Premonitory Urges in Patients with Gilles de la Tourette Syndrome: An Italian Translation and a 7-Year Follow-up

Abstract

Objective:

Premonitory sensations or urges (PUs) are described as characteristic sensory phenomena preceding tics, which are often described as unpleasant. They occur in 90% of patients affected by Gilles de la Tourette Syndrome (GTS). They may be localized (around the area of tic) or generalized (covering a wide area of the body). The PUs can be measured by the Premonitory Urge for Tics Scale (PUTS). In this study we translated the PUTS scale into Italian and then assessed children and adolescents/young people (CYP) with GTS using the scale.

Methods:

GTS patients were assessed at the initial interview and after 7 years to evaluate the PUs, and the correlations of the PUTS scores with tic severity, severity of comorbid disorders (obsessive–compulsive disorder [OCD], attention-deficit/hyperactivity disorder [ADHD]), and a variety of coexisting psychopathologies.

Results:

A total of 95 patients were studied. We successfully translated the PUTS into Italian, and our results indicated that our translated version had good psychometric properties. Results demonstrated that the CYP had PUs at both interviews, but that older CYP were more consistent in reporting PUs than younger CYP (i.e., PUTS scores increased with age). We found no correlations between PUTS score and tic severity at either interview. We found a statistical significant correlation between PUTS score and obsessive–compulsive symptoms (OCS) at both interviews; Moreover both the PUTS and Children's Yale-Brown Obsessive Compulsive Scale (CY-BOCS) scores increased significantly, whereas the Yale Global Tic Severity Rating Scale (YGTSS) score decreased significantly. We found no relationships between PUTS scores and anxiety, depression, ADHD, and externalizing/internalizing behavioral scores.

Conclusions:

Our results suggest the the Italian translation of the PUTS has good psychometric properties. Although both younger (<10 years of age) and older CYP (≤10 years of age) reported PUs, the scores at the initial interview were statistically significantly lower than at follow-up. Moreover, in CYP >10 years of age, the PUs correlated with obsessions and compulsions (CY-BOCS scores).

Introduction

Gilles de la Tourette Syndrome (GTS) is a complex neuropsychiatric disorder characterized by the presence of both chronic motor and one or more vocal/phonic tics (Diagnostic and Statistical Manual of Mental Disorders, 5th ed. [DSM-V]) (American Psychiatric Association 2013). In addition, it is characterized by neuropsychiatric comorbidities (obsessive–compulsive disorder [OCD], attention-deficit/hyperactivity disorder [ADHD]) and coexistent psychopathologies (anxiety, depression, externalizing/internalizing behaviors) in ∼90% of patients, with a prevalence of ∼1% (Robertson 2008). Tics are defined as sudden, repetitive movements or vocalizations (American Psychiatric Association 2013), which typically begin as simple tics, but can be more complex in some cases. In addition to comorbidities and coexistent psychopathologies, premonitory urges (PUs) a term coined by Cohen and Leckman (1992) are a common feature, occurring in ∼90% of adult patients (Kwak et al. 2003) and are often more intrusive or bothersome than the tics themselves (Leckman et al. 1994). PUs are essential to the subjective phenomenology of GTS, and a better understanding of these experiences could lead to improved treatment strategies or response to habit reversal therapy (HRT).

PUs are perceived as unusually “aversive.” They may include feelings of energy, pressure, tension, tightness, itchiness, achiness, discomfort and/or other unpleasant phenomena prior to the onset of the tics. Many patients describe these PUs as “building up” before a tic (or upon attempts to resist the tic); the PUs are temporarily alleviated by the occurrence of the tics. Furthermore, patients have described PUs as causing an urge/sensation to “have to do the tic,” similar to the “need to sneeze or itch” (Kwak et al. 2003). PUs may be somewhat difficult to categorize. They have been referred to as “just-right perceptions” (Leckman et al 1994); “premonitory sensory phenomena (PSP)” (Banaschewski et al 2003); and “sensory tics, sensory experiences, and incompleteness” (Prado et al 2008). Although PUs may occur in younger children and adolescents/young people (CYPs), they are not often associated with tics until later in development, usually after the age of 10 years (Banaschewski et al 2003; Woods et al. 2005; Steinberg et al. 2010), suggesting that the Premonitory Urge for Tics Scale (PUTS) should be used only in CYPs >10 years of age (Steinberg et al. 2010). The age differential in the onset of PUs may merely reflect aspects of cognitive development rather than intrinsic aspects of GTS (Banaschewski et al 2003). Alternatively, they may indicate patients' increasing awareness, rather than the presence, of PUs (Woods et al. 2005).

