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Transcript
INTERNATIONAL JOURNAL OF
CLINICAL NEUROSCIENCES
MENTAL HEALTH
AND
REVIEW
Repetitive behaviors in Tourette Syndrome and
Obsessive-Compulsive Disorder
Maria Miguel Brenha1, Carla Rio2, Filipa Sá-Carneiro3,4, and João Massano4-6
Abstract
Tourette Syndrome (TS) is a neuropsychiatric disorder caracterized by tics that are frequently associated with obsessive-compulsive symptoms (OCS), estimated to be present in 28-63% of patients, though not always sufficient for the
diagnosis of an Obsessive-Compulsive Disorder (OCD). Epidemiological, phenomenological and family-genetic studies
support an interrelationship between tic disorders and OCD. The repetitive behaviors present in either TS and OCD
—tics and compulsions—have been associated with dysfunctional cortico-striato-thalamo-cortical circuits, which is
consistent with the hypothesis that OCS and tics might be part of the same spectrum. According to that, OCD with
tics assumes an intermediate position between OCD without tics and TS, sharing clinical features with both entities.
On the other hand, many studies have reported that tic-related OCD presents specific clinical, neurobiological, genetic
and treatment response patterns and TS can be differentiated from OCD subgroups according to obsessive-compulsive
symptomatology, presence of sensory phenomena and treatment response. Thus, the phenomenological distinction of
repetitive behaviors in patients with TS is important to consider, since the treatment of tics and OCS differs.
Keywords: Tourette Syndrome, Obsessive-Compulsive Disorder, Repetitive Behaviors, Tic, Compulsion, Treatment.
2
Department of Psychiatry, Hospital de Magalhães Lemos, Porto, Portugal
Psychiatry Department, Centro Hospitalar Tâmega e Sousa, Penafiel, Portugal
Citation: Brenha et al. Repetitive behaviors in Tourette syndrome and
Obsessive-Compulsive Disorder. IJCNMH 2015; 2:5
Department of Child and Adolescent Psychiatry, Centro Hospitalar do Porto,
Portugal
Received: 04 Dec 2014; Accepted: 09 Oct 2015; Published: 14 Oct 2015
1
3
Department of Clinical Neurosciences and Mental Health, Faculty of Medicine University of Porto, Portugal
4
Department of Neurology Hospital Pedro Hispano/ULS Matosinhos,
Matosinhos, Portugal
5
Center for Neurosciences, CUF Porto, Porto, Portugal
6
Correspondence: Maria Miguel Brenha
Hospital de Magalhães Lemos, EPE. Rua Professor Álvaro Rodrigues
4149-003 Porto, Portugal
Email address: [email protected]
Open Access Publication
Available at http://ijcnmh.arc-publishing.org
© 2015 Brenha et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,
provided the original work is properly cited.
2
Introduction
Tourette Syndrome (TS) is a neuropsychiatric disorder
characterized by the presence of multiple motor tics and
one or more vocal tics, not necessarily concurrently, for
a period of more than one year and onset before the age
of 18 years. TS is relatively common, affecting around 1%
of school-aged children [1–3]. Males suffer from TS more
frequently than females (3/4:1) [4] and a multifactorial etiology has been proposed, in which immunological, environmental and genetic factors interact to establish vulnerability. TS has a polygenic inheritance, with the SLITRK1
gene in the chromosome 13q31 being proposed as one of
the possible genes involved in TS [5].
Tics, the clinical hallmark of TS, are sudden, rapid, recurrent, nonrhythmic motor movements (motor tics) or
sounds (vocal tics). Motor tics can be simple, such as blinking, or complex: coordinated and sequenced movements
resembling normal motor acts or gestures that are repetitive and inappropriately intense and timed. Examples of
complex motor tics are repetitive touching and jumping.
Vocal tics may also be simple, like coughing or grunting,
or complex, when they include linguistically meaningful
verbalizations, such as shouting obscenities or profanities
(coprolalia), repeating someone else’s words or phrases
(echolalia), and repeating one’s own utterances, particularly the last syllable or word in a sentence (palilalia).
By early adulthood, roughly three-quarters of children
with TS will have greatly diminished tic symptoms and
more than one-third will be virtually tic free [6].
