Premonitory Urge in Patients with Tics and Functional Tic‐like Behaviors

Abstract

Background

Premonitory urges (PU) are well described in primary tics, but their frequency and intensity in functional tic‐like behaviors (FTLB) are unclear.

Objective

To study the experience of PU in patients with FTLB.

Methods

We compared the results of the premonitory urge for tics scale (PUTS) in adults with tics and FTLB in the University of Calgary Adult Tic Registry.

Results

We included 83 patients with tics and 40 with FTLB. When comparing patients with tics, FTLB with tics and FTLB only, we did not detect significant differences either in the total PUTS score (P = 0.39), or in any of the individual PUTS item sub‐scores (P values ranging between 0.11 and 0.99).

Conclusions

Patients with FTLB report PU at similar frequency and intensity to patients with tics. This finding confirms that PU are not a useful feature to discriminate FTLB from tics.

Premonitory urges (PU) are unpleasant sensations that often precipitate the occurrence of tics. ¹ , ² They are described by patients as tension, pain, itchiness, pressure, “not just right feeling”, incompleteness, and building up of energy. ³ PU are usually localized in the body region where tics emerge. ³ , ⁴ The neurobiological substrates of PU include the cingulate cortex, ⁵ insula, ⁶ , ⁷ supplementary motor area, ⁸ , ⁹ and other regions of the brain. ¹⁰

Case series describing patients with functional tic like behaviors (FTLB) before the coronavirus disease 2019 (COVID‐19) pandemic suggested that patients with FTLB differ from those with tics with respect to several clinical characteristics, including adult onset, ¹¹ , ¹² , ¹³ , ¹⁴ lack of family history of tics, ¹¹ inability to suppress the pathological behaviors, ¹¹ lack of the typical rostrocaudal tic distribution, ¹¹ predominance of complex vocalizations and movements, co‐existence of other functional neurological symptoms, and a lack of PU. ¹¹ , ¹²

Since the onset of the COVID‐19 pandemic, there has been an increase in the incidence of FTLB which, unlike previously described FTLB, appear to be strongly socially influenced, ¹⁵ , ¹⁶ , ¹⁷ and include a wider range of behavioral manifestations. ¹⁷ , ¹⁸ , ¹⁹ , ²⁰ , ²¹ , ²² , ²³ , ²⁴ In our own clinical experiences with patients with FTLB in the pandemic era, we found that they commonly described premonitory sensations or urges in association with their behaviors. ¹⁸

The aim of this study was to compare frequency, intensity, and other characteristics of PU, as detected using the premonitory urge for tics scale (PUTS), between patients with tics only, patients with FTLB only, and patients with both tics and FTLB currently enrolled in the Adult Tic Registry, a prospective cohort study at the University of Calgary.

Methods

This study received ethical approval from the Conjoint Health Research Ethics Board of the University of Calgary (project ID REB20‐1643). We enrolled adult patients who were seen at the Movement Disorder Clinic at the Foothills Medical Center, Alberta Health Services and signed an informed consent. Patients were referred to the clinic by a primary care physician or other healthcare practitioner. During the initial visit, a diagnosis of a tic disorder and/or FTLB was made. All patients included in this study completed the PUTS, the most widespread self‐rated questionnaire for PU in patients with tics. ²⁵ This instrument allows a quantitative assessment of PU in adults, based on several domains that include diverse sensory experiences preceding tics, (eg, itchiness, pressure, tension, “just right” feeling, lack of completion, and overload of energy). In addition, the scale includes questions about the frequency of PU, the relief after tic performance, and ability to suppress tics. Each item is rated on a scale from 1 (not at all) to 4 (very much) and the final score ranges from 9 to 36.

All statistical analyses were conducted in Stata v16 (StataCorp, College Station, TX). We compared age, age at onset of symptoms, each item of the PUTS as well as the total PUTS score between patients with tics, and FLTB and complemented this analysis with the comparison of the individual PUTS items and the total PUTS score between patients with FTLBs and a previous history of tics and patients with FTLB only. The primary statistical method used to compare means between the groups was a one‐way analysis of variance. To compare sex and gender identity distribution, we used χ² test. As there was no group effect for any of the comparisons, we did not conduct any post hoc analysis.