Similar to the adverse effects of comorbid conditions and coexistent psychopathologies on patients' quality of life (QOL) (Eddy et al. 2011), PUs may be more bothersome than the tics themselves and may cause greater impairment. A follow-up study demonstrated that PUs, tic severity, and a family history of GTS all served as childhood predictors of poorer health-related QOL in late adolescence and adulthood) (Cavanna et al. 2012).

Several attempts have been made to measure these phenomena (Kwak et al. 2003), the University of Sao Paolo Sensory Phenomena Scale (USP-SPS) (Rosario et al. 2009), and the PUTS (Woods et al 2005). Woods et al. designed the PUTS as a patient self-reporting scale. Validated in GTS, the PUTS includes nine items and can measure both sensory and mental phenomena in CYP. In addition, it shows a high internal consistency, which has led to its status as the most widely used international scale of its kind. The USP-SPS has good psychometric properties and has been shown to correlate significantly with the PUTS (Rosario et al 2009). A recent study found that the PUTS also has good psychometric properties, temporal stability, and concordant validity (Reese et al. 2014). Furthermore, data suggest that the PUTS can differentiate between the types of urges associated with simple/complex tics and obsessive–compulsive phenomena (Rajagopal and Cavanna 2014).

Despite several investigations in people with GTS that use the PUTS, no consensus has been reached either about the clinical correlates of the PUTS and PUs with various aspects of GTS, or about which are or are not significantly related. We therefore decided to undertake a study that first translated the PUTS into Italian, and then sought to determine which aspects of GTS and PUs are related.

Study Aims

The present study was conducted with the following several aims in mind.

First, we aimed to establish the psychometric properties of a non-English (Italian) translation of the PUTS. We also aimed to identify any correlations between the PUTS and severity of 1) tics, 2) comorbid OCD), and 3) comorbid ADHD. Third, we aimed to explore possible relationships between PUTS scores and coexistent psychiatric problems, such as anxiety, depression, and externalizing/internalizing behaviors. Finally, we aimed to compare the initial PUTS scores with those measured at the 7 year follow-up, in order to establish possible differences in perception of PUs in the same patients at different ages.

Materials and Methods

Participants

Ninety-five patients (CYPs with GTS) of varying socioeconomic status all of whom were assessed at the time of their initial interviews (mean age 7.3±1.5 years) and again after 7 years (mean age 13.1±3.7 years) and were followed at our neuropsychiatric clinic. All were evaluated by the same child neurologist (R.R.), who has extensive experience in understanding and treating GTS and its comorbid conditions and psychopathologies.

Procedures

The study received approval from the local Ethics Committee. The parents of all CYP gave written informed consent, and the CYP assented. Diagnoses of GTS and other clinical conditions were made, in accordance with Diagnostic and Statistical Manual of Mental Disorders, 4th ed., Text Revision (DSM-IV-TR) criteria, by a child neurologist (R.R.) (American Psychiatric Association 2000).

Translation of the PUTS into Italian (PUTS-I)

Translation of the PUTS into Italian (PUTS-I) was undertaken using a “back-translation” process, as described by Steinberg et al (2010) in detailing their translation of the PUTS into Hebrew (PUTS-H). Thereafter, 50 CYP with GTS and 50 healthy matched controls completed this Italian version of the PUTS.

Onset evaluation

All GTS patients were assessed using a semistructured interview, the National Hospital Interview Schedule for Gilles de la Tourette Syndrome (Robertson and Eapen 1996). The PUs were evaluated using the Italian version of the PUTS. Tic severity scores were obtained using the Yale Global Tic Severity Rating Scale (YGTSS) (Leckman et al. 1989), and the presence of symptoms relating to OCD was assessed using the Children's Yale-Brown Obsessive Compulsive Scale (CY-BOCS) (Scahill et al. 1997). Parents completed the ADHD Rating Scale/DSM-IV Scale (CADS) as well as the Conners scale to provide information about their children's ADHD-related symptoms (Conners 1978).

