Neeladri Duttaa,b

Andrea E. Cavanna, MD, PhDa,b,c

a College of Medical and Dental Sciences, University of Birmingham, United Kingdomb The Michael Trimble Neuropsychiatry ResearchGroup, Department of Neuropsychiatry, BSMHFT and University of Birmingham, United Kingdomc Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, UCL,London, United Kingdom

Correspondence to: Andrea E. CavannaE-mail: Andrea.Cavanna@bsmhft.nhs.uk

Summary

Tourette syndrome (TS) is a neurodevelopmental disor-der characterized by multiple tics, which can requireactive intervention. It is recognized that behavioraltechniques, especially habit reversal therapy (HRT),can offer an effective alternative or complement topharmacotherapy in this setting. We conducted a sys-tematic literature review to evaluate the efficacy of HRTin TS and other chronic tic disorders (CTDs). Oursearch was restricted to randomized controlled trialsthat used standardized diagnostic and outcome meas-ures to compare the efficacy of HRT against a controltreatment. We identified five relevant studies, which in-cluded 353 patients. Significant post-treatment reduc-tions in tic severity scores (range: 18.3%-37.5%) wereseen in the HRT groups across all studies. Current evi-dence suggests that HRT can significantly reduce ticseverity in both adults and children with TS and otherCTDs. Further head-to-head studies are needed to com-pare the efficacy of HRT with other behavioral interven-tions for tic management.

KEY WORDS: behavioral therapy, habit reversal, tics, Tourette syn-drome, treatment

Introduction

Tourette syndrome (TS) is a neurodevelopmental disor-der characterized by the presence, for over a year, ofmultiple motor tics and at least one vocal or phonic tic(Cavanna et al., 2009). Tics are defined as repetitive, in-voluntary, non-rhythmic, sudden movements or vocal-izations that can involve discrete muscle groups and of-ten present between the ages of four and six years(Woods et al., 2007; Robertson and Cavanna, 2008),with a male:female ratio of approximately 4:1 (Cavannaet al., 2009). It has been shown that tics can affect

health-related quality of life across the lifespan (Hassanand Cavanna, 2012) and require active treatment inter-vention (Eddy et al., 2011, Cavanna et al., 2008).The European clinical guidelines for TS and other tic dis-orders state that the typical antipsychotics haloperidoland pimozide are the most effective medications for ticmanagement (Roessner et al., 2011). Although there isstrong evidence in favor of pharmacological interven-tion, it is also acknowledged that there are drawbacks tothis approach. For example, the currently availableagents are rarely able to eradicate tics completely. Fur-thermore, antidopaminergic medications are commonlyassociated with unwanted effects, including weight gain,sedation, extrapyramidal effects and dyskinesia. A de-cline in the use of neuroleptics, due to patients being un-able to tolerate their frequent and often severe adverseeffects, was recently reported (Roessner et al., 2011).Psychosocial management of TS and tic disorders, incombination with pharmacological interventions (Frankand Cavanna, 2013), has long been considered. Behav-ioral therapies are the psychological interventions mostcommonly used, with habit reversal therapy (HRT) con-sidered one of the most efficacious strategies. HRT is al-so the most researched of all behavioral therapies forTS, having first been mentioned in 1973 as a method ofsuppressing nervous tics (Azrin and Nunn, 1973). Sincethen, strong evidence has accumulated on the useful-ness, in tic disorders, of HRT combined with responseprevention (ERP), whilst studies on other behavioral in-terventions have given inconsistent findings (Frank andCavanna, 2013).Habit reversal therapy consists of several components,including awareness training with self-monitoring, relax-ation training and competing response training (Azrinand Peterson, 1988). Regardless of the way in whichHRT is administered (e.g. alone or as part of treatmentpackages such as Comprehensive Behavioral Interven-tion for Tics, CBIT), awareness training and competingresponse training are widely accepted to be the two keycomponents of this intervention (Azrin and Nunn, 1973;Woods and Miltenberger, 1995). Arguably, HRT offersan effective non-pharmacological method of suppress-ing tics, without causing unwanted effects such as thoseassociated with pharmacotherapy.The majority of studies on HRT have involved only smallnumbers of patients, and in several cases just one indi-vidual (Woods et al., 2007). Only a few studies have re-cruited large cohorts of participants and randomizedsubjects to two different treatment options. The aim ofthis systematic literature review was to analyze theserandomized studies of HRT in order to accurately evalu-ate its efficacy and to provide an up-to-date and reliableevidence base on the effect of HRT on tic suppressionin TS and other chronic tic disorders (CTDs).

The effectiveness of habit reversal therapy in thetreatment of Tourette syndrome and other chronictic disorders: a systematic review

Functional Neurology 2013; 28(1): 7-12 7

Methods

For this systematic literature review, the healthcaredatabases PubMed and PsycINFO were searched fol-lowing the methodology outlined in the Prisma guide-lines (Moher et al., 2009) (Fig. 1). First, using PubMed,relevant search terms were entered (“Tourette*”, “tic*”)using the “Map to Thesaurus” tool. The subject headings“Tourette syndrome” OR “Tics” OR “Tic disorders” AND“habit revers*” OR “comprehensive behav*” were en-tered, screening titles and abstracts of papers written inEnglish. This search produced a list of 36 papers. Theprocess was then repeated for the PsycINFO database,and this second search yielded 79 results. The results ofthe two literature searches were analyzed and dupli-cates were removed. This left 112 results, which werethen screened for inclusion in the present systematic lit-erature review. Only original studies looking at the effec-tiveness of HRT in the treatment of TS and other CTDs,in children or adults, could be included. With regard tostudy paradigms, we focused on the best level of evi-dence, i.e. randomized controlled trials involving HRT.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-cluded because they reported small case studies carriedout on fewer than thirty patients (n=5), or presented sin-gle case studies (n=7). Judging by their abstracts, thir-teen papers appeared to meet the search criteria de-

tailed above. After eliminating results which had escapedthe initial removal of duplicates, eight studies remainedwhich were then assessed more closely for their eligibil-ity to be included in the present review. Only studies thatused a standardized method for the diagnosis of tic dis-orders, such as the DSM-IV-TR criteria, could be includ-ed. Eligible studies also used a standardized outcomemeasure to quantify the efficacy of treatment, with theYale Global Tic Severity Scale (YGTSS) being the pre-ferred choice. Ideally, studies included would be blindedto those rating the effectiveness of treatment and an in-tention-to-treat (ITT) analysis would be implemented,however these were not strict criteria for inclusion.A further three studies were eventually excluded: an ear-ly study by Azrin et al. (1980) because the patients werenot selected according to specific criteria for the diagno-sis of TS or other tic disorders, and two others (Azrinand Peterson, 1990; O’Connor et al., 2001) becausethey did not compare HRT with a control treatment op-tion, instead using a waiting list as the control group.This left five studies which met all the criteria for inclu-sion in our systematic literature review.

