in the their medication may prefer this compromise. In com- study by Wilhelm et al. (2012), and 26.2% in the study plex conditions like TS, the choice between different by Piacentini et al. (2010), whereas obsessive-compul- treatment strategies should always take into account sive disorder was reported in 19.0% of patients in the both subjective and objective factors, in addition the study by Piacentini et al. (2010), 18.0% in the study by best level of evidence from the scientific literature.

Functional Neurology 2013; 28(1): 7-12 11 N. Dutta et al.

Acknowledgments drome: implications for clinical practice. Funct Neurol 27: 23-27. The authors are grateful to the Tourette Syndrome Asso- Moher D, Liberati A, Tetzlaff J, et al (2009). Preferred reporting ciation-USA and Tourettes Action-UK for their continuing items for systematic reviews and meta-analyses: the PRIS- support. MA statement. PLoS Med 6: e1000097. O’Connor KP, Brault M, Robillard S, et al (2001). Evaluation of a cognitive-behavioural program for the management of References chronic tic and habit disorders. Behav Res Ther 39:667-681. Piacentini J, Woods DW, Scahill L, et al (2010). Behavior ther- apy for children with Tourette disorder: a randomized con- Azrin NH, Nunn RG (1973). Habit reversal: a method of elimi- trolled trial. JAMA 303:1929-1937. nating nervous habits and tics. Behav Res Ther 11:619-628. Robertson M, Cavanna A (2008). Tourette syndrome: The facts. Azrin NH, Nunn RG, Frantz SE (1980). Habit reversal vs neg- 2nd ed. Oxford; Oxford University Press. ative practice treatment of nervous tics. Behav Ther 11: Roessner V, Plessen KJ, Rothenberger A, et al (2011). Euro- 169-178. pean clinical guidelines for Tourette syndrome and other tic Azrin NH, Peterson AL (1988). Habit reversal for the treatment disorders. Part II: pharmacological treatment. Eur Child Ado- of Tourette syndrome. Behav Res Ther 26: 347-351. lesc Psychiatry 20:173-196. Azrin NH, Peterson AL (1990). Treatment of Tourette syndrome Verdellen CW, Keijsers GP, Cath DC, et al (2004). Exposure by habit reversal: a waiting-list control group comparison. with response prevention versus habit reversal in Tourette’s Behav Ther 21:305-318. syndrome: a controlled study. Behav Res Ther 42:501-511. Cavanna AE, Schrag A, Morley D, et al (2008). The Gilles de la Verdellen C, van de Griendt J, Hartmann A, et al (2011). Euro- Tourette syndrome-quality of life scale (GTS-QOL): Devel- pean clinical guidelines for Tourette syndrome and other tic opment and validation. Neurology 71:1410-1416. disorders. Part III: behavioural and psychosocial interven- Cavanna AE, Servo S, Monaco F, et al (2009). The behavioural tions. Eur Child Adolesc Psychiatry 20:197-207. spectrum of Gilles de la Tourette syndrome. J Neuropsychi- Wilhelm S, Deckersbach T, Coffey BJ, et al (2003). Habit re- atry Clin Neurosci 21:13-23. versal versus supportive psychotherapy for Tourette’s dis- Deckersbach T, Rauch S, Buhlmann U, et al (2006). Habit re- order: a randomized controlled trial. Am J Psychiatry 160: versal versus supportive psychotherapy in Tourette’s disor- 1175-1177. der: a randomized controlled trial and predictors of treatment Wilhelm S, Peterson AL, Piacentini J, et al (2012). Randomized response. Behav Res Ther 44:1079-1090. trial of behavior therapy for adults with Tourette syndrome. Eddy CM, Rizzo R, Gulisano M, et al (2011). Quality of life in Arch Gen Psychiatry; 69:795-803. young people with Tourette syndrome: a controlled study. J Woods DW, Miltenberger RG (1995). Habit reversal: a review of Neurol 258:291-301. applications and variations. J Behav Ther Exp Psychiatry Frank M, Cavanna AE (2013). Behavioural treatments for 26:123-131. Tourette syndrome: An evidence-based review. Behav Neu- Woods DW, Piacentini JC, Walkup JT (2007) editors. Treating rol in press. Tourette syndrome and tic disorders: A guide for practition- Hassan N, Cavanna AE (2012). The prognosis of Tourette syn- ers. New York; The Guilford Press.

12 Functional Neurology 2013; 28(1): 7-12 Original Research published: 11 August 2016 doi: 10.3389/fpsyt.2016.00135

The effect of a new Therapy for children with Tics Targeting Underlying cognitive, Behavioral, and Physiological Processes

Julie B. Leclerc1,2*, Kieron P. O’Connor1,3, Gabrielle J.-Nolin1,2, Philippe Valois1,2 and Marc E. Lavoie1,3,4

1 Centre d’études troubles obsessionnels-compulsifs et tics, Centre de recherche de l’Institut universitaire en santé mentale de Montréal, Montreal, QC, Canada, 2 Laboratoire d’étude des troubles de l’ordre de la psychopathologie en enfance, Département de psychologie, Université du Québec à Montréal, Montreal, QC, Canada, 3 Département de Psychiatrie, Université de Montréal, Montreal, QC, Canada, 4 Laboratoire de Psychophysiologie Cognitive et Sociale, Montreal, QC, Canada

Edited by: Tourette disorder (TD) is characterized by motor and vocal tics, and children with TD Kirsten R. Müller-Vahl, tend to present a lower quality of life than neurotypical children. This study applied a Hannover Medical School, Germany manualized treatment for childhood tics disorder, Facotik, to a consecutive case series Reviewed by: of children aged 8–12 years. The Facotik therapy was adapted from the adult cogni- Ewgeni Jakubovski, University of Heidelberg, Germany tive and psychophysiological program validated on a range of subtypes of tics. This Tárnok Zsanett, approach aims to modify the cognitive–behavioral and physiological processes against Vadaskert Child Psychiatry Hospital and Outpatient Clinic, Hungary which the tic occurs, rather than only addressing the tic behavior. The Facotik therapy