Follow-up evaluation

The 7 year follow-up evaluations used the same instruments as in the initial interview. In addition, GTS CYP completed the Multidimensional Anxiety Scale for Children (MASC) (March et al. 1997) to assess symptoms of anxiety, and the Child Depression Inventory (CDI) (Kovacs 1988) to assess symptoms of depression. Meanwhile, parents completed the Child Behavior Checklist (CBCL) (Achenson 1991) to assess the presence of externalizing behaviors in their children. All patients were also assessed by a psychologist, using the Wechsler Intelligence Scale for Children, 3rd ed. (WISC-III) (Wechsler 1991), to evaluate their intelligence quotient (IQ) and level of cognitive function.

Measures

We used the following well-known, internationally accepted scales/interviews/schedules to assess all participants.

1. The PUTS, a nine item scale, developed by Woods et al. (2005), to measure PUs in patients with tic or TS. Each item is rated using a four point scale, ranging from 1 to 4 (1, not true to 4, very much true). The total score is the sum of all nine items (range from 9 to 36). Higher scores reflect the presence of PUs.

2. The YGTSS, an 11-item clinician rated interview of motor and phonic tic severity (Leckman et al. 1989). The clinician initially notes the presence of motor and phonic tics based on child and parent report over the past week, as well as making behavioral observations. Following this, the clinician rates the severity of motor and phonic tic on five separate dimensions each: Number, frequency, intensity, complexity, and interference. These scale score rating from 0 to 50. The YGTSS also includes a separate impairment rating scale also rated from 0 to 50. Higher scores indicate the presence of severe symptoms and impairment.

3. The CY-BOCS, which is the most used and reproducible instrument to assess the severity of obsessive–compulsive symptoms in children (Scahill et al. 1997). The clinician initially notes the presence of obsessions and compulsions based on child and parent report over the past week, as well as making behavioral observations. Following this, the clinician rates the severity of obsessions and compulsions on separate dimensions each: Number, frequency, intensity, resistance, and interference. Three index scores are obtained: Obsession score, Compulsion score, and Total score. The total score evaluates the impairment that obsessive– compulsive symptoms caused to the patient.

4. The CADS, a self- and proxy-rated (parent, teacher) symptom-oriented scale (Conners 1978). The scale discriminates youth with the psychiatric diagnoses of ADHD predominantly inattentive, ADHD predominantly hyperactive-impulsive, and combined ADHD, as opposed typically developing youth. The CADS has been extensively validated, and is an acceptable index of the severity of ADHD. It is designed for youth ages 12–17. Both parent (CADS-P) and self-report (CADS-A) versions were employed in this study.

5. The CBCL, a widely used parent-rated scale assessing the frequency and intensity of behavioral and emotional problems exhibited by the child in the past 6 months (Achenbach 1991). Items are rated on a scale of 0 (not true), 1 (somewhat or sometimes true), or 2 (very true or often true). The CBCL consists of eight syndrome scales (withdrawn, somatic complaints, anxious/depressed, social problems, thought problems, attention problems, delinquent behavior, and aggressive behavior) and two composite scales (externalizing and internalizing problems). The CBCL has excellent psychometric properties and construct validity (Achenbach, 1991).

6. The MASC, a validated and widely used tool which assesses anxiety disorders in child and adolescent patients (March et al. 1997). Items are rated on a scale of 0 (not true), 1 (somewhat or sometimes true), 2 (often true), or 3(very true). The MASC consists of three subscales (Physical, Harm and Social) and a Total score.

7. The CDI, a self-rated symptom oriented instrument (Kovacs 1988). The instrument discriminates children and adolescents with the psychiatric diagnosis of major depressive or dysthymic disorder, as opposed to typically developing youth. It is sensitive to changes in depression over time, and is an acceptable index of the severity of the depressive disorder. The CDI has been extensively validated and is designed for children and adolescents ages 7–17 years.

Entry criteria

We conducted our study by first screening our database of 500 GTS CYP, and then selected for inclusion 95 CYP with GTS who had IQs in the normal range (100±2 SD) (enabling them to complete the PUTS-I), and who had been fully assessed, both initially, and after a follow-up period of 7 years. We excluded patients who could not be fully assessed at the initial evaluation and/or at the 7 year follow-up. Moreover, we excluded all patients who showed evidence of severe neurological or physical impairment.