Results

Table I sets out the main findings of the five relevantstudies identified by our search.Three of these studies (Wilhelm et al., 2003; Deckers-

N. Dutta et al.

8 Functional Neurology 2013; 28(1): 7-12

Records identified through

database searching

(n = 115)

Scre

enin

g In

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ed

Elig

ibili

ty

Iden

�fica

�on

Records after duplicates removed

(n = 112)

Records screened

(n = 112)

Records excluded as not

relevant to HRT

(n = 87)

Full-text articles

assessed for eligibility

(n = 13)

Studies excluded

because of unspecified

diagnosis

(n = 1)

Studies included in

systematic literature

review (n = 5)

Records excluded as

small case-studies

(n = 5)

Records excluded as

single case-studies

(n = 7)

Studies included after

further removal of

duplicates (n = 8) Studies excluded

because of lack of

control treatment group

(n = 2)

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

bach et al., 2006; Wilhelm et al., 2012) only includedadults (aged 18 years or older), while one study (Pia-centini et al., 2010) focused solely on the effect of HRTin children (under 18 years). All of the studies includedboth males and females. A total of 353 patients were in-cluded in this review, of whom 326 met formal diagnos-tic criteria for TS (92.4%) and 244 were males (69.1%).The number of patients included in each study rangedfrom 30 to 126, with a mean of 70.6 participants perstudy. Three studies included patients with a specific di-agnosis of TS only, whereas the largest two studies in-cluded patients with both TS and other CTDs. Four stud-ies compared the efficacy of HRT with that of supportivepsychotherapy, and one compared HRT with ERP. TheYGTSS was used to measure tic severity in all of the in-cluded studies.The specific elements of the HRT intervention variedacross the five studies (Table II): Verdellen et al. (2004)focused on competing response and awareness trainingonly, whilst Piacentini et al. (2010) and Wilhelm et al.(2012) implemented the most comprehensive treatmentprotocols.Table III (over) highlights the key findings of the studiesincluded in this review. In all five studies, HRT wasshown to substantially reduce tic severity.Most of the studies included follow-up data ranging from3 to 10 months in order to assess whether the findingswere maintained over time. Table IV (over) shows theYGTSS scores recorded at follow-up in the reviewedstudies. As shown by all the studies that provided long-

term data, patients followed up after undergoing HRT ap-peared to experience continued reduction of tic severity.

Discussion

The aim of this literature review was to provide an up-to-date source of evidence-based information on the effica-cy of HRT in the treatment of TS and other CTDs, con-sidering the results of suitable randomized controlled tri-als. Our main finding was that HRT can significantly re-duce tic severity in both adults and children with TS andother CTDs, which is in line with the results of the firstrandomized trial of HRT in the treatment of tic disorders(Azrin et al., 1980) and of subsequent small case stud-ies (Woods et al., 2007).The male:female ratio of the patients identified in this re-view supports previous evidence that TS is about fourtimes more common in males than in females (Azrin andNunn, 1973). The studies by Wilhelm et al. (2003, 2012),Deckersbach et al. (2006), and Piacentini et al. (2010) allcompared HRT with supportive psychotherapy. Each ofthese studies found that HRT was much more effectiveat reducing tic severity, producing a mean reduction of32.3% (range -25.8% to -37.5%). This contrasts with theabsent or limited reduction in symptoms observed withsupportive psychotherapy, which averaged 7.0% (range+1.1% to -14.2%). The study by Verdellen et al. (2004)compared HRT with ERP and found that both therapiessignificantly improved symptoms in patients with TS.

Habit reversal therapy for tic disorders

Functional Neurology 2013; 28(1): 7-12 9

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-basedresponse training training training interventions

Wilhelm et al. 2003 ✓ ✓ ✓ ✓

Verdellen et al. 2004 ✓ ✓

Deckersbach et al. 2006 ✓ ✓ ✓ ✓

Piacentini et al. 2010 ✓ ✓ ✓ ✓

Wilhelm et al. 2012 ✓ ✓ ✓ ✓

However, in this study (Verdellen et al., 2004), HRT didnot appear to reduce tic severity to the same extent as inthe other four studies reviewed in the present article. Inaddition, the proportion of patients who showed a >30%reduction in tic severity was 58% in the ERP group,which was substantially greater than the 28% found byWilhelm et al. (2003) in the HRT group. Although all the reviewed studies met our strict inclusioncriteria, we nevertheless identified a number of method-ological limitations. In particular, the follow-up protocolspresented problems in all the studies. Wilhelm et al.(2003) carried out follow-up assessments at 10 months,which is the longest time of all the reviewed studies.They found that a significant improvement in tic severitywas still apparent in the HRT group at 10 months, al-though the mean YGTSS scores had risen since thetreatment intervention. Conversely, mean YGTSSscores in the supportive psychotherapy group had fall-en. As a result, the post-treatment difference betweenYGTSS scores in the HRT and supportive psychothera-py groups was no longer significant at the final follow-up. For this reason, even though this study gave prom-

ising short-term results, its long-term findings were lessconvincing. In the study by Verdellen et al. (2004), over-all follow-up rates at three months were relatively low:only 59% of the patients from the HRT group and 57%of those from the ERP group. Of these, 12 patients (8 inthe HRT group and 4 in the ERP group) did not completethe follow-up. Most importantly, due to the crossover de-sign of the study in the post-treatment phase, 25 of thefollow-up patients (68%) subsequently received the op-posite treatment to the initial one they were assigned to.This made it impossible to extrapolate any informationabout the long-term efficacy of either treatment, and tosee how they compared over this time period. In thisstudy, as well as in the ones by Piacentini et al. (2010)and Deckersbach et al. (2006), a significant number ofpatients initially assessed were subsequently lost to fol-low-up, which introduced a bias in the evaluation of fol-low-up tic severity scores. Moreover, in the study by Pi-acentini et al. (2010), only selected patients deemed tobe “positive responders” to treatment, i.e. patients whohad improved significantly with the initial treatment inter-vention, were given booster sessions at three-month in-

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

Study Treatment groupYGTSS

Pre-treatment Post-treatment % change

Wilhelm et al. 2003 Habit reversal 30.5 19.8 -35.1Supportive psychotherapy 26.6 26.9 1.1

Verdellen et al. 2004 Habit reversal 24.1 19.7 -18.3Exposure with response prevention 26.2 17.6 -32.8

Deckersbach et al. 2006 Habit reversal 29.3 18.3 -37.5Supportive psychotherapy 27.7 26.8 -3.2

Piacentini et al. 2010 Habit reversal 24.7 17.1 -30.8Supportive psychotherapy 24.6 21.1 -14.2

Wilhelm et al. 2012 Habit reversal 24.0 17.8 -25.8Supportive 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.