Both motor and vocal tics are often preceded by a sense
of urgency and imperiousness. This premonitory phenomenon consists of either localizable sensation or discomfort
in the region of the tic that compels for its execution and is
relieved by the movement [7].
Obsessive-Compulsive Disorder (OCD) is characterized by obsessive thinking and/or compulsive behavior
and has a lifetime prevalence rate in the general population between 1.9 and 3.2% [8]. Although its diagnostic
criteria remain the same in DSM-5, this disorder is now
grouped in a new chapter entitled “Obsessive-Compulsive
and Related Disorders”, along with Hoarding Disorder,
Skin-Picking Disorder, Body Dysmorphic Disorder and
Trichotillomania, among others. This new categorization
reflects the recent evidence of these disorders’ similarities,
such as an obsessive preoccupation and repetitive behaviors, and probable relatedness to each other, albeit several
contradicting family and twins studies proving an association between OCD and anxiety disorders, namely in paediatric populations [9,10].
Although children may present obsessive ideas and
compulsive behaviors as elements of normal development,
a very similar phenomenology of adult OCD may also be
present in children. So, as in adults, child OCD is an often chronic and in many cases disabling condition affecting 1–3% of the pediatric population [11]. This early onset
Tourette syndrome and Obsessive-Compulsive Disorder
subtype seems to be related to tic disorders, namely TS,
being frequently comorbid conditions. Roughly one-third
to one-half of children with TS will experience comorbid
OCD throughout their lifetime. Symptoms of OCD that
are subclinical in severity are even more common [6].
Repetitive behaviors (RB) in TS have been the subject
of several analyses, mainly due to its high prevalence and
controversy in phenomenological categorization: are they
complex motor tics or compulsions? Are they part of TS or
indicate OCD comorbidity [12]?
These questions prompt another one: to what extent
are RB in TS and OCD mediated by overlapping versus
distinct substracts [13]?
Tourette Syndrome and Obsessive-Compulsive
Disorder
Epidemiological, phenomenological and family-genetic
studies support an interrelationship between tic disorders
and OCD. This association appears to be bidirectional, with
20-60% of tic disorder patients meeting criteria for OCD, and
20-38% of children with OCD reporting comorbid tics [14].
Obsessive-compulsive symptoms (OCS) are present
in 28-63% of patients with TS and genetic studies report
an increased prevalence of OCD in first-degree relatives
of TS patients, independently of concurrent OCD in
these patients, and an increased prevalence of tics or TS
in first-degree relatives of OCD patients [15]. However,
OCD seems to be an etiologically heterogeneous entity,
with only a tic-related form of OCD being related to TS,
which is characterized by an earlier age of onset, greater
prevalence in male and higher frequency of premonitory
sensory phenomena preceding RB [12,16]. The average
age at symptom onset is even lower in a subgroup of children, the PANDAS (pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections)
subgroup, in which an abrupt onset of tic disorders, obsessions and compulsions and a temporal association with
a group-A-beta-hemolytic streptococcal (GAS) infection
were identified. In this PANDAS subgroup, the average
onset age is nearly 3 years lower than that reported for
childhood-onset OCD and up to 2 years lower than the average age of onset for tic disorders. These neuropsychiatric
symptoms are postulated to arise from an interaction of
GAS antibodies with neurons of the basal ganglia [17].
TS and OCD share several characteristics: both disorders have a chronic waxing and waning course throughout the lifetime; they are characterized by the presence of
RB, and have a childhood or juvenile onset. And although
OCD may manifest later in life, an association is apparent,
such that a large proportion of children diagnosed with
OCD also present with tics. But despite the many similarities between TS and OCD, there are of course clear
differences, as tics appear overall more likely to improve
with age, whereas OCD symptoms may worsen over time
[18]. Research has also shown that while OCD phenomARC Publishing
3
Brenha et al.
ena are accompanied by more complex thought processes
and autonomic anxiety, tics are usually preceded by shortlived sensory symptoms and feelings of incompleteness.