Statistical analysis

The internal consistency of the PUTS was calculated by Cronbach's α. We compared PUTS, CY-BOCS, YGTSS, and CADS scores at the time of initial interview and again at the 7 year follow-up with the t test for paired samples (for data with normal distribution) or with the Wilcoxon test for paired samples (for data with abnormal distribution). To analyze the correlations between the scores, we used the Pearson test (for data with normal distribution) or the Spearman test (for data with abnormal distribution). We conservatively set significance at p<0.05, because our main hypotheses were unidirectional.

Results

Our demographic and neuropsychological data are summarized in Table 1. As depicted, our study included 95 patients (83 male, 12 female). At the time of the initial interview, these participants were 4–10 years of age (mean 7.3, SD 1.5); at 7 year follow-up, they were 10–16 years of age (mean 13.1, SD 3.7).

Table 1.

Comparison Between Demographic and Neuropsychological Data at the Onset and at Follow-up

	Onset	Follow-up	p/z value
Age	7.3 (1.5)	13.1 (3.7)
PUTS	13.4 (5.5)	24.1 (6.1)	0.000
YGTSS	33.1 (8.2)	26.5 (8.3)	0.000
CY-BOCS	19.1 (7.4)	30 (5.9)	0.006
CADS	33.7 (17.1)	16.9 (9.9)	0.000
CBCL Total		33.4 (23.7)
MASC		42.1 (14.1)
CDI		8.1 (5.8)

Standard deviation in shown in parentheses.

PUTS, Premonitory Urge for Tic Scale; YGTSS, Yale Global Tic Severity Scale; CY-BOCS, Child Yale-Brown Obsessive Compulsive Scale for Children; CADS, Attention-Deficit/Hyperactivity Disorder (ADHD) Rating Scale /Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) Scale; CBCL, Child Behavior Check List; MASC: Multidimensional Anxiety Scale for Children; CDI: Child Depression Inventory.

Our sample at the time of the initial interview had the following mean scores: PUTS 13.45 (SD 1.5), YGTSS 33.1 (8.2), CY-BOCS 19.1 (7.4), and CADS 33.7 (17.1). At 7 year follow-up, the scores were as follows: PUTS 24.1 (6.1), YGTSS 26.5 (8.3), CY-BOCS 30 (5.9), and CADS 16.9 (9.9).

The PUTS and CY-BOCS scores showed statistically significant increases with time/patient age, whereas the YGTSS scores showed a statistically significant decrease over the years (Table 1).

Internal consistency of PUTS-I

Cronbach's α was calculated to determine the PUTS-I internal consistency. Calculating the internal consistency in the two age groups revealed a higher result for patients >10 years of age (α=0.85) than for younger patients (α=0.70).

Our comparison between the scores of the various schedules at the time of the initial interview and again after 7 years showed statistically significant differences (measured with p or z<0.00) on all scales.

We examined the correlation between PUTS scores and tic severity as measured by the YGTSS; no statistically significant values, either at the time of the initial interview or after 7 years, were reported (Table 2). The correlation between PUTS scores and obsessive–compulsive symptoms (OCS), as measured by the CY-BOCS, revealed a positive significant correlation between PUTS scores and obsessionality (as measured by CY-BOCS), both at the time of the initial interview and at the 7 year follow-up (Table 2).

Table 2.

Correlation Among PUTS, CY-BOCS and YGTSS Scores

		YGTSS onset	CY-BOCS onset	YGTSS follow-up	CY-BOCS follow-up	YGTSS Var %	CY-BOCS Var%
PUTS onset	Correlation coefficient Rho Spearman	−0.156	0.037^*
	Sig. (2 code)	0.131	0.720
PUTS follow-up	Correlation coefficient Rho Spearman			0.158	0.088^*
	Sig. (2 code)			0.127	0.394
PUTS var%	Correlation coefficient Rho Spearman					−0.21	0.003^*
	Sig. (2 code)					0.837	0.978

Boldface indicates statistically significant

PUTS, Premonitory Urge for Tic Scale; YGTSS, Yale Global Tic Severity Scale; CY-BOCS: Child Yale-Brown Obsessive Compulsive Scale for Children; Var, variance.