StudyTreatment group

YGTSS score Follow-up (no. of patients)

(no. of patients) Pre- Post- 3 6 10 % changeTx Tx months months months since pre-Tx

Wilhelm et al. 2003 HR (16) 30.5 19.8 21 (10) -31.1SP (13) 26.6 26.9 23.8 (11) -10.5

Verdellen et al. 2004 HR (22) 24.1 19.7 13.5 (13) -44.0ERP (21) 26.2 17.6 14 (12) -46.6

Deckersbach et al. 2006 HR (15) 29.3 18.3 18.4 (8) -37.2SP (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) -46.2SP (65) 24.6 21.1 9.9 (12) 10.4 (8) -57.7

Wilhelm et al. 2012 HR (63) 24.0 17.8SP (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.

tervals. A greater proportion of patients from the HRTgroup were evaluated as positive responders comparedwith the supportive psychotherapy group, resulting in apossible bias in follow-up tic severity scores.The study by Wilhelm et al. (2012) used a similar para-digm to that of Piacentini et al. (2010) in order to inves-tigate the efficacy of HRT as part of a tailored compre-hensive intervention (CBIT). Again, only participantsshowing positive results were invited for follow-up as-sessments. The reliability of the follow-up data was re-duced by the fact that of the 24 participants invited, on-ly 15 were available for assessment. Additionally, theauthors rated clinical improvement at 6-month follow-upusing the Clinical Global Impression-Improvement Scalerather than the YGTSS, thus limiting the accuracy andgeneralizability of the findings.A further set of problems with the examined literature re-lates to the blinding procedure and ITT analysis. In thestudy by Wilhelm et al. (2003), the interviewers who rat-ed the YGTSS were not blinded to which treatmentgroup the patients were in. Moreover, although patientswho dropped out before the eighth session of their treat-ment (two in the HRT group, one in the supportive psy-chotherapy group) were excluded from the analysis,those who dropped out after this point (one in the HRTgroup, two in the supportive psychotherapy group) wereincluded. In the more recent study by Wilhelm et al.(2012), tic severity was assessed by a blinded inde-pendent clinician and conventional ITT analysis wasperformed. In the study by Deckersbach et al. (2006),the YGTSS ratings, the clinical diagnoses and the treat-ment interventions for the patients were all performed bythe same author. Therefore, it is likely that this studywas not assessor-blinded. Moreover, in this study two ofthe initial 32 patients dropped out. Data from these twopatients were not included in the analysis. However,when the analysis was repeated using an ITT paradigm,incorporating the two drop-out patients, there was nochange in the significance of the results. In contrast tothese articles, the studies by Verdellen et al. (2004) andPiacentini et al. (2010) were both assessor-blinded andused an ITT analysis, thus increasing the reliability andvalidity of their findings.Treatment protocols varied widely across the reviewedstudies. Although all had a treatment group allocated toHRT, the specific elements incorporated into the treat-ment intervention and the frequency with which it wasadministered differed between the studies. For example,the protocols adopted by Piacentini et al. (2010) andWilhelm et al. (2012) included eight HRT sessions,whereas the protocols of the other studies included ten(Verdellen et al., 2004) or fourteen (Wilhelm et al., 2003;Deckersbach et al., 2006) sessions. Likewise, althoughthe five studies used competing response and aware-ness training as part of the HRT procedure, the othercomponents of the HRT intervention were not consistentacross all the studies. Finally, outcome data may havebeen affected by the different rates of psychiatric disor-ders across the studies: comorbid attention deficit andhyperactivity disorder was reported in 30.2% of patientsin the study by Verdellen et al. (2004), 27.9% in thestudy by Wilhelm et al. (2012), and 26.2% in the studyby Piacentini et al. (2010), whereas obsessive-compul-sive disorder was reported in 19.0% of patients in thestudy by Piacentini et al. (2010), 18.0% in the study by

Wilhelm et al. (2012), and 14% in the study by Verdellenet al. (2004). Deckersbach et al. (2006) reported onlyfigures for comorbid obsessive-compulsive disorder,which was present in 30.0% of patients, whilst Wilhelmet al. (2003) did not report rates of comorbid diagnoses.This systematic review provides an up-to-date summaryof the existing scientific evidence for the use of HRT inthe treatment of tics in TS and other CTDs. However,there are some intrinsic limitations to our literature re-view strategy. For example, relevant information mighthave been missed by choosing to use selective inclu-sion criteria for the reviewed studies. Moreover, thereemerged significant differences between the studies incovariate variables, such as gender and age. Althoughsuch differences are acknowledged in this review, ad-justment for these variables was not performed. Further-more, other potential confounders, such as socio-eco-nomic status, ethnic origin, etc., were not considered.The overall results of our systematic literature review re-inforce the conclusions of the recently published Euro-pean clinical guidelines on behavioral and psychosocialtreatments for TS and other CTDs (Verdellen et al.,2011), which suggest that HRT is an effective treatmentoption for reducing tic severity in both adults and chil-dren. This supports the clinicians’ perception that HRTshould be considered as a first-line behavioral treatmentfor obtaining tic suppression in patients of all ages(Verdellen et al., 2011). However, currently there are on-ly a few specialists who are trained and experiencedenough to administer HRT sessions (Piacentini et al.,2010). More teaching and training in this technique arerequired in order to expand its application to the treat-ment of tics throughout healthcare systems (Woods etal., 2007). Existing evidence would justify a more wide-spread diffusion of HRT, which in turn would allow fur-ther research on larger and clinically diverse cohorts ofpatients.This review has highlighted some potential areas for fur-ther research. Verdellen et al. (2004) noted statisticallysignificant reductions in tic severity in patients treatedwith ERP. The use of this behavioral therapy is support-ed by relatively little research in TS populations. Futurestudies should investigate the efficacy of ERP in largersamples of patients with TS and other CTDs, in order toallow reliable comparisons with HRT. More research in-to whether behavioral therapies could represent a validcomplement or alternative to pharmacological interven-tion for tic management is also required. Some patientsin the reviewed studies were taking medication whilstundergoing the behavioral interventions, and otherswere not. Research comparing tic severity in patients re-ceiving first-choice antidopaminergic medication versusthose receiving HRT could shed more light on the realefficacy of HRT compared with drug therapy. Quality oflife should also be taken into consideration, in additionto tic severity. By replacing pharmacotherapy with HRT,adverse effects may be reduced and quality of life im-proved. Even if tic severity scores remain higher in pa-tients undergoing HRT compared with those on medica-tions, patients who experience severe side effects fromtheir medication may prefer this compromise. In com-plex conditions like TS, the choice between differenttreatment strategies should always take into accountboth subjective and objective factors, in addition thebest level of evidence from the scientific literature.

Habit reversal therapy for tic disorders

Functional Neurology 2013; 28(1): 7-12 11

Acknowledgments

The authors are grateful to the Tourette Syndrome Asso-ciation-USA and Tourettes Action-UK for their continuingsupport.

References

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Cavanna AE, Schrag A, Morley D, et al (2008). The Gilles de laTourette syndrome-quality of life scale (GTS-QOL): Devel-opment and validation. Neurology 71:1410-1416.

Cavanna AE, Servo S, Monaco F, et al (2009). The behaviouralspectrum of Gilles de la Tourette syndrome. J Neuropsychi-atry Clin Neurosci 21:13-23.

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Eddy CM, Rizzo R, Gulisano M, et al (2011). Quality of life inyoung people with Tourette syndrome: a controlled study. JNeurol 258:291-301.

Frank M, Cavanna AE (2013). Behavioural treatments forTourette syndrome: An evidence-based review. Behav Neu-rol in press.