*Correspondence: lasted 12–14 weeks. Each week 90-min session contained 20 min of parental training. Julie B. Leclerc The therapy for children followed 10 stages including: awareness training; improving [email protected] motor control; modifying style of planning; cognitive and behavioral restructuring; and relapse prevention. Thirteen children were recruited as consecutive referrals from the Specialty section: This article was submitted to general population, and seven cases completed therapy and posttreatment measures. Child and Adolescent Psychiatry, Overall results showed a significant decrease in symptom severity as measured by the a section of the journal Frontiers in Psychiatry YGTSS and the TSGS. However, there was a discrepancy between parent and child

Received: 26 February 2016 rating, with some children perceiving an increase in tics, possibly due to improvement Accepted: 19 July 2016 of awareness along therapy. They were also individual changes on adaptive aspects Published: 11 August 2016 of behavior as measured with the BASC-2, and there was variability among children. Citation: All children maintained or improved self-esteem posttreatment. The results confirm the Leclerc JB, O’Connor KP, J.-Nolin G, Valois P and Lavoie ME (2016) The conclusion of a previous pilot study, which contributed to the adaptation of the adult Effect of a New Therapy for Children therapy. In summary, the Facotik therapy reduced tics in children. These results underline with Tics Targeting Underlying Cognitive, Behavioral, and that addressing processes underlying tics may complement approaches that target tics Physiological Processes. specifically. Front. Psychiatry 7:135. doi: 10.3389/fpsyt.2016.00135 Keywords: Tourette disorder, tics, children, treatment, cognitive–behavioral therapy, psychophysiological

Frontiers in Psychiatry | www.frontiersin.org 1 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics

INTRODUCTION the negative reinforcement process. Therefore, the mechanisms underlying tics and therapeutic processes remain unclear. Definition and Symptoms In treatment by exposure and response prevention [ERP, Ref. Tourette disorder (TD) is considered a motor disorder in the (36)], the aim is to reduce tics by breaking the negative reinforce- neurodevelopmental disorders section of the DSM-5 (1). TD is ment loop between the premonitory urge and the tic itself. The diagnosed by multiple motor tics and at least one vocal tic present individual learns to tolerate the premonitory urge and resists for at least 1 year. This child-onset disorder appears to be a com- the appearance of tics for longer and longer periods (response plex condition with the changing nature of tics evolving over time prevention). A study comparing two treatment protocols ERP/ in frequency, intensity, localization, and complexity (2). Children HR in 43 participants with TD (aged 7 to 55 years old) showed and adolescents are the most affected by TD with a prevalence no significant difference between groups in reduction of tics, rate between 0.3 and 0.9% (3). where 58% of the participant in the ERP group and 28% of the Studies report that children with TD are more likely to expe- participant in the HR group showed a decrease of at least 30% on rience daily struggles in several spheres of activities (4). Cutler the YGTSS (37). However, some children are unable to feel and et al. (5) showed that 66% of 57 young participants reported detect the premonitory urges (38), and the therapy to resist the some physical consequences associated with tics (e.g., pain, aches, tic may be sometimes emotionally difficult for the child because physical discomfort). In a school setting, tics may interfere with of the pressure to succeed. academic performance and produce difficulty concentrating, writing, or reading (6). Children with TD may also experience Cognitive Psychophysiological Treatment relationship problems because they can be victimized when An elaboration of the functional role of tics in sensorimotor regu- their tics are severe and complex, and they can be stigmatized lation is found in O’Connor’s (39) cognitive psychophysiological or have more conflicts with their parents and teachers than other model. This model conceives of tics as serving a function of sen- children (7–9). Hoekstra and colleagues (10) reported an increase sorimotor autoregulation, while decreasing tension in muscles in emotional problems over time in TD children and a higher rate inappropriately contracted. Tension in TD seems characterized of cognitive difficulties than children in the general population by a cycle where the muscle is inappropriately prepared prior to (p < 0.05) (11). Consequently, children with TD tend to present a execution (40). For example, during an activity, the individual lower quality of life than neurotypical children (5, 12, 13). with a tic is preparing too quickly for an immediate response, About 85% of individuals with TD report at least one but, at the same time, preparing more muscles with more effort comorbid disorder (14, 15). The most frequent comorbidity in than necessary. This preparation is inappropriate so the tic action children with TD is attention deficit hyperactivity disorder and relieves, in part, through local tension release. Electromyographic oppositional defiant disorder (16, 17), but they can also show (EMG) recordings of tic-affected muscles show that these mus- obsessive–compulsive disorder, anxiety disorder, and depres- cles are rarely associated with zero tension and have a greater sive disorder (18, 19). The severity of the comorbidity seems to difficulty compared to non-affected muscles achieving different worsen the quality of life of these children often more than tics. degrees of tension rather just an all or nothing state of tension The variety of symptoms then interferes in daily functioning, [(41) and replication is in preparation]. People suffering from tics leading to several impairments in children with TD and comor- also subjectively report chronic tension, and Hoogduin et al. (36) bidity (20, 21). reported high overall muscle tension as a consistent feeling in all patients, when identifying premonitory urges. The originality of Behavioral Therapies this approach is its targeting of excessive overall sensorimotor Canadian, American, and European clinical guidelines recom- activations by addressing cognitions, behaviors, and physiologi- mend medication plus a cognitive–behavioral treatment for cal strategies, which engender excessive tension leading to and reducing tics (22–24). Behavioral therapies are recommended maintaining tics, rather than learning a competitive response to as evidence-based interventions to manage tics, and behavioral the tic or to the urge to tic. approaches have taken several forms depending on whether the The cognitive psychophysiological [CoPs; Ref. (40)] treatment tic is conceptualized. for tics was developed in order to focus on the processes influenc- The comprehensive behavioral intervention for tics (CBIT) ing thoughts and behaviors underlying tics, rather than working proposed by Woods and colleagues (25) is mainly based on the exclusively on the tic per se. Several cognitive factors are targeted habit reversal treatment [HRT, Ref. (26)], which was reported in the CoPs treatment, such as anticipation, rigid beliefs (e.g., to be effective for both children and adults (27–31). In addition about action and organization), a judgmental style of thinking, to HRT components, such as awareness training, relaxation, attentional focus, and a perfectionistic style of planning action competing response, contingency management, and generaliza- involving over-activity and over-preparation. This thinking tion training, CBIT emphasizes the importance of addressing can encourage the tendency to complete several tasks rapidly environmental factors that can influence tic manifestations. This and at the same time (a style termed over-activity), together 8-week treatment also uses strategies such as psychoeducation with an over-investment in preparation for action by recruiting about tics and function-based interventions. CBIT appears to redundant muscles and employing more effort than necessary be effective for tic reduction in children and adults with TD (a style termed over-preparation). People with tics frequently (32–34). However, the premonitory urge remained unchanged experienced rigid thinking about how they should act and appear, across therapy (35), whereas, in theory, it should decrease with resulting in inflexible black and white thoughts, which impair