Furthermore, we explored the relationships among PUTS, MASC, CDI, CADS and CBCL scores. No significant correlations were found (Table 3).

Table 3.

Correlation Among PUTS and CADS, MASC, CDI, and CBCL

		CADS onset	CADS follow-up	MASC follow-up	CDI follow-up	CBCL follow-up
PUTS onset	Correlation coefficient Rho Spearman	−0.156
	Sig. (2 code)	0.121
PUTS follow-up	Correlation coefficient Rho Spearman		0.162	0.158	0.188	0.170
	Sig. (2 code)		0.130	0.127	0.194	0.141

PUTS, Premonitory Urge for Tic Scale; CADS, Attention-Deficit/Hyperactivity Disorder (ADHD) Rating Scale /Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) Scale; MASC, Multidimensional Anxiety Scale for Children; CDI, Child Depression Inventory; CBCL, Child Behavior Check List.

Discussion

Our review of existing literature suggested that despite several investigations in GTS patients who have used the PUTS, no absolute consensus has been reached on the relationship between various aspects of GTS and PUs. Consequently, we undertook this study first to translate the PUTS into Italian, and then to determine which aspects of GTS and PUs may be related.

In our study, we first reported the good psychometric properties of the first Italian translation of the PUTS (PUTS-I), providing a useful measure of PUs in Italian CYPs with GTS. We were also able to show that PUs help to characterize both younger and older CYPs with GTS. However, the reliability (defined as the capacity of the tool to produce stable results) of the PUTS-I was higher (better) in older children, suggesting that although both age groups experience PUs, older children are more consistent in reporting them. Our results, therefore, confirm previous findings (Woods et al 2005). We have, therefore, shown that the PUTS-I plays an important role evaluating CYPs with GTS and tic disorders, that the psychometric properties of the scale are good, and that our findings are consistent with those of previous studies (e.g. Woods et al 2005). Whereas our study focused on PUTS in children, Crossley et al (2014) used the PUTS successfully in 102 GTS adults, suggesting that the scale is applicable across patient lifespans.

Second, our study sought to identify any significant correlations between PUTS scores and tic severity. We found, in our sample, no such correlations using YGTSS scores, either at the time of the initial interview or at 7 year follow-up (Table 2). No correlations were found either with motor/phonic scores or total score. Our results are similar to those of other investigators who found no relationship between tic severity and the PUTS in either CYP (Steinberg et al. 2010) or in patients 10–41 years of age (Sutherland Owens et al. 2011). However, our findings are in contrast to those of Woods et al. (2005), Steinberg et al. (2013), and Reese et al. (2014), all of whom examined CYP, with two of these studies using the YGTSS. They also contrast with the findings of Cavanna et al. (2012) and Crossley and Cavanna (2013), who used the YGTSS and the Motor Tic, and Compulsions, Vocal Tic Evaluation Survey (MOVES) self-rated scales; and Crossley et al. (2014), who used the YGTSS alone. These latter studies were undertaken in adults with GTS, and all demonstrated significant correlations with either tic severity or tic-related impairments. In addition, Ganos et al (2012) reported that PUTS scores correlated with the interference section of the YGTSS. However, we feel that the conflicting evidence suggests the need for further research.

Our study next investigated the relationships between PUTS scores and the severity ratings of a typical GTS comorbidity, OCD. In this regard, we found a positive significant correlation between PUTS scores and obsessionality (CY-BOCS), both at the time of the initial interview and at 7 year follow-up (more so at follow-up). Interestingly, we also found that CY-BOCS scores increased significantly with age. Our results are in agreement with those of Woods et al. (2005), Steinberg et al. (2010), and Reese et al (2014), all of whom reported significant correlations between PUTS scores and obsessive–compulsive behavior/disorder (OCB/D) measures in CYP. Our results also align with those of Crossley and Cavanna (2013) who, while using other measures, found relationships between sensory phenomena in GTS and obsessionality in adults with GTS. Although Kwak et al. (2003) used an in-house scale, they, too, reported a correlation between sensory phenomena (also known as “just-right phenomena”) and comorbid OCD. Sutherland Owens et al. (2011) examined 18 GTS patients (ages 10–41 years) and reported no correlations between PUTS (and USP-SPS) scores and OCB/D measures; low participant numbers and group heterogeneity may account for these negative findings. The aforementioned results (majority concordant) indicate that the PUTS and other scales are tapping well into OCB/D aspects of GTS, which have been demonstrated for years to be an integral part of the syndrome, even in mildly affected patients in the community (Robertson 2008). In addition, there is agreement in the literature that GTS and OCB/D are genetically related (Davis et al. 2013).