Hassan N, Cavanna AE (2012). The prognosis of Tourette syn-

drome: implications for clinical practice. Funct Neurol 27:23-27.

Moher D, Liberati A, Tetzlaff J, et al (2009). Preferred reportingitems for systematic reviews and meta-analyses: the PRIS-MA statement. PLoS Med 6: e1000097.

O’Connor KP, Brault M, Robillard S, et al (2001). Evaluation ofa cognitive-behavioural program for the management ofchronic 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-trolled trial. JAMA 303:1929-1937.

Robertson M, Cavanna A (2008). Tourette syndrome: The facts.2nd ed. Oxford; Oxford University Press.

Roessner V, Plessen KJ, Rothenberger A, et al (2011). Euro-pean clinical guidelines for Tourette syndrome and other ticdisorders. Part II: pharmacological treatment. Eur Child Ado-lesc Psychiatry 20:173-196.

Verdellen CW, Keijsers GP, Cath DC, et al (2004). Exposurewith response prevention versus habit reversal in Tourette’ssyndrome: a controlled study. Behav Res Ther 42:501-511.

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Wilhelm S, Deckersbach T, Coffey BJ, et al (2003). Habit re-versal versus supportive psychotherapy for Tourette’s dis-order: a randomized controlled trial. Am J Psychiatry 160:1175-1177.

Wilhelm S, Peterson AL, Piacentini J, et al (2012). Randomizedtrial of behavior therapy for adults with Tourette syndrome.Arch Gen Psychiatry; 69:795-803.

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12 Functional Neurology 2013; 28(1): 7-12

August 2016 | Volume 7 | Article 1351

Original researchpublished: 11 August 2016

doi: 10.3389/fpsyt.2016.00135

Frontiers in Psychiatry | www.frontiersin.org

Edited by: Kirsten R. Müller-Vahl,

Hannover Medical School, Germany

Reviewed by: Ewgeni Jakubovski,

University of Heidelberg, Germany Tárnok Zsanett,

Vadaskert Child Psychiatry Hospital and Outpatient Clinic, Hungary

*Correspondence:Julie B. Leclerc

leclerc.julie@uqam.ca

Specialty section: This article was submitted to

Child and Adolescent Psychiatry, a section of the journal Frontiers in Psychiatry

Received: 26 February 2016Accepted: 19 July 2016

Published: 11 August 2016

Citation: Leclerc JB, O’Connor KP, J.-Nolin G,

Valois P and Lavoie ME (2016) The Effect of a New Therapy for Children

with Tics Targeting Underlying Cognitive, Behavioral, and

Physiological Processes. Front. Psychiatry 7:135.

doi: 10.3389/fpsyt.2016.00135

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

Tourette disorder (TD) is characterized by motor and vocal tics, and children with TD tend to present a lower quality of life than neurotypical children. This study applied a manualized treatment for childhood tics disorder, Facotik, to a consecutive case series of children aged 8–12 years. The Facotik therapy was adapted from the adult cogni-tive and psychophysiological program validated on a range of subtypes of tics. This approach aims to modify the cognitive–behavioral and physiological processes against which the tic occurs, rather than only addressing the tic behavior. The Facotik therapy lasted 12–14 weeks. Each week 90-min session contained 20 min of parental training. The therapy for children followed 10 stages including: awareness training; improving motor control; modifying style of planning; cognitive and behavioral restructuring; and relapse prevention. Thirteen children were recruited as consecutive referrals from the general population, and seven cases completed therapy and posttreatment measures. Overall results showed a significant decrease in symptom severity as measured by the YGTSS and the TSGS. However, there was a discrepancy between parent and child rating, with some children perceiving an increase in tics, possibly due to improvement of awareness along therapy. They were also individual changes on adaptive aspects of behavior as measured with the BASC-2, and there was variability among children. All children maintained or improved self-esteem posttreatment. The results confirm the conclusion of a previous pilot study, which contributed to the adaptation of the adult therapy. In summary, the Facotik therapy reduced tics in children. These results underline that addressing processes underlying tics may complement approaches that target tics specifically.

Keywords: Tourette disorder, tics, children, treatment, cognitive–behavioral therapy, psychophysiological

2

Leclerc et al. Intervention in Children with Tics

Frontiers in Psychiatry | www.frontiersin.org August 2016 | Volume 7 | Article 135

inTrODUcTiOn

Definition and symptomsTourette disorder (TD) is considered a motor disorder in the neurodevelopmental disorders section of the DSM-5 (1). TD is diagnosed by multiple motor tics and at least one vocal tic present for at least 1 year. This child-onset disorder appears to be a com-plex condition with the changing nature of tics evolving over time in frequency, intensity, localization, and complexity (2). Children and adolescents are the most affected by TD with a prevalence rate between 0.3 and 0.9% (3).

Studies report that children with TD are more likely to expe-rience daily struggles in several spheres of activities (4). Cutler et  al. (5) showed that 66% of 57 young participants reported some physical consequences associated with tics (e.g., pain, aches, physical discomfort). In a school setting, tics may interfere with academic performance and produce difficulty concentrating, writing, or reading (6). Children with TD may also experience relationship problems because they can be victimized when their tics are severe and complex, and they can be stigmatized or have more conflicts with their parents and teachers than other children (7–9). Hoekstra and colleagues (10) reported an increase in emotional problems over time in TD children and a higher rate of cognitive difficulties than children in the general population (p < 0.05) (11). Consequently, children with TD tend to present a lower quality of life than neurotypical children (5, 12, 13).

About 85% of individuals with TD report at least one comorbid disorder (14, 15). The most frequent comorbidity in children with TD is attention deficit hyperactivity disorder and oppositional defiant disorder (16, 17), but they can also show obsessive–compulsive disorder, anxiety disorder, and depres-sive disorder (18, 19). The severity of the comorbidity seems to worsen the quality of life of these children often more than tics. The variety of symptoms then interferes in daily functioning, leading to several impairments in children with TD and comor-bidity (20, 21).

Behavioral TherapiesCanadian, American, and European clinical guidelines recom-mend medication plus a cognitive–behavioral treatment for reducing tics (22–24). Behavioral therapies are recommended as evidence-based interventions to manage tics, and behavioral approaches have taken several forms depending on whether the tic is conceptualized.

The comprehensive behavioral intervention for tics (CBIT) proposed by Woods and colleagues (25) is mainly based on the habit reversal treatment [HRT, Ref. (26)], which was reported to be effective for both children and adults (27–31). In addition to HRT components, such as awareness training, relaxation, competing response, contingency management, and generaliza-tion training, CBIT emphasizes the importance of addressing environmental factors that can influence tic manifestations. This 8-week treatment also uses strategies such as psychoeducation about tics and function-based interventions. CBIT appears to be effective for tic reduction in children and adults with TD (32–34). However, the premonitory urge remained unchanged across therapy (35), whereas, in theory, it should decrease with

the negative reinforcement process. Therefore, the mechanisms underlying tics and therapeutic processes remain unclear.