Results

In this analysis, we included 83 patients with tics, 26 patients with FTLB only, and 14 with FTLB and previous history of tics. When comparing all patients with FTLB (n = 40) with patients with tics (n = 83) regarding demographic characteristics, FTLB group was characterized by later age of onset (P < 0.001), younger age at clinical assessment (P < 0.001), female predominance (P < 0.001), higher total tic severity as measured with the Yale Global Tic Severity Scale Total Tic Score (P < 0.001), and higher prevalence of gender diverse individuals (P = 0.009) in comparison to adults with tics (Table 1). On the contrary, there were no significant differences in the final PUTS score, or in any of the individual PUTS items between the groups, including patient with and without prior history of tics (Tables 1 and 2). Patients with the FTLB and prior history of tics had higher total PUTS score and individual item subscores than patients in the other two groups, although these differences did not reach statistical significance.

TABLE 1.

Comparison between patients with tics and functional tic‐like behaviors

Variable	All (n = 123)	Patients with tics (n = 83)	Patients with functional tic‐like behaviors (n = 40)	P (OR)
Sex (male, %)	57 (46.3%)	53 (63.9%)	4 (10%)	OR = 9.4 (3.54–24.8), P < 0.0001
Male	54	52	2	OR = 0.03 (0.007–0.14), P < 0.0001
Female	61	30	31	OR = 6.1 (2.6–14.5), P < 0.0001
Gender minority	8	1	7	OR = 17.4 (2.06–146.9), P = 0.009
Age (mean ± SD)	29.3 ± 13.96	33.4 ± 15.2	20.7 ± 3.24	P < 0.0001
Age of symptoms onset (mean ± SD)	12.47 ± 7.17	9.98 ± 6.74	16.8 ± 5.74	P < 0.0001
Childhood onset (n, %)	92 (74.8%)	73 (88.0%)	19 (47.5%)	OR = 0.06 (0.018–0.2), P < 0.0001
YGTSS‐TTS (mean ± SD)	24.11 ± 9.64	20.45 ± 7.65	31.7 ± 8.94	P < 0.0001
PUTS total (mean ± SD)	26.2 ± 7.02	26.34 ± 6.8	25.9 ± 7.53	P = 0.75
PUTS itchy (mean ± SD)	1.95 ± 1.07	1.91 ± 1.07	2.03 ± 1.1	P = 0.59
PUTS pressure (mean ± SD)	2.75 ± 1.11	2.74 ± 1.07	2.76 ± 1.2	P = 0.92
PUTS tense (mean ± SD)	3.04 ± 1.07	3.05 ± 1.07	3.03 ± 1.08	P = 0.90
PUTS just right (mean ± SD)	2.74 ± 1.13	2.74 ± 1.19	2.74 ± 1.03	P = 0.98
PUTS not complete (mean ± SD)	2.44 ± 1.15	2.55 ± 1.23	2.21 ± 0.96	P = 0.14
PUTS energy (mean ± SD)	2.91 ± 1.12	2.88 ± 1.14	2.97 ± 1.1	P = 0.69
PUTS time (mean ± SD)	2.85 ± 0.98	2.87 ± 0.99	2.82 ± 0.98	P = 0.78
PUTS frequency (mean ± SD)	2.43 ± 0.97	2.49 ± 0.97	2.29 ± 0.98	P = 0.29
PUTS relief (mean ± SD)	2.48 ± 0.93	2.44 ± 0.91	2.55 ± 0.98	P = 0.55
PUTS suppression (mean ± SD)	2.63 ± 0.96	2.69 ± 0.92	2.5 ± 1.03	P = 0.32

Abbreviations: OR, odds ratio; SD standard deviation; YGTSS‐TTS, the Yale Global Tic Severity Scale‐Total Tic Score PUTS, Premonitory Urge for Tics Scale.

TABLE 2.

ANOVA comparison between patients with tics, FTB without history of tics in the childhood, FTB with tics in the childhood