Frontiers in Psychiatry | www.frontiersin.org 2 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics adaptation (42). In addition, meta-cognitive factors, as defined and stable for the duration of the therapy. Exclusion criteria were: by O’Connor as thoughts about performing the tic and expecta- a diagnosis of autism spectrum disorder or intellectual disability, tions or beliefs about tic onset, are targeted along with how people receiving another behavioral treatment for tics during the study, with tics evaluate and judge situations at high risk for eliciting and a problem of geographical location to assure treatment tics (42). These cognitive factors also interact with physiological adherence. Thirteen children were originally recruited and seven factors such as an increased sensorimotor activation, leading to children completed therapy and posttreatment measures (one hypersensitivity and over-reactivity and so, as a circular linking, retracted before therapy, four abandoned during therapy, and to tic onset (42). A behavioral target of this therapy is to break one completed the therapy, but did not complete the follow-up). the negative reinforcement cycle between the tic onset and the Table 1 summarizes age, sex, medication intake, and number immediate relief of the accumulation of muscular tensions caused of days between the first and the last therapy session for each by the heightened sensorimotor activation (40). There is evidence participant that completed the therapy. The mean age of the seven of tension building up, prior to ticking, and subjective reports of participants was 10.29 years (six boys, one girl). Mean age of the relief, post-ticking (40). The aim of the CoPs treatment is to help non-completers was 9.4 years (four boys, two girls). There was the individual in understanding how these cognitive–behavioral no statistical difference between completers and non-completers and physiological factors lead to tension and how gradually over all measures of tic severity in the pre-treatment assessment addressing and modifying them can prevent tension build-up as shown in Table 2. and tic onset, while increasing self-control. An open trial showed the efficacy of CoPs treatment in adults Assessment Measures with tics compared to waitlist with a 6:1 ratio (43). Results showed Yale Global Tic Severity Scale that 10 of the 85 participants completely reduced tic onset after The Yale Global Tic Severity Scale [YGTSS, Ref. (50)] is used to therapy (gains maintained at 6-month follow-up). Prior results assess a global scale based on a tic severity subscale with five also showed efficacy in tic reduction in adults with or without dimensions (number, frequency, intensity, complexity, and inter- medication, following CoPs treatment (44, 45). The therapy was ference of tics) and an impairment subscale. Inter-rater agree- applied to five adolescents with TD, in a pilot study (46). Results ment ranges from 0.52 to 0.99 and 0.85 for the global severity showed a decrease in tic frequency and intensity and improve- score. Factor loadings on the items in factor analyses revealed ment in social functioning for the five participants. The CoPs two separated factors, one for motor tics and overall impairment treatment has also been adapted for children with TD address- and one for phonic tics, although the two factors account only ing explosive outbursts (EO). Results showed a decrease of EO for 8% of the variance showing a low-factor validity. The YGTSS frequency of at least 34% for four participants out of six. Another participant showed a 75% decrease in posttreatment, but did not complete the follow-up assessment. The last participant showed TABLE 1 | Age, sex, medication intake, and length of the therapy for each a 67% decrease between the beginning of therapy and follow-up, participant. despite an increase of EO frequency at baseline assessment (47). Finally, a single-case design study of the CoPs treatment address- Participant Age Sex Medication Days between first and intake last therapy session ing tic severity in childhood was conducted with 11 children aged 8–12 years old (48). A decrease of 29.8% of tic onset was 1 11 Girl Valerian, atomoxetine 91 observed posttreatment (p < 0.001, d = 0.97), and the decrease 2 10 Boy – 98 was monitored over 1 year. Results showed a decrease of at least 3 10 Boy – 115 4 12 Boy – 98 1 SD in measures, post 12 months. 5 11 Boy Melatonin 104 After this pilot study, a manualized version of the treatment 6 9 Boy Methylphenidade, 106 protocol in children termed Facotik has been finalized (49), and risperidone the aim of the current study is to evaluate its efficacy in a larger 7 9 Boy – 105 consecutive case series. Based on previous research, a decrease of tic severity was expected after treatment. The efficacy of the treat- TABLE 2 | Tests of tic severity differences between completers and ment adapted for children will have important implications for non-completers on the YGTSS and on the TSGS. the intervention in TD and whether addressing the underlying sensorimotor processes is sufficient to reduce tics. Scale Median score Median Asymptotic for completers score for Wilcoxon–Mann– (participants) non-completers Whitney Test MATERIALS AND METHODS YGTSS Global 37.00 29.50 Z = −0.857, p = 0.39 Participants Tic severity 23.00 19.50 Z = −0.714, p = 0.48 Deterioration 10.00 10.00 Z = −0.158, p = 0.87 The recruitment was carried out through the Centre d’études troubles obsessionnels-compulsifs et tics – Institut universitaire en TSGS Global 25.50 21.08 Z = −0.286, p = 0.78 santé mentale de Montréal. Consecutive referrals were evaluated Tic domain 13.00 10.00 Z = −0.644, p = 0.52 according to the inclusion criteria: 8–12 years old, a primary TD Social functioning 10.00 10.00 Z = 0.443, p = 0.66 diagnosis, and medication stable at least 1 month before treatment domain