In treatment by exposure and response prevention [ERP, Ref. (36)], the aim is to reduce tics by breaking the negative reinforce-ment loop between the premonitory urge and the tic itself. The individual learns to tolerate the premonitory urge and resists the appearance of tics for longer and longer periods (response prevention). A study comparing two treatment protocols ERP/HR in 43 participants with TD (aged 7 to 55 years old) showed no significant difference between groups in reduction of tics, where 58% of the participant in the ERP group and 28% of the participant in the HR group showed a decrease of at least 30% on the YGTSS (37). However, some children are unable to feel and detect the premonitory urges (38), and the therapy to resist the tic may be sometimes emotionally difficult for the child because of the pressure to succeed.

cognitive Psychophysiological TreatmentAn elaboration of the functional role of tics in sensorimotor regu-lation is found in O’Connor’s (39) cognitive psychophysiological model. This model conceives of tics as serving a function of sen-sorimotor autoregulation, while decreasing tension in muscles inappropriately contracted. Tension in TD seems characterized by a cycle where the muscle is inappropriately prepared prior to execution (40). For example, during an activity, the individual with a tic is preparing too quickly for an immediate response, but, at the same time, preparing more muscles with more effort than necessary. This preparation is inappropriate so the tic action relieves, in part, through local tension release. Electromyographic (EMG) recordings of tic-affected muscles show that these mus-cles are rarely associated with zero tension and have a greater difficulty compared to non-affected muscles achieving different degrees of tension rather just an all or nothing state of tension [(41) and replication is in preparation]. People suffering from tics also subjectively report chronic tension, and Hoogduin et al. (36) reported high overall muscle tension as a consistent feeling in all patients, when identifying premonitory urges. The originality of this approach is its targeting of excessive overall sensorimotor activations by addressing cognitions, behaviors, and physiologi-cal strategies, which engender excessive tension leading to and maintaining tics, rather than learning a competitive response to the tic or to the urge to tic.

The cognitive psychophysiological [CoPs; Ref. (40)] treatment for tics was developed in order to focus on the processes influenc-ing thoughts and behaviors underlying tics, rather than working exclusively on the tic per se. Several cognitive factors are targeted in the CoPs treatment, such as anticipation, rigid beliefs (e.g., about action and organization), a judgmental style of thinking, attentional focus, and a perfectionistic style of planning action involving over-activity and over-preparation. This thinking can encourage the tendency to complete several tasks rapidly and at the same time (a style termed over-activity), together with an over-investment in preparation for action by recruiting redundant muscles and employing more effort than necessary (a style termed over-preparation). People with tics frequently experienced rigid thinking about how they should act and appear, resulting in inflexible black and white thoughts, which impair

TaBle 1 | age, sex, medication intake, and length of the therapy for each participant.

Participant age sex Medication intake

Days between first and last therapy session

1 11 Girl Valerian, atomoxetine 912 10 Boy – 983 10 Boy – 1154 12 Boy – 985 11 Boy Melatonin 1046 9 Boy Methylphenidade,

risperidone106

7 9 Boy – 105

TaBle 2 | Tests of tic severity differences between completers and non-completers on the YgTss and on the Tsgs.

scale Median score for completers (participants)

Median score for

non-completers

asymptotic Wilcoxon–Mann–

Whitney Test

YgTssGlobal 37.00 29.50 Z = −0.857, p = 0.39Tic severity 23.00 19.50 Z = −0.714, p = 0.48Deterioration 10.00 10.00 Z = −0.158, p = 0.87

TsgsGlobal 25.50 21.08 Z = −0.286, p = 0.78Tic domain 13.00 10.00 Z = −0.644, p = 0.52Social functioning domain

10.00 10.00 Z = 0.443, p = 0.66

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adaptation (42). In addition, meta-cognitive factors, as defined by O’Connor as thoughts about performing the tic and expecta-tions or beliefs about tic onset, are targeted along with how people with tics evaluate and judge situations at high risk for eliciting tics (42). These cognitive factors also interact with physiological factors such as an increased sensorimotor activation, leading to hypersensitivity and over-reactivity and so, as a circular linking, to tic onset (42). A behavioral target of this therapy is to break the negative reinforcement cycle between the tic onset and the immediate relief of the accumulation of muscular tensions caused by the heightened sensorimotor activation (40). There is evidence of tension building up, prior to ticking, and subjective reports of relief, post-ticking (40). The aim of the CoPs treatment is to help the individual in understanding how these cognitive–behavioral and physiological factors lead to tension and how gradually addressing and modifying them can prevent tension build-up and tic onset, while increasing self-control.

An open trial showed the efficacy of CoPs treatment in adults with tics compared to waitlist with a 6:1 ratio (43). Results showed that 10 of the 85 participants completely reduced tic onset after therapy (gains maintained at 6-month follow-up). Prior results also showed efficacy in tic reduction in adults with or without medication, following CoPs treatment (44, 45). The therapy was applied to five adolescents with TD, in a pilot study (46). Results showed a decrease in tic frequency and intensity and improve-ment in social functioning for the five participants. The CoPs treatment has also been adapted for children with TD address-ing explosive outbursts (EO). Results showed a decrease of EO 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 a 67% decrease between the beginning of therapy and follow-up, despite an increase of EO frequency at baseline assessment (47). Finally, a single-case design study of the CoPs treatment address-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 observed posttreatment (p < 0.001, d = 0.97), and the decrease was monitored over 1 year. Results showed a decrease of at least 1 SD in measures, post 12 months.

After this pilot study, a manualized version of the treatment protocol in children termed Facotik has been finalized (49), and the aim of the current study is to evaluate its efficacy in a larger consecutive case series. Based on previous research, a decrease of tic severity was expected after treatment. The efficacy of the treat-ment adapted for children will have important implications for the intervention in TD and whether addressing the underlying sensorimotor processes is sufficient to reduce tics.

MaTerials anD MeThODs

ParticipantsThe recruitment was carried out through the Centre d’études troubles obsessionnels-compulsifs et tics – Institut universitaire en santé mentale de Montréal. Consecutive referrals were evaluated according to the inclusion criteria: 8–12 years old, a primary TD diagnosis, and medication stable at least 1 month before treatment

and stable for the duration of the therapy. Exclusion criteria were: a diagnosis of autism spectrum disorder or intellectual disability, receiving another behavioral treatment for tics during the study, and a problem of geographical location to assure treatment adherence. Thirteen children were originally recruited and seven children completed therapy and posttreatment measures (one retracted before therapy, four abandoned during therapy, and one completed the therapy, but did not complete the follow-up). Table  1 summarizes age, sex, medication intake, and number of days between the first and the last therapy session for each participant that completed the therapy. The mean age of the seven participants was 10.29 years (six boys, one girl). Mean age of the non-completers was 9.4 years (four boys, two girls). There was no statistical difference between completers and non-completers over all measures of tic severity in the pre-treatment assessment as shown in Table 2.

assessment MeasuresYale Global Tic Severity ScaleThe Yale Global Tic Severity Scale [YGTSS, Ref. (50)] is used to assess a global scale based on a tic severity subscale with five dimensions (number, frequency, intensity, complexity, and inter-ference of tics) and an impairment subscale. Inter-rater agree-ment ranges from 0.52 to 0.99 and 0.85 for the global severity score. Factor loadings on the items in factor analyses revealed two separated factors, one for motor tics and overall impairment and one for phonic tics, although the two factors account only for 8% of the variance showing a low-factor validity. The YGTSS

TaBle 3 | Basc-2 T-scores indicating thresholds scores for clinical and adaptive scales.