Variable	All (n = 123)	Patients with tics (n = 83)	Patients with functional tic‐like behaviors without history of tics in childhood (n = 26)	Patients with functional tic‐like behaviors with history of tics in childhood (n = 14)	P
PUTS total (mean ± SD)	26.2 ± 7.02	26.34 ± 6.8	24.65 ± 7.6	27.8 ± 7.27	0.39
PUTS itchy (mean ± SD)	1.95 ± 1.07	1.91 ± 1.07	1.74 ± 0.92	2.47 ± 1.25	0.11
PUTS pressure (mean ± SD)	2.75 ± 1.11	2.74 ± 1.07	2.61 ± 1.2	3 ± 1.2	0.57
PUTS tense (mean ± SD)	3.04 ± 1.07	3.05 ± 1.07	3.04 ± 1.1	3 ± 1.1	0.99
PUTS just right	2.74 ± 1.13	2.74 ± 1.19	2.61 ± 1.03	2.93 ± 1.03	0.69
PUTS not complete (mean ± SD)	2.44 ± 1.15	2.55 ± 1.23	2.22 ± 1.09	2.2 ± 0.77	0.33
PUTS energy (mean ± SD)	2.91 ± 1.12	2.88 ± 1.14	2.83 ± 1.07	3.2 ± 1.15	0.56
PUTS time (mean ± SD)	2.85 ± 0.98	2.87 ± 0.99	2.7 ± 1.02	3 ± 0.93	0.63
PUTS frequency (mean ± SD)	2.43 ± 0.97	2.49 ± 0.97	2.17 ± 1.07	2.47 ± 0.83	0.38
PUTS relief (mean ± SD)	2.48 ± 0.93	2.44 ± 0.91	2.35 ± 0.88	2.87 ± 1.06	0.20
PUTS suppression (mean ± SD)	2.63 ± 0.96	2.69 ± 0.92	2.39 ± 1.08	2.67 ± 0.98	0.43

Abbreviations: ANOVA, analysis of variance; FTB, functional tic‐like behaviors; PUTS, Premonitory Urge for Tics Scale; SD, standard deviation.

Discussion

We present the results of the first study comparing PU in patients with tics, FTLB with prior history of tics, and FTLB only, using the PUTS. Apart from the previously reported demographic differences between these groups, we failed to determine any differences in PUTS scores.

Some previous studies have demonstrated that patients with FTLB either do not feel any PU preceding their symptoms or their PU are very uncommon. ¹¹ , ¹⁴ , ¹⁷ , ²¹ , ²⁶ , ²⁷ , ²⁸ , ²⁹ , ³⁰ Some observational studies of patients with FTLB did not report about PU, ¹⁸ , ³¹ , ³² whereas other authors concluded that this is not a relevant distinguishing factor between tics and FTLB. ²⁰ , ²³ , ²⁷ , ³³ , ³⁴ In the recently published study summarizing findings from the international database of FTLB, ³⁵ authors gathered information from 10 tertiary centers specialized in tic disorders from Canada, France, United Kingdom, Germany, Australia, Italy, and Hungary. They analyzed a variety of clinical features of FTLB including repertoire of movements and vocalizations, sex and age distribution, the age of onset, time of symptom progression, the presence of self‐injurious behaviors, rostrocaudal distribution, and the presence of PU, suppressibility, distractibility, and suggestibility as well as the profile of comorbidities, treatment with anti‐tic medications, and outcomes. Fewer than half (137/294, 47%) of the patients reported PU indicating that these are less frequently reported by patients with FTLB than by individuals with tics. Some previous studies have also shown similar results. Demartini et al ¹¹ published a case series of 11 patients with FTLB, only three of whom (27%) had PU. Similarly, in a small case series from Hungary by Nagy et al ²⁹ including five cases, all patients denied having PU. Likewise, Hull and Parnes ²⁸ underline the lack of PU as a feature distinguishing FTLB from tics.

In contrast to these reports, more studies have shown that PU is also frequently found in FTLB. In a small case series, Janik et al ¹² described five cases of FTLB in a cohort of 268 patients with tic disorders, reporting PU in three of these five patients, but without clarifying whether PU referred to FTLB or to tics in these patients. Similar overlap between PU secondary to tics and/or FTLB is also mentioned in other studies. ²⁰ , ³⁶ The group from the Hannover Medical School ²¹ provided a more detailed analysis of PU from a cohort of 32 FTLB patients. The vast majority of patients experienced PU (84.4%) and, similarly to patients with tics, it was often located in the body part where FTLB occurred (n = 14, 43.8%). Fifteen patients (46.9%) gave PU descriptions such as having “a stone collar around neck,” “a dam inside the stomach,” or “trembling inside the head,” which the authors denominate as “unusual.” Buts et al ²⁷ published results of the retrospective chart review of 34 consecutive pediatric FTLB patients, and the rate of patients reporting about PU was very similar (77% for tics group vs. 62% for FTLB group). In another study by Paulus et al, ²³ 13 patients with FTLB were compared with 13 matched patients with tics. Again, no differences in self‐reported frequency of PU between patients with FTLB and tics were found. A case series from Denmark ³⁴ reporting on 17 teenagers with FTLB demonstrated that 15/17 (88.2%) of the patients had PU. Finally, Pringsheim et al ²⁰ mention that typical features of tics, such as the report of subsequent relief of PU after the tic, suggestibility, and distractibility, can be present in association with both tics and FTLB and are less helpful in distinguishing these two phenomena.