This difference in how RB are experienced by patients has
led to their subdivision into two categories: “OCD-like”,
or OCD-related compulsions and “Tic-like”, or TS-related impulsions [12,15]. Other differentiations include the
ego-syntonic/ego-dystonic nature of the RB, perceived
voluntariness and duration of the RB. Thus, RB in TS are
considered to be not anxiety-related, to have an egosyntonic character, to be performed in a stereotypical way,
to be stimulus-bound and to be more frequently accompanied by premonitory sensory phenomena, feelings of
incompleteness and “not just right” perceptions. Although
these “not just right” experiences are also frequently described in OCD [19], these overall features near RB to the
concept of impulsion, but it is important to note that many
of these behaviors may actually be complex motor tics.
Also, the use of terminology impulsion in TS, although is
related mainly with RB’s purpose and relation with anxiety, may associate it with Impulse Control Disorders and
to date there are no indications that these disorders are
specifically related to TS. For this reason, a more neutral
terminology has been suggested, such as “non-anxiety related” or “stimulus bound” repetitions [15].
TS and OCD-related RB, tics and compulsions, have
been associated with a dysfunction of cortico-striato-thalamo-cortical circuits, consistent with the hypothesis that obsessive-compulsive symptoms and tics might
be part of the same spectrum [12,20]. The corticostriatal
circuits are multiple parallel, segregated feedback circuits
with outputs from striatum targeting primary motor areas, and specific pre-motor and prefrontal cortical areas.
They are typically grouped in the sensorimotor circuit
(sensorimotor cortex), the associative or cognitive circuit
(dorsolateral prefrontal cortex) and the limbic circuit (anterior cingulated and orbitofrontal cortex). The primary
function of the corticostriatal circuits is to control and select goal-directed motor, cognitive and motivational behavior. Although anatomical and functional disturbances
in corticostriatal circuits are thought to be centrally involved in TS and OCD, recent neuroimaging data suggest
that motor and vocal tics in TS correspond to changes
in sensorimotor loop, whereas obsession and compulsion
in OCD are associated with the limbic loop. In TS with
comorbid OCS, not only the sensorimotor cortex is involved in motor stereotypies, but also the orbitofrontal
circuit is implicated in comorbid obsessions and compulsions. The involvement of the associative loop has been
associated with impulsive and rigid behaviors [13]. Differences in the neurobiological mechanisms underlying
RB in TS and OCD may help to explain differences in
clinical presentations and disparities in how RB are experienced by OCD and TS patients. Therefore, the driving
forces behind RB in OCD are likely to include greater focus on mental events while in TS patients there may be
IJCNMH 2015; 2:5
hyperawareness of sensory and physical experiences. In
other words, repetitive thinking in OCD is more associated with anxiety and negative emotions, involving greater
high-order conscious experience of the RB [8] and consequently being a more prefrontal-limbic phenomenon
than repetitive behavior in TS.
Children who present at the onset with pure TS generally have a quite good long-term clinical course, whereas
those who present a comorbid condition at the onset present
a more severe prognosis. Rizzo et al. (2012) reported that
OCD can have a significant negative impact on the course
of TS because of its deleterious effects on quality of life [4].
Obsessive-Compulsive Spectrum
Several authors agree with the existence of an obsessive-compulsive spectrum incorporating diverse clinical entities that share characteristics with OCD, including symptom overlap, family history, neurobiologic
features, clinical course and treatment response. Thus,
obsessive-compulsive spectrum disorders (OCSD) can be
viewed along a continuum with a compulsive risk-aversive pole at one end and an impulsive risk-seeking pole at
the opposite end [15]. In this scheme, tic-free OCD with
predominant obsessions and compulsions is positioned at
the compulsive end, whereas Impulse Control Disorders
are positioned at the impulsive pole. However, as Eric Hollander underlines, it has now become evident that many of
the OCSD have both compulsive and impulsive features,
so rather than polar opposites, compulsivity and impulsivity represent key factors that contribute in varying degrees
to each one of the OCSD that will in this sense adopt different positions along the spectrum. Hollander et al. also
point that the one unifying feature of OCSDs seems to be
that they all are linked by a RB domain [21].