Frontiers in Psychiatry | www.frontiersin.org 3 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics is completed by the children with the help of an independent TABLE 3 | BASC-2 T-scores indicating thresholds scores for clinical and evaluator. Scores for the YGTSS ranged from 0 to 100. adaptive scales. Type of scales T-scores Tourette’s Syndrome Global Scale 30 40 50 60 70 The Tourette’s Syndrome Global Scale [TSGS, Ref. (51)] is used to < > assess a global scale based on a tics domain and a social function- Clinical Normal At-risk Clinical ing domain. The tics domain evaluates frequency and disruption Adaptive Clinical At-risk Normal of different subtypes of tics (motor/phonic and simple/complex). The gray shade are visual indicator of the At-risk and Clinical score range for the Social functioning domain included the assessment of learning, BASC-2. motor restlessness, and occupational problems. There is a good inter-rater agreement (0.89) for the global scale, and the criterion good validity of the test. Confirmatory factor analysis results were validity was demonstrated as a correlation between TSGS’s global equivalent on the SRP, with a comparative fit index of 0.90 and a scale and severity of TD symptomatology ranked by four raters root mean square error of approximation of 0.11, indicating good ranging from 0.46 to 0.99. The TSGS highly correlates with the and near good validity of the test. YGTSS for motor, phonic, and total tics (from 0.86 to 0.91), but the correlation is moderate for the global score. The TSGS is com- Culture-Free Self-esteem Inventory pleted by the children with the help of an independent evaluator The Culture-Free Self-Esteem Inventory – second edition form B and by one of their parents. Scores for the TSGS ranged from 0 [CFSEI, Ref. (53)] was used to evaluate change in self-esteem in to 100. children between pre- and posttreatment as a secondary benefit of the therapy. The CFSEI form B included 30 yes or no items Behavior Assessment System for assessing five subscales (general, social, academic, parents, and Children – Second Edition defensiveness) extracted from form A. Correlation between the The Behavior Assessment System for Children – Second Edition two forms was 0.86. Test–retest reliability was ranging from 0.79 [BASC-2, Ref. (52)] is a multidimensional and multimodal to 0.92 for the total score and was ranging from 0.49 to 0.80 for assessment for adaptive and clinical aspects of behavior and subscales. Concurrent validity was obtained with the self-esteem personality in children. Two tests were used to assess participants inventory (54), ranging from 0.71 to 0.80. on secondary outcomes of the therapy, one by the parents and one by the children. The Parent Rating Scale (PRS) assesses nine Treatment Material clinical scales (hyperactivity, aggression, conduct problems, The Facotik treatment is a manualized therapy (therapist and anxiety, depression, somatization, atypicality, withdrawal, and child manual), including a self-monitoring diary and a token attention problems), five adaptive scale (adaptability, social skills, economy motivational board. The therapist’s manual includes leadership, activities of daily living, and functional communica- an explicit protocol for every exercise and instructions for the tion), three clinical composite scale (externalizing problems participants and their parents for each session of the therapy composite, internalizing problems composite, and behavioral with time estimation. The child’s manual contains information symptoms index), and one adaptive composite scale (Adaptive on each topic of the treatment with colorful examples, activities skills composite), over 160 items. The self-reported personality named “challenges,” and exercises to practice between therapy (SRP) for children assesses 10 clinical scales (attitude to school, sessions named “missions of the week.” A particular concern was attitude to teachers, atypicality, locus of control, social stress, to adapt the CoPs exercises to a child’s cognitive level of func- anxiety, depression, sense of inadequacy, attention problems, tioning. For this purpose, a narrative approach was proposed in and hyperactivity), four adaptive scales (Relations with parents, Facotik where two characters named Lea and Nico accompanied Interpersonal relations, Self-esteem and Self-reliance), 4 clini- the child over the treatment. To improve understanding, new ele- cal composite scales (school problems composite, internalizing ments have been added in the children adaptation of the therapy, problems composite, inattention/hyperactivity composite, and such as concrete language, practical examples, metaphors, visual emotional symptoms index), and 1 adaptive composite scale analogies, and pictures. Also, behavioral restructuring precedes (personal adjustment composite), over 139 items. cognitive restructuring, unlike the adult version. The self-mon- For both tests, scores were converted to T-score based on the itoring diary is used for assessing frequency of tics, conducting age of the participant. Intervals of T-scores indicating thresholds a functional analysis (antecedents, consequences), and clinical for “normal,” “at risk,” and “clinically significant” ranges are awareness training. Each participant notes the frequency of a presented in Table 3, for the clinical scales and for the adaptive targeted tic for a 15-min period, once a day, in a predetermined scales. Internal consistency of scales and composite scales for high-risk tic onset situation. The child also estimates the intensity the PRS were all above α = 0.80, and test–retest reliability were of the tics (low, medium, or high) and his/her principal activity all above 0.77. For the SRP, internal consistency of scales and at this time. The token economy motivational system works on composite scales ranged from α = 0.71 to α = 0.96 and test–retest a three-point award for each therapy session, one for participat- reliability ranged from 0.66 to 0.83. Change in time on the SRP ing in the challenges during the session, one for completing the could be attributed to low reliability. Confirmatory factor analysis self-monitoring diary every day and one for completing the for the PRS showed a comparative fit index of 0.88 and a root weekly exercises or missions between sessions. Children could mean square error of approximation of 0.13, both indicating near exchange nine points for a specific reward (not necessarily