Overall, the previous evidence regarding the presence of PU in FTLB is conflicting, limited by different sample size across studies, lack of comparison between FTLB, and tic groups, inclusion of patients with both disorders in some of these studies, and lack of psychometric assessment of PU. As a result, lack of PU or its atypical character was not included in the recently published European Society for the Study of Tourette Syndrome 2022 criteria for clinical diagnosis of FTLB. ³⁷

Although our findings indicate that the lack of PU cannot serve as a single supporting factor for FTLB diagnosis, these preliminary results should ideally be corroborated by the investigation of a larger, multicentric population because results of the international FTLB database ³⁵ have shown that there are significant differences in characteristics of patients with FTLB enrolled in diverse centers. It would also be crucial to conduct a more extensive comparison between patients without a history of tics in childhood and those with such history. One can speculate that being exposed to PU related to tics could be a sensitizing factor that makes patients more aware of PU related to FTLB. Cavanna et al ³⁸ observed that patients with FTLB and history of tics in childhood reported PU related to FTLB more frequently than patients with FTLB without history of tics. This is in line with the previously observed association between aberrant interoceptive awareness and perception of PU in patients with tics, indicating that interoception might be involved in self‐reported PU. ³⁹ Whether patients with FTLB share a similar aberrant interoception with patients with tics remains unexplored to date. Another relevant topic for future research is the development of new analytic measures of PU that would allow a better self‐report of their presence and intensity on a tic‐by‐tic basis. This new tool should incorporate psycho‐physical measurements such as previously developed urge‐monitors. ⁴⁰ , ⁴¹

Finally, it is worth mentioning that in the majority of previous studies only open questions about the presence of PU were posed, whereas this is the first study in which a patient‐rated measure (PUTS) was used. It is, therefore, logical to speculate that the results of these two types of studies may differ. Similarly, studies trying to measure other subjective symptoms in psychogenic non‐epileptic seizures, another type of functional neurological disorder, have demonstrated different results for open questions, and patient‐based surveys. For example, reports of altered consciousness were found to be relatively rare during clinical interviews, ⁴² but considerably more frequent when using a patient‐rated measure. ⁴³

In conclusion, we did not detect differences in frequency and intensity between FTLB‐related PU in patients with FTLB and tic‐related PU in those with primary tic disorders. Therefore, we propose that PU are not a useful feature when discriminating FTLB from tics.

Author Roles

(1) Research project: A. Conception, B. Organization, C. Execution; (2) Statistical Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript: A. Writing of the First Draft, B. Review and Critique.

N.S.Z.: 1B, 1C, 2B, 3A, 3B.

J.F.: 1B, 1C.

D.M.: 1A, 2A, 2C, 3B.

T.P.: 1A, 1B, 1C, 2A, 2B, 2C, 3B.

Disclosures

Ethical Compliance Statement: This study received ethical approval from the Conjoint Health Research Ethics Board of the University of Calgary (project ID REB20‐1643). Written informed consent was obtained from all the participants. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this work is consistent with those guidelines.

Funding Sources and Conflicts of Interest: N.S.Z. received salary support to perform this research by the Clinical Research Training Scholarship in Tourette syndrome funded by the American Academy of Neurology, Tourette Association of America, and American Brain Foundation. The Calgary Adult Tic Registry was set up through funding from the Owerko Centre of Alberta Children's Hospital Research Institute.

Financial Disclosures for the Previous 12 Months: T.P. has received research funding from the Canadian Institutes of Health Research and the University of Calgary's Azrieli Accelerator. D.M. received personal compensation for consultancies for Roche; he serves in the Advisory Board of Sunovion and Merz Pharmaceuticals; he received honoraria from Dystonia Medical Research Foundation Canada, American Academy of Neurology, Movement Disorders Society, royalties from Springer‐Verlag, and Oxford University Press. He also received grant research support from Dystonia Coalition (National Institutes of Health), Weston Foundation, Owerko Foundation, Canadian Institutes of Health Research, Dystonia Medical Research Foundation Canada, and the Michael P. Smith Family. J.F. has no financial disclosures. N.S.Z. received Clinical Research Training Scholarship in Tourette syndrome funded by the American Academy of Neurology, Tourette Association of America, and American Brain Foundation.