Even though OCD is classified as an unitary nosological entity, recent research has indicated that OCD seems
in fact to be an heterogenous disorder, with a variety of
putative clinical phenotypes and probably different etiologies. So far, one of the best described OCD subgroup is
composed of OCD patients with an associated tic disorder. Many studies have reported that the tic-related OCD
subgroup presents specific clinical, comorbidity, neurobiological, genetic and treatment response patterns. The existence of this tic-related OCD subgroup with an overlap
of clinical features of TS and OCD explains why it may be
so difficult to differentiate these two entities [16].
By integrating RB into the referred obsessive-compulsive spectrum, TS with TS-related impulsions, compulsions and obsessions will assume a position slightly deviated towards the impulsive pole, while tic-related OCD will
be positioned closer the compulsive pole, between tic-free
OCD and TS with or without OCS. This intermediate position of tic-related OCD is justified by its shared clinical
features with both tic-free OCD and TS. But what are the
exact relative positions of these categories?
4
The precise delineation of TS and OCD subgroups is
important because the different subtypes might be related to different treatment responses and genetic transmission. One way to delineate TS from OCD subgroups is to
compare their (a) obsessive-compulsive symptomatology,
evaluate the presence of (b) sensory phenomena and (c)
treatment response.
Obsessive-Compulsive Symptomatology
It has been described that intrusive aggressive or inappropriate sexual thoughts and images are more common in TS
than OCD, whereas obsessions and compulsions in OCD
alone are more often related to fears about contamination
or harm coming to another person [8].
According to symptomatology, patients with tic-related OCD have more frequently religious obsessions, contamination worries and washing compulsions, whereas in
TS with comorbid OCD (TS+OCD) patients have more
intrusive violent and sexual images/thoughts, hoarding behaviors, counting and symmetry searching rituals,
touching behaviors, “just right” feelings, echophenomena and self-injurious behaviors. There may also be more
mental rituals in TS+OCD than in pure OCD [11,18].
Thus, according to phenomenology, although tic-related
OCD presents intermediate symptoms, it seems that it is
more closely related to tic-free OCD than to TS, whereas
TS+OCD is more similar to TS than OCD [12,15,22].
The presence of touching behaviors and echophenomena seems to better discriminate between TS and
OCD [8,15].
Although there are phenomenological differences between OCD with and without tics, they do not seem to
influence the severity of OCS [14,16], which is also not related to the presence of sensory phenomena [23].
When symptoms are measured based on dimensions,
two OCD symptom dimensions have been more frequently associated with tic-related OCD: the aggressive/
sexual/religious and the symmetry/ordering/arranging
dimensions [18].
It has also been suggested in the literature that OCS in
TS changes in character with age, with younger patients exhibiting more difficulties related to impulse control and older patients being more concerned with checking, arranging
and fear of contamination [24,25], closer to the symptoms
of non tic-related OCD. Rizzo et al (2012) reported that almost half of the children with pure TS at onset changed
their phenotype to TS+OCD after 10 years of follow-up
[4]. Together these findings raise the intriguing question of
whether OCD could actually reflect a more neurodevelopmentally mature manifestation of the same condition diagnosed as TS in some (often younger) patients [8].
Sensory Phenomena
Sensory phenomena consisting of mental or bodily sensations preceding the compulsions in the absence of any
thought, fear or worry were first described in TS patients.
Tourette syndrome and Obsessive-Compulsive Disorder
Different terms have been used in the literature to describe
these subjective experiences, including energy release,
pressure, “just-right” perceptions, premonitory urges and
other mental sensations [26]. It has been shown that up
to 93% of patients with TS can report premonitory urges, whether local or generalized with regard to body location, with a trend towards increased premonitory urges’
awareness with increased age through adolescence [26].
However, several OCD patients have described that their
compulsions are preceded not by obsessions but by subjective experiences that are compatible with the descriptions
of sensory phenomena. These phenomena, which have
been initially described in TS, have now been also associated with OCD [23], especially tic-related OCD [16, 18],
although some authors consider that these urges have a
cognitive origin in OCD whereas they are originated peripherally in TS [11].
When OCD presents sensory phenomena, often there
is higher frequency of symmetry/ordering/arranging and
contamination/washing OCS dimensions, higher frequency of comorbid TS, more common family history of tic disorders, and lower levels of insight [23]. Thus, according
to the presence of sensory phenomena, tic-related OCD is
closer to TS than to tic-free OCD.