Frontiers in Psychiatry | www.frontiersin.org 4 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics tangible, e.g., a specificactivity), ­ determined with their parents lasted 12 to 14 sessions depending on the understanding and on at the second session. the success of the steps by the child. Each 90-min session began by reviewing the content previously discussed and ended with Procedure 20 min of parental training (information on the clinical objective Participants and one of their parents completed the pre-treatment of the session, supportive coping strategies, and how to give posi- assessment with a trained specialized evaluator, including YGTSS, tive reinforcement for home exercises to their child). Information TSGS, BASC-2, and CFSEI. The certified evaluator was independ- was also given to the parents on the theoretical approach to ent of the therapy process and research protocol. The evaluator enable them to act as a collaborator in the therapy process based completed the scoring of the YGTSS and the TSGS, after semi- on a psychoeducation method (55, 56). Psychotherapists wrote structured interviews with the parents and the children separately. a progress report at the end of each therapy session, indicating Afterward, each participant followed the Facotik therapy with children’s progress and difficulties. one of the two trained psychotherapists: a licensed psychologist The Facotik treatment is progressive and passes through and a certified final year graduate student. TheFacotik therapy progressive therapeutic steps with a “one tic at a time” approach.

TABLE 4 | Procedure, therapeutic components, and clinical objectives of each Facotik session.

Clinical Session Procedure and therapeutic components objectives

Awareness 1 – Introduction to the therapy; psychoeducation about TD and tics training – Identifying a targeted tic (the most preoccupying or frequent) – Identifying form of tic in details (muscles involved, sequence) – Establishing a list of inconveniences to tics – Presentation of the self-monitoring diary and token economy motivational boards 2 – Psychoeducation and presentation of the CoPs approach to managing tics – Explanation of the triple link between thoughts, feelings and global tension, and tics 3 – Tic profiling: identifying personal high and low tic onset risk situation – Analyzing situation profiles; activities, and feelings in each of those situations? (establishing distinctions) 4 – Cognitive and emotional analysis of high and low tic onset risk situation – Analyzing the link between thoughts (anticipations), emotions, physiological state, and actions/tics 5 – Video recording of a high and a low tic onset risk situation (a real-life experience forms the basis for the script) – Each situation is filmed for 10 min during the session. – Viewing the scenes together with the child to analyze the differences between both situation (behavioral situational analysis) Muscle 6 – Awareness training of muscular tension and muscular discrimination discrimination – Increasing tic muscle flexibility and gaining control over tension in the tic-affected muscles – Learning to graduate the muscle tension level through practice in slowly contracting/relaxing muscles by degree (normalize effort involved; not yet progressive muscular relaxation) Relaxation 7 – Practicing abdominal breathing and progressive muscular relaxation to improve motor control learned with discrimination exercises and to prevent tension in everyday life Sensory- 8 – Reducing sensory–motor activation in avoiding anticipatory vigilance to sensation and not attributing significance to sensation in high tic motor onset risk situations (stopping negative reinforcement process) activation – Identification of personal style of planning action (over-activity, over-investment) Style of 9–10 – Understanding the link between a tension-producing style of planning action and specific experienced muscle tension, and tics (reducing planning over-activity and over-investment) action – Identifying personalized advantages and disadvantages of those styles of action; which may relate to irrational thoughts that can be addressed with cognitive restructuring – Realizing that optimal preparation is already in their person’s repertoire Cognitive 11–13 – Modifying core beliefs about perceptions of others and related to style of action planning restructuring – Activities at high-risk tic onset are evaluated for the presence of beliefs and judgments about the activity likely to impede optimal planning – Addressing perfectionist thinking and irrational thoughts on how to behave Behavioral 11–13 – Modifying preparation for a situation (e.g., prevention by relaxation) restructuring – Eliminating tension-producing strategies to inhibit or disguise the tic (e.g., holding in the tic) – Highlighting existing abilities rather than learning a new response Global 11–13 – Cognitive, sensorimotor, emotional, and behavioral components of this planning can be addressed at the same time during cognitive– restructuring behavioral modification – Cognitive and behavioral restructuring are two steps integrated during the last session of global restructuring – Generalizing practice to different situations Generalization 14 – Applying strategies to other high-risk situations or to unforeseen situations – Applying strategies to other tics or behavior Relapse 14 – Keep practicing, refresh knowledge, and maintain gains prevention – Anticipate situations that may trigger relapse of tics and change other aspects of life style – Feedback and therapy conclusion