Our study revealed no significant correlations between PUTS and ADHD (CADS scale) scores, either at the time of the initial interview or at 7 year follow-up (Tables 1 and 2). Our results are, once again, in agreement with those of Woods et al (2005), Steinberg et al (2010), and Reese et al (2014), all of whom also found no correlations between PUTS scores and ADHD measures. It is important to note that the aforementioned studies were performed in CYP. Crossley and Cavanna (2013), on the other hand, studied GTS adults and did find a correlation between ADHD self-report scale and PUTS scores. The fact that the three studies in CYP (our present study, Woods et al. 2005, and Steinberg et al. 2010) all obtained consistent results (no correlations between PUTS scores and ADHD measures) is important, because the PUTS instrument was designed specifically for use in CYP. Therefore, age may well be a central influence. The partial agreements about relationships among GTS and ADHD and PUTS are not surprising, given the inconsistent long-term findings concerning these relationships (Robertson 2006).

Our study next sought to detect any correlations between PUTS scores and the various coexistent psychopathologies associated with GTS, such as anxiety, depression, and externalizing/internalizing behaviors. We found that there were none (Tables 1 and 3). Our results in the context of anxiety are in agreement with those of Steinberg et al. (2010), who also reported no correlation between PUTS scores and anxiety measures in CYP. On the other hand, they did show a significant relationship between PUTS scores and depression. Our results stand in contrast to those of Crossley and Cavanna (2013), who reported a positive correlation between anxiety and PUTS scores in GTS adults. Woods et al. (2005), meanwhile, did report a relationship between anxiety and depression (from CBCL subscales) and PUTS in CYP. It is important to note that both Steinberg et al. (2010) and the investigators in the present study focused on CYP and used a specifically designed child inventory (CDI) for measuring depression in the cohorts. Therefore, our results are more likely to reflect the correct relationships. The relationship between GTS and depression is complicated: Although there are suggestions of a relationship with PUs, there is no genetic relationship; however, depression is related to both tic severity and duration, as well as to echo- and copro-phenomena, OCD, ADHD, childhood conduct disorder (CD), self-injurious behavious, aggression, sleep disturbances, and (only possibly) ADHD (Robertson 2006).

It must be noted that, in our sample, the YGTSS score significantly decreased with age (at the time of initial interview and after 7 years). This is not surprising, given the documentation of the GTS course that includes a reduction in tics with age. In addition, 32 out of our 95 patients were being treated with medication at the time of the initial interview, and 69 of the 95 were being treated at the 7 year follow-up. The observed reduction in tic severity may well have been a response to this therapy. In contrast, we found that patients' obsessional symptoms (measured by CY-BOCS) significantly increased with age, which is consistent with other reports stating that the most severe OCD occurs after the most severe tics (Robertson 2008).

Because PUs occur, by definition, before tics, it comes as no surprise that studies have addressed neurophysiological phenomena prior to tics. In this regard, the Bereitschaftspotential in GTS was first studied by Obeso et al. (1981), who described simple tics in GTS as not prefaced by a normal premovement electroencephalographic (EEG) potential (which does occur with voluntary movements). This, in turn, suggested that spontaneous tics were not generated in the same manner as normal voluntary movements. These results were subsequently replicated by Karp et al. (1996), who successfully studied five GTS patients, and again, demonstrated no premotor Bereitschaftspotential before tics. However, premotor negativity was present with spontaneous tics in two patients, and resembled the NS segment (the earliest part of the premotor potential) seen with self-paced voluntary movements. Finally, with regard to PUs, Duggal and Nizamie (2002) investigated the Bereitschaftspotential and PUs in three GTS patients. Their results—positive PUs and the absence of potentials—led them to speculate that tics are not entirely involuntary, but rather “quasivolitional” in nature. Duggal and Nizamie also suggested that the Bereitschaftspotential represents a neurophysiological marker of PUs in GTS (Duggal and Nizamie [2002]).