Treatment response
The phenomenological distinction of repetitive behaviors in patients with TS is important to consider, since the
treatment of tics and OCS differs [12].
According to treatment response, TS+OCD and tic-related OCD respond differently to Selective Serotonin Reuptake Inhibitors (SSRIs) when compared to non tic-related OCD. While “Tic-like” repetitive behaviors respond
to dopamine antagonists and α2-receptors agonists (clonidine), “OCD-like” repetitive behaviors improve under
serotoninergic agents. As the use of antipsychotics in
monotherapy does not control obsessive symptoms and
the single use of SSRIs may worsen tics, the addition of antipsychotics to SSRIs is particularly useful in patients with
TS+OCD and tic-related OCD [12,27,28]. Studies evaluating the augmentation of SSRIs with antipsychotics for
treatment of refractory OCD suggest that OCD patients
with comorbid tics on an SSRI may have better response
to this intervention [6, 18]. These data may support, from
a pharmacological perspective, the existence of a continuum between OCD and TS. They also show the importance
of knowing whether tics, or obsessions and compulsions,
are the primary target of treatment, as this will affect the
selection of pharmacological agents.
Both TS and OCD might also improve with Cognitive-Behavioral Therapy, but with slight differences in
the behavioral strategies and approaches: while exposure-based cognitive behavioral therapy is useful in OCS,
Habit Reversal Training (HRT) is directed to tics [29].
Thus, regarding treatment response, tic-related OCD is
closer to TS than to tic-free OCD.
ARC Publishing
5
Brenha et al.
To date, pharmacotherapy has been considered the
treatment of choice for TS with several randomized trials
documenting the efficacy of haloperidol, pimozide, risperidone and clonidine. However, many patients refuse or
discontinue medication because of intolerable side effects,
while others are unresponsive to medication or suffer from
residual tics despite pharmacotherapy. As a result, a behavioral treatment, HRT, has become increasingly popular,
mainly as a non-pharmacologic adjunct to pharmacological treatments. Briefly, HRT involves training patients to
respond to uncomfortable sensations preceding tics with
voluntary behavior that is physically incompatible with
tics. This means that patients learn to apply antagonistic,
competing movements to inhibit the occurrence of tics.
Competing response training involves implementation
of contingent movements/ behaviors on early sensations/
urges preceding a tic that are incompatible with its execution, thereby preventing their occurrence. For this reason,
the sensory component of tics is an essential element of
HRT, as gaining awareness and describing it is a key procedure in this behavioral treatment. The trained responses,
that aim to interrupt the tic execution cycle, function as
negative reinforcements and thereby reduce the probability of future recurrence of the tic [6,30,31].
Brain stimulation techniques, including transcranial
and deep brain stimulation, constitute new approaches.
Although the efficacy of repetitive transcranial magnetic
stimulation (rTMS) has not been proven yet, some studies have reached promising results with this non-invasive
brain stimulation, as low-frequency (1Hz) rTMS to the
supplemental motor area may correct abnormal cortical
excitability in TS patients and improve symptoms [32].
Further studies using rTMS are needed in order to recognize it as an useful therapeutic tool in the future.
Chronic Motor/ Vocal Tics
Although comorbid OCD is more frequent in TS than
in other tic disorders [6], phenomenological differences in OCD phenotype have been detected according to
the presence of either TS or Chronic Motor- Vocal Tics
(CMVT) [16].
CMVT is characterized by the presence of either motor or vocal tics, but not both, for a period of more than
one year [3], having a prevalence of approximately 5% in
children [6]. Patients with OCD with comorbid CMVT
present clinical characteristics that are intermediate between those of tic-related OCD and TS+OCD according
to age at onset of OCS, frequency of sensory phenomena,
bodily sensations and "just-right" perceptions and clinical
characteristics. From a phenomenological point of view,
these results provide further evidence of a possible continuum between OCD and TS, where patients with OCD plus
tics have intermediate phenotypic features [16,18].