Type of scales T-scores

<30 40 50 60 >70

Clinical Normal At-risk Clinical

Adaptive Clinical At-risk Normal

The gray shade are visual indicator of the At-risk and Clinical score range for the BASC-2.

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is completed by the children with the help of an independent evaluator. Scores for the YGTSS ranged from 0 to 100.

Tourette’s Syndrome Global ScaleThe Tourette’s Syndrome Global Scale [TSGS, Ref. (51)] is used to assess a global scale based on a tics domain and a social function-ing domain. The tics domain evaluates frequency and disruption of different subtypes of tics (motor/phonic and simple/complex). Social functioning domain included the assessment of learning, motor restlessness, and occupational problems. There is a good inter-rater agreement (0.89) for the global scale, and the criterion validity was demonstrated as a correlation between TSGS’s global scale and severity of TD symptomatology ranked by four raters ranging from 0.46 to 0.99. The TSGS highly correlates with the 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-pleted by the children with the help of an independent evaluator and by one of their parents. Scores for the TSGS ranged from 0 to 100.

Behavior Assessment System for Children – Second EditionThe Behavior Assessment System for Children  –  Second Edition [BASC-2, Ref. (52)] is a multidimensional and multimodal assessment for adaptive and clinical aspects of behavior and personality in children. Two tests were used to assess participants on secondary outcomes of the therapy, one by the parents and one by the children. The Parent Rating Scale (PRS) assesses nine clinical scales (hyperactivity, aggression, conduct problems, anxiety, depression, somatization, atypicality, withdrawal, and attention problems), five adaptive scale (adaptability, social skills, leadership, activities of daily living, and functional communica-tion), three clinical composite scale (externalizing problems composite, internalizing problems composite, and behavioral symptoms index), and one adaptive composite scale (Adaptive skills composite), over 160 items. The self-reported personality (SRP) for children assesses 10 clinical scales (attitude to school, attitude to teachers, atypicality, locus of control, social stress, anxiety, depression, sense of inadequacy, attention problems, and hyperactivity), four adaptive scales (Relations with parents, Interpersonal relations, Self-esteem and Self-reliance), 4 clini-cal composite scales (school problems composite, internalizing problems composite, inattention/hyperactivity composite, and emotional symptoms index), and 1 adaptive composite scale (personal adjustment composite), over 139 items.

For both tests, scores were converted to T-score based on the age of the participant. Intervals of T-scores indicating thresholds for “normal,” “at risk,” and “clinically significant” ranges are presented in Table 3, for the clinical scales and for the adaptive scales. Internal consistency of scales and composite scales for the PRS were all above α = 0.80, and test–retest reliability were all above 0.77. For the SRP, internal consistency of scales and composite scales ranged from α = 0.71 to α = 0.96 and test–retest reliability ranged from 0.66 to 0.83. Change in time on the SRP could be attributed to low reliability. Confirmatory factor analysis for the PRS showed a comparative fit index of 0.88 and a root mean square error of approximation of 0.13, both indicating near

good validity of the test. Confirmatory factor analysis results were equivalent on the SRP, with a comparative fit index of 0.90 and a root mean square error of approximation of 0.11, indicating good and near good validity of the test.

Culture-Free Self-esteem InventoryThe Culture-Free Self-Esteem Inventory  –  second edition form B [CFSEI, Ref. (53)] was used to evaluate change in self-esteem in children between pre- and posttreatment as a secondary benefit of the therapy. The CFSEI form B included 30 yes or no items assessing five subscales (general, social, academic, parents, and defensiveness) extracted from form A. Correlation between the two forms was 0.86. Test–retest reliability was ranging from 0.79 to 0.92 for the total score and was ranging from 0.49 to 0.80 for subscales. Concurrent validity was obtained with the self-esteem inventory (54), ranging from 0.71 to 0.80.

Treatment MaterialThe Facotik treatment is a manualized therapy (therapist and child manual), including a self-monitoring diary and a token economy motivational board. The therapist’s manual includes an explicit protocol for every exercise and instructions for the participants and their parents for each session of the therapy with time estimation. The child’s manual contains information on each topic of the treatment with colorful examples, activities named “challenges,” and exercises to practice between therapy sessions named “missions of the week.” A particular concern was to adapt the CoPs exercises to a child’s cognitive level of func-tioning. For this purpose, a narrative approach was proposed in Facotik where two characters named Lea and Nico accompanied the child over the treatment. To improve understanding, new ele-ments have been added in the children adaptation of the therapy, such as concrete language, practical examples, metaphors, visual analogies, and pictures. Also, behavioral restructuring precedes cognitive restructuring, unlike the adult version. The self-mon-itoring diary is used for assessing frequency of tics, conducting a functional analysis (antecedents, consequences), and clinical awareness training. Each participant notes the frequency of a targeted tic for a 15-min period, once a day, in a predetermined high-risk tic onset situation. The child also estimates the intensity of the tics (low, medium, or high) and his/her principal activity at this time. The token economy motivational system works on a three-point award for each therapy session, one for participat-ing in the challenges during the session, one for completing the self-monitoring diary every day and one for completing the weekly exercises or missions between sessions. Children could exchange nine points for a specific reward (not  necessarily

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

clinical objectives

session Procedure and therapeutic components

Awareness training

1 – Introduction to the therapy; psychoeducation about TD and tics – 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 discrimination

6 – Awareness training of muscular tension and muscular 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-motor activation

8 – Reducing sensory–motor activation in avoiding anticipatory vigilance to sensation and not attributing significance to sensation in high tic onset risk situations (stopping negative reinforcement process)

– Identification of personal style of planning action (over-activity, over-investment)

Style of planning action

9–10 – Understanding the link between a tension-producing style of planning action and specific experienced muscle tension, and tics (reducing over-activity and over-investment)

– 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 restructuring

11–13 – Modifying core beliefs about perceptions of others and related to style of action planning – 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 restructuring

11–13 – Modifying preparation for a situation (e.g., prevention by relaxation) – 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 restructuring

11–13 – Cognitive, sensorimotor, emotional, and behavioral components of this planning can be addressed at the same time during cognitive–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 prevention

14 – Keep practicing, refresh knowledge, and maintain gains – Anticipate situations that may trigger relapse of tics and change other aspects of life style – Feedback and therapy conclusion

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tangible, e.g., a specific activity), determined with their parents at the second session.