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Table 4 presents a schema of the clinical objectives and the Figure 1 shows the global scale on the YGTSS for pre- and therapeutic components of each therapy session. The clinical posttreatment as assessed by the children and their parent. Four objective distributed over 14 sessions are: awareness training, participants showed a decrease on the YGTSS global scale for muscle discrimination, relaxation, reduced sensorimotor activa- both child and parent, while the other three reported discrepant tion, modifying style of planning action, cognitive restructura- results. Correlations between parents and children showed good tion of anticipation and appraisals, behavioral restructuration, agreement for pre-treatment scores (r = 0.70, p = 0.005), but poor generalizations, and preventing relapse. The first clinical objective agreement for posttreatment scores (r = 0.34, p = 0.234) and for (awareness training) is spread over several sessions, while, from difference scores (r = 0.30, p = 0.300). the 9th therapy session, several clinical objectives are addressed Analysis of the YGTSS subscales showed a significant decrease in the same sessions. Between each therapy session, the child in both the tic severity subscale (Mdn = 27.00 to Mdn = 15.00, completed the self-monitoring diary and the weekly exercises. Z = −2.37, p = 0.008, r = −0.63) and the impairment subscale Three participants completed treatment in 13 sessions, and four (Mdn = 20.00 to Mdn = 10.00, Z = −2.19, p = 0.031, r = −0.69), as others completed therapy in 14 sessions (the total duration of the observed by parents. Children reported a significant decrease on therapy was an average of 102.49 days between the first and the last the tic severity subscale (Mdn = 23.00 to Mdn = 16.00, Z = −2.29, session, all children skipped at least 1 week between two sessions p = 0.016, r = −0.66), but not on the impairment subscale due to sickness or scheduling constraints). At posttreatment, each (Mdn = 10.00 to Mdn = 10.00, Z = 0.81, p = 0.813). Correlations participant and one of their parents completed all assessments on between parents and children on the tic severity subscale were the YGTSS, the TSGS, the BASC-2, and the CFSEI. moderate for pre-treatment scores (r = 0.60, p = 0.023), nega- tive for posttreatment scores (r = -0.35, p = 0.220), and poor for Ethics difference scores (r = 0.29, p = 0.315). Correlations between This study was approved by the local ethic review board of the parents and children on the impairment subscale were poor for Institut universitaire en santé mentale de Montréal in accordance pre-treatment scores (r = 0.61, p = 0.021), good for posttreatment with the ethical standards of the Canadian Tri-Council Policy scores (r = 0.75, p = 0.002), and moderate for difference scores Statement of Ethical Conduct for Research Involving Humans. The (r = 0.50, p = 0.069). parents of the participants (or the legal guardian) gave their signed In contrast to YGTSS, results on the TSGS global scale showed consent for the participation of their child to the study (assess- a significant symptom decrease after treatment, as assessed by ments and therapy), and the child himself gave his or her approval. children (from Mdn = 25.50 to Mdn = 11.67, Z = −2.37, p = 0.008, r = −0.59), and by the parents (from Mdn = 16.83 to Mdn = 12.00, Data Analyses Z = −2.20, p = 0.016, r = −0.59). Figure 2 shows scores on the Two analysis procedures were planned. For statistical analyses, TSGS global scale for pre- and posttreatment as assessed by chil- one-sided exact Wilcoxon signed-rank test was conducted due dren and parents for each participant. Five participants showed to the small sample on the children and parents’ assessments to a decrease in tic symptoms on the TSGS global scale, while a evaluate global symptoms decrease after treatment, as measured further two reported discrepant results. Correlations between by the YGTSS global scale and the TSGS global scale. Additional parents and children showed good agreement for pre-treatment one-sided exact Wilcoxon signed-rank tests were conducted with scores (r = 0.74, p = 0.002), poor agreement for posttreatment the tic severity subscale and the impairment subscale of the YGTSS scores (r = 0.19, p = 0.515), and moderate agreement for differ- and with the tics domain and the social functioning domain of the ence scores (r = 0.47, p = 0.090). TSGS, using a Pratt correction in the case of tied ranks. Person’s Analysis of the TSGS domains as reported by parents correlations were computed between parents and children for showed a significant decrease in the tics domain (Mdn = 13.00 pre-treatment scores, posttreatment scores, and difference scores to Mdn = 4.00, Z = −2.37, p = 0.008, r = −0.63), but not on on all scales and subscales. Difference scores were computed as the social functioning domain (Mdn = 10.00 to Mdn = 10.00, pre-treatment score minus posttreatment score for each parents Z = −0.71, p = 0.750). Children reported a significant decrease and children. All analyses were calculated with n = 7 based on on tics domain (Mdn = 13.00 to Mdn = 6.00, Z = −2.37, a complete dataset. All statistical analyses were computed using p = 0.008, r = −0.63), but not on the social functioning domain R statistical software (57) and the coin package (58). For clinical (Mdn = 10.00 to Mdn = 6.67, Z = 0.78, p = 0.281). Correlations results, changes of at least 1 SD on the BASC-2 subscales and on between parents and children on the tics domain were good for the CFSEI were reported. pre-treatment scores (r = 0.75, p = 0.002), moderate for post- treatment scores (r = −0.41, p = 0.145), and good for difference RESULTS scores (r = 0.77, p = 0.001). Correlations between parents and children on the social functioning domain were moderate for Statistical Results pre-treatment scores (r = 0.55, p = 0.042), poor for posttreatment Results of the parents’ assessments on the YGTSS global scale scores (r = 0.20, p = 0.493), and negative for difference scores showed a general and significant symptom decrease at posttreat- (r = −0.11, p = 0.708). ment (from Mdn = 43.00 to Mdn = 27.00, Z = −2.37, p = 0.008, r = −0.63). This decrease was not perceived by the children Clinical Results themselves, as they estimated no significant symptoms decrease The BASC-2 and the CFSEI were used to detect if theFacotik (from Mdn = 37.00 to Mdn = 26.00, Z = −0.85, p = 0.234). therapy brought secondary benefits to develop adaptive and

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FIGURE 1 | Results on the YGTSS for parents and children in pre- and posttreatment.