In a similar vein, Sutherland Owens et al. (2011) examined PUs and sensorimotor gating deficits using the PUTS, the USP-SPS, the Sensory Gating Inventory (SGI), the Structured Interview for Assessing Perceptual Anomalies (SIAPA), and various scales measuring symptom severity, both in GTS patients and in matched controls. Their results showed that, in GTS subjects, PUTS and USP-SPS scores correlated significantly with each other, but not with SGI or SIAPA scores. Neither PUs nor sensory gating scales correlated with symptom severity. The SGI was elevated in GTS subjects, but SIAPA scores were not. Consequently, Sutherland Owens et al. (2011) concluded that SGI scores may be valuable for studying these phenomena in GTS.

Recent literature has suggested that tics may be negatively reinforced by the removal of PUs (Capriotti et al. 2014). In the same context, Ganos et al. (2012) studied 15 adult GTS patients using the PUTS; despite the fact that all patients reported PUs preceding tics, there was no correlation between PUTS scores and either Rush score-based inhibition potency or pure motor tic inhibition potency. PUTS scores did correlate with the interference subscale of the YGTSS. Ganos et al., therefore, suggested that urges and tic inhibition are not directly related. They further posited that at least two distinct neurophysiological systems of urge/tic generation and tic control appear to exist in adults with GTS (Ganos et al. 2012).²⁷

However, it must be emphasized that the ultimate aim for clinicians dealing with GTS is the reduction of patients' distress and symptom severity and the improvement of their QOL. These goals may be attained through psychoeducation and reassurance, as well as a regimen of medication over many years. Today, however, behavioural methods are not only considered in vogue, they have also proven highly successful, with examples including habit reversal training exposure and response prevention and comprehensive behavioral intervention for tics (Verdellen et al. 2011). All of these are, to date, considered somewhat dependent on the perception of PUs.

Limitations

First, ours is a tertiary expert clinic; therefore, our results may not be generalized to all individuals with GTS. In our study, we did not take into account the effect of medications on the PUs, which may be a fruitful area of exploration in the future. In addition, we used some self-report scales; however,—because we also used clinician-/parent-rated schedules—this probably militates in favor of our findings, given the large quantity of available literature on the CDI and the MASC in CYP. Our study did include a 7 year follow-up component, but we would have liked this to be a longer period. Finally, we did not include gender as a variable; doing so might have yielded additional interesting data.

Conclusions and Suggestions for Future Research

In our study, we reported the good psychometric properties of the PUTS-I, providing a useful measure of PUs in CYP with GTS. PUs are essential to the subjective phenomenology of TS, and a better understanding of these experiences could lead to improved treatment strategies or response to HRT in CYP.

We tentatively suggest that the instrument may also be useful in adults, as has been shown with the original (English) version of the scale. However, this suggestion is debatable, as the original designer of the PUTS felt very strongly that it should only be used in CYP.

We found no correlations between PUTS scores and tic severity, either at the time of initial interview or at 7 year follow-up. This conclusion was in agreement with two other studies, but in contrast to eight that reported correlations between PUs/PUTS and tic severity/impairment. Age may well have accounted for some of these differences, as may have the “translation factors,” but as tics are the main symptom of GTS, the conflicting results suggest that more studies must be undertaken.

Clinical Significance

Clinically, we suggest that family history (GTS, tics, OCB/OCD) be included in the assessment and analyses of future studies. We suggest that in the future, longitudinal studies using the PUTS be conducted, and that they simultaneously use both neurophysiological and neuroimaging tools (e.g., functional MRI and Bereitschaftspotential). In doing so, the GTS community may well find a neurophysiological marker (of PUs) and/or endophenotypes in GTS. We also suggest investigating further GTS sensorimotor gating deficits using the SGI, and possibly the SIAPA, which may further the search for endophenotypes and phenomena associated with GTS.

Acknowledgement

Dr. Robertson thanks Tourettes Action (U.K.), The USA Tourette Syndrome Association, and the European Society for the Study of Tourette Syndrome (ESSTS) (and COST Action) for their continuing support.

Disclosures

No competing financial interests exist.

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