ProcedureParticipants and one of their parents completed the pre-treatment assessment with a trained specialized evaluator, including YGTSS, TSGS, BASC-2, and CFSEI. The certified evaluator was independ-ent of the therapy process and research protocol. The evaluator completed the scoring of the YGTSS and the TSGS, after semi-structured interviews with the parents and the children separately. Afterward, each participant followed the Facotik therapy with one of the two trained psychotherapists: a licensed psychologist and a certified final year graduate student. The Facotik therapy

lasted 12 to 14 sessions depending on the understanding and on the success of the steps by the child. Each 90-min session began by reviewing the content previously discussed and ended with 20 min of parental training (information on the clinical objective of the session, supportive coping strategies, and how to give posi-tive reinforcement for home exercises to their child). Information was also given to the parents on the theoretical approach to enable them to act as a collaborator in the therapy process based on a psychoeducation method (55, 56). Psychotherapists wrote a progress report at the end of each therapy session, indicating children’s progress and difficulties.

The Facotik treatment is progressive and passes through progressive therapeutic steps with a “one tic at a time” approach.

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Table  4 presents a schema of the clinical objectives and the therapeutic components of each therapy session. The clinical objective distributed over 14 sessions are: awareness training, muscle discrimination, relaxation, reduced sensorimotor activa-tion, modifying style of planning action, cognitive restructura-tion of anticipation and appraisals, behavioral restructuration, generalizations, and preventing relapse. The first clinical objective (awareness training) is spread over several sessions, while, from the 9th therapy session, several clinical objectives are addressed in the same sessions. Between each therapy session, the child completed the self-monitoring diary and the weekly exercises. Three participants completed treatment in 13 sessions, and four others completed therapy in 14 sessions (the total duration of the therapy was an average of 102.49 days between the first and the last session, all children skipped at least 1 week between two sessions due to sickness or scheduling constraints). At posttreatment, each participant and one of their parents completed all assessments on the YGTSS, the TSGS, the BASC-2, and the CFSEI.

ethicsThis study was approved by the local ethic review board of the Institut universitaire en santé mentale de Montréal in accordance with the ethical standards of the Canadian Tri-Council Policy Statement of Ethical Conduct for Research Involving Humans. The parents of the participants (or the legal guardian) gave their signed consent for the participation of their child to the study (assess-ments and therapy), and the child himself gave his or her approval.

Data analysesTwo analysis procedures were planned. For statistical analyses, one-sided exact Wilcoxon signed-rank test was conducted due to the small sample on the children and parents’ assessments to evaluate global symptoms decrease after treatment, as measured by the YGTSS global scale and the TSGS global scale. Additional one-sided exact Wilcoxon signed-rank tests were conducted with the tic severity subscale and the impairment subscale of the YGTSS and with the tics domain and the social functioning domain of the TSGS, using a Pratt correction in the case of tied ranks. Person’s correlations were computed between parents and children for pre-treatment scores, posttreatment scores, and difference scores on all scales and subscales. Difference scores were computed as pre-treatment score minus posttreatment score for each parents and children. All analyses were calculated with n = 7 based on a complete dataset. All statistical analyses were computed using R statistical software (57) and the coin package (58). For clinical results, changes of at least 1 SD on the BASC-2 subscales and on the CFSEI were reported.

resUlTs

statistical resultsResults of the parents’ assessments on the YGTSS global scale showed a general and significant symptom decrease at posttreat-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 themselves, as they estimated no significant symptoms decrease (from Mdn  =  37.00 to Mdn  =  26.00, Z  =  −0.85, p  =  0.234).

Figure  1 shows the global scale on the YGTSS for pre- and posttreatment as assessed by the children and their parent. Four participants showed a decrease on the YGTSS global scale for both child and parent, while the other three reported discrepant results. Correlations between parents and children showed good agreement for pre-treatment scores (r = 0.70, p = 0.005), but poor agreement for posttreatment scores (r = 0.34, p = 0.234) and for difference scores (r = 0.30, p = 0.300).

Analysis of the YGTSS subscales showed a significant decrease in both the tic severity subscale (Mdn = 27.00 to Mdn = 15.00, Z = −2.37, p = 0.008, r = −0.63) and the impairment subscale (Mdn = 20.00 to Mdn = 10.00, Z = −2.19, p = 0.031, r = −0.69), as observed by parents. Children reported a significant decrease on the tic severity subscale (Mdn = 23.00 to Mdn = 16.00, Z = −2.29, p  =  0.016, r  =  −0.66), but not on the impairment subscale (Mdn = 10.00 to Mdn = 10.00, Z = 0.81, p = 0.813). Correlations between parents and children on the tic severity subscale were 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 difference scores (r  =  0.29, p  =  0.315). Correlations between parents and children on the impairment subscale were poor for pre-treatment scores (r = 0.61, p = 0.021), good for posttreatment scores (r = 0.75, p = 0.002), and moderate for difference scores (r = 0.50, p = 0.069).

In contrast to YGTSS, results on the TSGS global scale showed a significant symptom decrease after treatment, as assessed by 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, Z = −2.20, p = 0.016, r = −0.59). Figure 2 shows scores on the TSGS global scale for pre- and posttreatment as assessed by chil-dren and parents for each participant. Five participants showed a decrease in tic symptoms on the TSGS global scale, while a further two reported discrepant results. Correlations between parents and children showed good agreement for pre-treatment scores (r = 0.74, p = 0.002), poor agreement for posttreatment scores (r = 0.19, p = 0.515), and moderate agreement for differ-ence scores (r = 0.47, p = 0.090).

Analysis of the TSGS domains as reported by parents showed a significant decrease in the tics domain (Mdn = 13.00 to Mdn  =  4.00, Z  =  −2.37, p  =  0.008, r  =  −0.63), but not on the social functioning domain (Mdn =  10.00 to Mdn =  10.00, Z = −0.71, p = 0.750). Children reported a significant decrease on tics domain (Mdn  =  13.00 to Mdn  =  6.00, Z  =  −2.37, p = 0.008, r = −0.63), but not on the social functioning domain (Mdn = 10.00 to Mdn = 6.67, Z = 0.78, p = 0.281). Correlations between parents and children on the tics domain were good for pre-treatment scores (r =  0.75, p =  0.002), moderate for post-treatment scores (r = −0.41, p = 0.145), and good for difference scores (r = 0.77, p = 0.001). Correlations between parents and children on the social functioning domain were moderate for pre-treatment scores (r = 0.55, p = 0.042), poor for posttreatment scores (r =  0.20, p =  0.493), and negative for difference scores (r = −0.11, p = 0.708).

clinical resultsThe BASC-2 and the CFSEI were used to detect if the Facotik therapy brought secondary benefits to develop adaptive and

FigUre 1 | results on the YgTss for parents and children in pre- and posttreatment.

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clinical aspects of behaviors and self-esteem. Table  5 showed clinical changes of at least 1 SD on the BASC-2 SRP and on the BASC-2 Parent rating scale (PRS). There were no globally signifi-cant changes over participants even if there were some changes at the individual level. For all participants and all clinical subscales together, parents reported improvements in 13 subscales and decreases in 6 subscales, while the children report 9 improvements and 9 decreases. An overall decrease is observed for participant 1 (as noted by the parent) and participant 7 (as noted by the child). Participant 6 is the only one to present only slight increases observed by the parent (atypicality) and the child (anxiety, atten-tion problems). However, children scoring shows that the attitude toward school, teachers, and the school problems composite increased slightly for three participants. All other participants showed decreases and increases in some subscales without gen-eral trend. For the adaptive scales, improvements are observed by parents in five subscales for the seven participants (adaptability for two participants, leadership, functional communication, and adaptive skills). Children have noted improvements in three subscales (self-esteem for two participants and self-reliance) and one decrease (interpersonal relations). All these results are not significant, but showed clinical changes of at least 1 SD.