clinical aspects of behaviors and self-esteem. Table 5 showed subtest of 1.5 SD, the parent subtest of 1 SD and the academic clinical changes of at least 1 SD on the BASC-2 SRP and on the subtest of 2.7 SD. All other participants maintained medium to BASC-2 Parent rating scale (PRS). There were no globally signifi- high levels of self-esteem from pre- to posttreatment. Table 6 cant changes over participants even if there were some changes at shows data for all participants on the CFSEI. the individual level. For all participants and all clinical subscales together, parents reported improvements in 13 subscales and DISCUSSION decreases in 6 subscales, while the children report 9 improvements and 9 decreases. An overall decrease is observed for participant 1 Principal Results (as noted by the parent) and participant 7 (as noted by the child). The purpose of the current study was to evaluate the efficiency of Participant 6 is the only one to present only slight increases the Facotik treatment to decrease the severity of tics in children observed by the parent (atypicality) and the child (anxiety, atten- aged 8–12 years old. Secondary benefits to improve adaptive and tion problems). However, children scoring shows that the attitude clinical aspects of behaviors and self-esteem were also anticipated. toward school, teachers, and the school problems composite The overall results showed a significant decrease in tics increased slightly for three participants. All other participants as assessed by the parents of children with TD. The results showed decreases and increases in some subscales without gen- as assessed by children were discrepant; tics decreased sig- eral trend. For the adaptive scales, improvements are observed by nificantly for all children as measured with the TSGS and parents in five subscales for the seven participants (adaptability four participants on seven reported a non-significant decrease for two participants, leadership, functional communication, and on the YGTSS. However, children and parents, all reported a adaptive skills). Children have noted improvements in three significant decrease in tic severity when the subscales of the two subscales (self-esteem for two participants and self-reliance) and questionnaires were analyzed. What is interesting is that, even one decrease (interpersonal relations). All these results are not considering this change in tics, children and parents generally significant, but showed clinical changes of at least 1 SD. perceive no changes in the impairment subscale. This could be One child showed improvement on self-esteem as measured by explained by the presence of comorbidity symptoms, which was the CFSEI, with an increase on the total score of 2 SD, the global not controlled in this study or by the subjective experience of

Frontiers in Psychiatry | www.frontiersin.org 7 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics

FIGURE 2 | Results on the TSGS for parents and children in pre- and posttreatment.

the impairment. The correlations between the child/parents’ Adaptive and clinical aspects of behaviors in children, as rating showed a good agreement regarding the tic severity in measured by the BASC-2, showed no significant changes, but pre-treatment, but not in posttreatment, neither for difference improvements and clinical changes were reported individually, scores (pre-minus posttreatment), suggesting a disagreement suggesting a regular fluctuation over time. There are further about the perception of change. There are two possible explana- improvements to clinical subscales than deterioration as tions for the preceding results. First, the difference between the reported by children and parents. As an example, internal- child/parents’ rating on the YGTSS and the TSGS may highlight izing problems showed punctual improvement. Improvements the sensitivity of the TSGS, which is multidimensional and have also been noticed in general for the adaptive scales. This is rated on a scale rather than in categories as in the YGTSS. highlights positive results although there are no significant dif- Second, the tic decrease might not always be detected by the ferences. All the participants maintained or reached medium to children themselves and discrepancies between the child/par- high levels of self-esteem from pre- to posttreatment. However, ents’ rating may be explained by one of the therapy components attitude toward school or teacher appear to have increased for termed “awareness training” (59). Children are more aware of three participants after therapy. This could be explained by the their tics after the therapy and they can detect and report them fact that the therapy ended concurrently with or after the end more accurately than at pre-treatment, while the parents noticed of the school year, and posttreatment assessment took place a decrease of tics because they were already conscious of the (particularly for participants 4 and 5) just before the return to tics. The self-monitoring diaries are a key component of the school period (in August). tic awareness training (60). The focus on a single tic may help In terms of experiential factors, all children benefited from the children to acknowledge the difference between a situation with therapy, and no adverse effects were reported by the participants high risk of tic onset versus low-risk situations. Some situations or their parents. The participants reported to the therapists that may be perceived as a high risk in the first place, but may become theoretical concepts and exercises were presented in a clear and low risk following the self-monitoring diary. Thus, the mixed colorful way, which made them comprehensive for all, even for results may be more of an indication of the therapy process than participant 4 who had language issues; some activities took more an absence of progress in tic reduction. time, but without causing a significant delay. Some children

Frontiers in Psychiatry | www.frontiersin.org 8 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics

TABLE 5 | Clinical change between pre- and posttreatment on the BASC-2a.

Participant 1 Participant 2 Participant 3 Participant 4 Participant 5 Participant 6 Participant 7

Pre Post Pre Post Pre Post Pre Post Pre Post Pre Post Pre Post

(A) Data from the Parent Rating Scale (PRS) Clinical scales Conduct problems 65 51 – – – – – – – – – – – – Externalizing problems 62 52 – – – – – – – – – – – – Anxiety 72 49 – – – – 57 72 – – – – – – Depression 68 52 11 49 – – 67 54 – – – – – – Somatization – – 67 47 53 36 – – 44 56 – – 44 70 Internalizing problems 65 46 – – 53 40 – – – – – – – – Atypicality 65 52 – – – – 44 54 – – 49 65 – – Withdrawal 69 56 – – – – 65 54 – – – – – – Behavioral symptoms index 68 56 – – – – – – – – – – – –

Adaptive scales Adaptability – – – – 32 53 – – – – 16 28 – – Leadership – – – – 38 51 – – – – – – – – Functional communication – – 30 55 – – – – – – – – – – Adaptive skills – – – – 40 53 – – – – – – – –

(B) Data from the self-reported personality (SRP) Clinical scales Attitude to school – – – – – – – – 45 61 – – – – Attitude to teachers 49 71 – – – – 36 49 – – – – – – School problems composite 52 68 – – – – – – 42 52 – – – – Atypicality – – – – – – – – – – – – 59 45 Locus of control – – – – 53 42 – – 51 37 – – 58 46 Social stress 13 48 – – 50 64 – – – – – – 52 37 Anxiety – – – – – – – – – – 39 51 62 47 Depression – – – – – – – – – – – – 61 45 Internalizing problems composite – – – – – – – – – – – – 57 42 Attention problems – – – – – – – – – – 40 51 – – Emotional symptoms index – – – – – – – – – – – – 54 40

Adaptive scales Interpersonal relations – – – – 50 38 – – – – – – – – Self-esteem – – – – 41 58 – – – – – – 47 58 Self-reliance – – – – 47 59 – – – – – – – –

a(A) data from the Parent Rating Scale (PRS); (B) data from the self-reported personality (SRP). Only scores that changed for at least 1 SD (10 T-score) are shown. Clinical scales: scores ≥ 60 are “at-risk”; scores ≥ 70 are “clinically significant.” Adaptive scales: scores ≤ 40 are “at-risk”; scores ≤ 30 are “clinically significant.”