Since several genetic studies have been unsuccessful in
identifying the most likely mode of transmission of OCD,
IJCNMH 2015; 2:5
the hypothesis that gene are added to produce a cumulative effect seems plausible. Therefore, from a quantitative
point of view, some authors speculate that the degree of
genetic loading is higher for the disorders at the poles of
this spectrum: OCD and TS+OCD, whereas patients with
OCD+CMVT fall in between. Supporting this hypothesis
there are recent data pointing towards earlier age at onset
of OCS in the TS pole, and the earlier the age at onset, the
higher the genetic load in OCD [11,16]. But not all studies
support these data: Lewin et al. (2010) found no significant
differences in the onset age of OCS between the OCD and
OCD with comorbid tic disorder groups [14].
Conclusion
Several authors have pointed out the similarities and differences between OCD and TS, which are frequently comorbid, supporting the growing evidence that these two
entities are neurobiologically and genetically related.
There are clinical differences in OCD patients according to the presence of tics, CMVT or TS, presenting the
phenotype OCD with comorbid CMVT intermediate
characteristics compared to the other disorders, probably
reflecting the different number and type of genes involved
in the several phenotypes of tic disorders [15]. The frequent comorbidity between OCD and tic disorders, mainly in the pediatric population, has opened the way to the
discussion about a possible inclusion of a new tic-related
OCD subgroup in the future diagnostic classifications.
The term RB refers to broad and often disparate classes
of behavior linked by repetition, rigidity, invariance and
inappropriateness. RB are characteristic of many psychiatric disorders, as well as of stages of typical development.
Two types of RB can be found in TS: “Tic-like”, which
are very likely an integral part of TS and “OCD-like”, which
can be considered as a comorbid condition of TS. When
TS patients present “OCD-like” RB, generally they present
more complex and severe tics, better response to SSRIs and
antipsychotic drugs and less successful socio-professional
adaptation [12]. Thus, a meticulous semiological analysis
of RB in TS patients will help adjusting treatment and predict prognosis.
Attempts to distinguish between OCD and TS based on
the specific types of RB presented are not without limitations, as categorization will depend, among other factors,
on the awareness of the compulsive experience which will
vary according to the individual’s own subjective nature
of interpretation. This in turn could be affected by other
factors that are rarely considered in RB research studies,
such as personality, intelligence and locus of control, and
that can potentially influence results when administering
self-assessment measures. Also, evaluation of the literature pertaining to the phenomenological experience of
OCD and TS has its own limitations as different studies
categorize patients differently: for example, some included
TS+OCD and tic-related OCD in the same group, while
6
others did not differentiate TS+OCD from TS with comorbid subclinical OCS. These diverse methodologies reflect
the difficulties in RB categorization. Overall, however, it
seems that contamination worries are probably indicative of OCD, and RB linked to echophenomena, touching,
symmetry and counting may be most common in TS. It
may be of use also to note that while patients with OCD
seem to be focused on avoiding harm as much as possible, patients with TS often display RB which are ironically
self-defeating, dangerous (e.g. touching very hot or sharp
objects) and socially inappropriate (e.g. coprolalia) [8].
A further difficulty with assessing RB includes the dynamicity of the phenomenological experience. That is,
these symptoms can change in nature over time, perhaps as
the RB become more automated, or as continued reflection
allows the subject to become more aware of any preceding
cognitions or sensory cues. This could help explain why
the report of RB can change with age and the finding that
changes in diagnosis may occur over time, being tics more
often diagnosed in children and OCD more often seen in
adults [4,8]. Furthermore, corticostriatal circuits have a
protracted development trajectory and neurobiological
changes associated with RB may change over development.
Finally, TS is characterized by different clinical phenotypes at the onset that are not always stable over the years
and that mean different severity of symptoms, response to
the pharmacological treatment and impairment in quality
of life. Further research focusing the response of different
RB to SSRIs, anti-dopaminergic medications and other
interventions will be of great value in tailoring interventions to the needs of individual patients within the obsessive-compulsive spectrum [4,7].
Abreviations
CMVT: Chronic motor-vocal tics; HRT: Habit reversal training; OCD:
Obsessive-compulsive disorder; OCS: Obsessive-compulsive symptoms;
OCSD: Obsessive-compulsive spectrum disorders; rTMS: Repetitive
transcranial magnetic stimulation; RB: Repetitive behaviors; SSRIs:
Selective Serotonin Reuptake Inhibitors; TS: Tourette Syndrome
Competing interests
The authors declare no conflict of interest.
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