One child showed improvement on self-esteem as measured by the CFSEI, with an increase on the total score of 2 SD, the global

subtest of 1.5 SD, the parent subtest of 1 SD and the academic subtest of 2.7 SD. All other participants maintained medium to high levels of self-esteem from pre- to posttreatment. Table  6 shows data for all participants on the CFSEI.

DiscUssiOn

Principal resultsThe purpose of the current study was to evaluate the efficiency of the Facotik treatment to decrease the severity of tics in children aged 8–12 years old. Secondary benefits to improve adaptive and clinical aspects of behaviors and self-esteem were also anticipated.

The overall results showed a significant decrease in tics as assessed by the parents of children with TD. The results as assessed by children were discrepant; tics decreased sig-nificantly for all children as measured with the TSGS and four participants on seven reported a non-significant decrease on the YGTSS. However, children and parents, all reported a significant decrease in tic severity when the subscales of the two questionnaires were analyzed. What is interesting is that, even considering this change in tics, children and parents generally perceive no changes in the impairment subscale. This could be explained by the presence of comorbidity symptoms, which was not controlled in this study or by the subjective experience of

FigUre 2 | results on the Tsgs for parents and children in pre- and posttreatment.

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the impairment. The correlations between the child/parents’ rating showed a good agreement regarding the tic severity in pre-treatment, but not in posttreatment, neither for difference scores (pre-minus posttreatment), suggesting a disagreement about the perception of change. There are two possible explana-tions for the preceding results. First, the difference between the child/parents’ rating on the YGTSS and the TSGS may highlight the sensitivity of the TSGS, which is multidimensional and is rated on a scale rather than in categories as in the YGTSS. Second, the tic decrease might not always be detected by the children themselves and discrepancies between the child/par-ents’ rating may be explained by one of the therapy components termed “awareness training” (59). Children are more aware of their tics after the therapy and they can detect and report them more accurately than at pre-treatment, while the parents noticed a decrease of tics because they were already conscious of the tics. The self-monitoring diaries are a key component of the tic awareness training (60). The focus on a single tic may help children to acknowledge the difference between a situation with high risk of tic onset versus low-risk situations. Some situations may be perceived as a high risk in the first place, but may become low risk following the self-monitoring diary. Thus, the mixed results may be more of an indication of the therapy process than an absence of progress in tic reduction.

Adaptive and clinical aspects of behaviors in children, as measured by the BASC-2, showed no significant changes, but improvements and clinical changes were reported individually, suggesting a regular fluctuation over time. There are further improvements to clinical subscales than deterioration as reported by children and parents. As an example, internal-izing problems showed punctual improvement. Improvements have also been noticed in general for the adaptive scales. This highlights positive results although there are no significant dif-ferences. All the participants maintained or reached medium to high levels of self-esteem from pre- to posttreatment. However, attitude toward school or teacher appear to have increased for three participants after therapy. This could be explained by the fact that the therapy ended concurrently with or after the end of the school year, and posttreatment assessment took place (particularly for participants 4 and 5) just before the return to school period (in August).

In terms of experiential factors, all children benefited from the therapy, and no adverse effects were reported by the participants or their parents. The participants reported to the therapists that theoretical concepts and exercises were presented in a clear and colorful way, which made them comprehensive for all, even for participant 4 who had language issues; some activities took more time, but without causing a significant delay. Some children

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

aChange in T-score of at least 1 SD.

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had a little trouble to identify their irrational thoughts during high-risk tic onset situations, and all participants reported that completing their self-monitoring diary and relaxation exercises were most helpful to them. According to the therapists, the set of strategies formed a coherent whole, and children were open-minded to the complementary elements of the therapy; they were particularly interested when the style of action planning was addressed.

limitationsThe limitations of the present study are those inherent in a con-secutive case series without baseline or control group and a lim-ited number of participants. The attrition rate was around 40%, but there were no clinical or demographical differences between participants and those who abandoned. Personal motivation and difficulty scheduling therapy sessions appear to account for attrition. This protocol had a confounding variable, considering

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that the posttreatment was concomitant with the preparation of a new school year. This situation could have an impact on tics 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. Nonetheless, the statistical and clinical significance of the tic reduction indicates potential efficacy of the Facotik treatment.

Future researchThe main strength of the current study is the demonstration of the effect of the Facotik treatment for the decrease of tic severity in children as a first step of the validation procedure. These findings, with a manualized treatment and a structured protocol, highlight the clinical importance of working on the cognitive and central processes underlying tics in children as in adults (40). CoPs treatment in adults has been shown to produce neurocognitive changes in style of action and concomitant cerebral functioning (61, 62). Such physiological changes (activation of the pre-motor and motor cortex) related to the intervention remain to be vali-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 target for effective interventions or if the processes underlying tics should also be addressed to obtain greater symptom reduc-tion and wider behavioral impact. Future research will include a randomized clinical trial design where the efficacy of Facotik treatment as well as CoPs treatment in adults is compared to CBIT (2015–2020). Follow-up data and the effect of the therapy on quality of life for all the participants of the present study are still pending. Finally, the Facotik therapy manual will be published as

a workbook for therapists and specialized training will be offered to clinicians to facilitate knowledge transfer.

aUThOr cOnTriBUTiOns

JL created a new therapy for children with tics (Facotik). She oversaw the project (e.g., method, ethics, supervision) and coordinated the writing of the article with a focus on the results analysis and the discussion. KO is the author of the conceptual model that led to the new therapy for children presented in this article. He is the principal researcher on the grant that supported this study. He revised the text and helped with the data analysis. GJ-N contributed to the writing of the manuscript, especially the introduction and the review of the literature. PV contributed to the writing and the text formatting and was in charge of the statistical analysis. ML revised the manuscript and was on the funding grant that supported this study. His research focus is on psychophysiological data and on event-related potentials [see other article in the same topic: Morand-Beaulieu et al. (62)].

acKnOWleDgMenTs

This research was supported by a grant from the “Fonds de la Recherche en Santé du Québec (FRSQ); Regroupement multidis-ciplinaire de la recherche clinique sur le spectre du trouble obses-sionnel compulsif” (Research group #20573). The authors would like to acknowledge the Obsessive–Compulsive Disorder and Tic Disorder Studies Centre team for their participation with assess-ment and treatment.

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Conflict of Interest Statement: The authors declare that the research was con-ducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The reviewer EJ and handling Editor declared their shared affiliation, and the handling Editor states that the process nevertheless met the standards of a fair and objective review.

Copyright © 2016 Leclerc, O’Connor, J.-Nolin, Valois and Lavoie. This is an open-access article distributed under the terms of the Creative Commons 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 original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.