TABLE 6 | T-score on the CFSEI for each participant in pre- and posttreatment on each scale.

Total score Global subtest Parent subtest Academic subtest Social subtest

Pre Post Pre Post Pre Post Pre Post Pre Post

Part 1 63 60 65 65 50 50 63 63 55 46 Part 2 63 65 60 65 60 60 63 63 55 55 Part 3 55 52 55 55 60 60 54 54 46 38 Part 4 63 63 60 60 60 60 63 63 55 46 Part 5 65 68 65 65 60 60 63 63 55 55 Part 6 60 63 60 60 60 60 63 63 46 46 Part 7 45 65a 50 65a 50 60a 36 63a 46 46

aChange in T-score of at least 1 SD.

had a little trouble to identify their irrational thoughts during Limitations high-risk tic onset situations, and all participants reported that The limitations of the present study are those inherent in a con- completing their self-monitoring diary and relaxation exercises secutive case series without baseline or control group and a lim- were most helpful to them. According to the therapists, the set ited number of participants. The attrition rate was around 40%, of strategies formed a coherent whole, and children were open- but there were no clinical or demographical differences between minded to the complementary elements of the therapy; they participants and those who abandoned. Personal motivation were particularly interested when the style of action planning and difficulty scheduling therapy sessions appear to account for was addressed. attrition. This protocol had a confounding variable, considering

Frontiers in Psychiatry | www.frontiersin.org 9 August 2016 | Volume 7 | Article 135 Leclerc et al. Intervention in Children with Tics that the posttreatment was concomitant with the preparation of a workbook for therapists and specialized training will be offered a new school year. This situation could have an impact on tics to clinicians to facilitate knowledge transfer. and on clinical aspects of behaviors. A 6- and 12-month follow- up assessment is planned. The participants were prescribed a variety of medications, and comorbidities were not controlled. AUTHOR CONTRIBUTIONS Nonetheless, the statistical and clinical significance of the tic JL created a new therapy for children with tics (Facotik). She reduction indicates potential efficacy of the Facotik treatment. oversaw the project (e.g., method, ethics, supervision) and Future Research coordinated the writing of the article with a focus on the results analysis and the discussion. KO is the author of the conceptual The main strength of the current study is the demonstration of the model that led to the new therapy for children presented in this effect of theFacotik treatment for the decrease of tic severity in article. He is the principal researcher on the grant that supported children as a first step of the validation procedure. These findings, this study. He revised the text and helped with the data analysis. with a manualized treatment and a structured protocol, highlight GJ-N contributed to the writing of the manuscript, especially the clinical importance of working on the cognitive and central the introduction and the review of the literature. PV contributed processes underlying tics in children as in adults (40). CoPs to the writing and the text formatting and was in charge of the treatment in adults has been shown to produce neurocognitive statistical analysis. ML revised the manuscript and was on the changes in style of action and concomitant cerebral functioning funding grant that supported this study. His research focus is on (61, 62). Such physiological changes (activation of the pre-motor psychophysiological data and on event-related potentials [see and motor cortex) related to the intervention remain to be vali- other article in the same topic: Morand-Beaulieu et al. (62)]. dated in children with tics (61, 62). In conclusion, this study has important implications for the conceptualization of interventions in TD; namely to know if tics are the necessary and sufficient ACKNOWLEDGMENTS target for effective interventions or if the processes underlying tics should also be addressed to obtain greater symptom reduc- This research was supported by a grant from the “Fonds de la tion and wider behavioral impact. Future research will include Recherche en Santé du Québec (FRSQ); Regroupement multidis- a randomized clinical trial design where the efficacy of Facotik ciplinaire de la recherche clinique sur le spectre du trouble obses- treatment as well as CoPs treatment in adults is compared to sionnel compulsif” (Research group #20573). The authors would CBIT (2015–2020). Follow-up data and the effect of the therapy like to acknowledge the Obsessive–Compulsive Disorder and Tic on quality of life for all the participants of the present study are still Disorder Studies Centre team for their participation with assess- pending. Finally, the Facotik therapy manual will be published as ment and treatment.

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61. Lavoie ME, Imbriglio TV, Stip E, O’Connor KP. Neurocognitive changes The reviewer EJ and handling Editor declared their shared affiliation, and the following cognitive-behavioral treatment in Tourette syndrome and chronic handling Editor states that the process nevertheless met the standards of a fair and tic disorder. Int J Cogn Ther (2011) 4(1):34–50. doi:10.1521/ijct.2011.4.1.34 objective review. 62. Morand-Beaulieu SM, O’Connor KP, Sauvé G, Blanchet PJ, Lavoie ME. Cognitive behavioural therapy induces sensorimotor and specific electrocor- Copyright © 2016 Leclerc, O’Connor, J.-Nolin, Valois and Lavoie. This is an tical changes in chronic tic and Tourette’s disorder. Neuropsychologia (2015) open-access article distributed under the terms of the Creative Commons 79(B):310–21. doi:10.1016/j.neuropsychologia.2015.05.024 Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the Conflict of Interest Statement: The authors declare that the research was con- original publication in this journal is cited, in accordance with accepted academic ducted in the absence of any commercial or financial relationships that could be practice. No use, distribution or reproduction is permitted which does not comply construed as a potential conflict of interest. with these terms.

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