s00415-016-8373-z.pdf

J Neurol (2017) 264:1536–1541 DOI 10.1007/s00415-016-8373-z NEUROLOGICAL UPDATE Focal task specific dystonia: a review and update Christine M. Stahl1 Steven J. Frucht1 Received: 14 October 2016 / Revised: 16 December 2016 / Accepted: 19 December 2016 / Published online: 30 December 2016  T...

J Neurol (2017) 264:1536–1541 DOI 10.1007/s00415-016-8373-z NEUROLOGICAL UPDATE Focal task specific dystonia: a review and update Christine M. Stahl1 Steven J. Frucht1 Received: 14 October 2016 / Revised: 16 December 2016 / Accepted: 19 December 2016 / Published online: 30 December 2016  The Author(s) 2016. This article is published with open access at Springerlink.com Abstract In this review, we summarize recent advances in While the term ‘‘dystonia’’ was first used in 1911 by understanding the etiology, risk factors and pathophysiol- Oppenheim, the clinical phenomenon had been described ogy of focal task specific dystonia (FTSD), movement almost a century earlier in patients with FTSD. In 1830, disorders characterized by abnormal motor activation dur- clerks in the British Civil Service were noted to develop ing the performance of specific, repetitive actions. We difficulty with writing. After observing these clerks, Sir focus on two common FTSD, musician’s dystonia and Charles Bell remarked that he ‘‘found the action necessary writer’s cramp. FTSD may pose a threat to the patient’s for writing gone, or the motions so irregular as to make the livelihood, and improved therapeutic treatments are letters be written zig-zag, whilst the power of strongly needed. moving the arm for fencing remained…’’. Later in the 1860s, Samuel Solly labeled this condition ‘‘scrivener’s Keywords Focal task specific dystonia (FTSD)
Writer’s palsy’’. While ‘‘scrivener’s palsy’’ or writer’s cramp, as cramp
Musician’s dystonia it is now called, is one of the more recognized forms of FTSD, dystonia may affect musicians, typists, hairdressers, painters, shoemakers and tailors [5–7]. Sport-related FTSD Introduction have also been described in golfers, pistol shooters and ping-pong players, among others. Because of their associ- Dystonias are a diverse ‘‘group of movement disorders ation with repetitive, fine motor tasks often linked to one’s characterized by sustained or intermittent muscle contrac- profession, FTSD have also been referred to as occupa- tions causing abnormal, often repetitive, movements, pos- tional dystonias. Interestingly, until the 1980s FTSD were tures, or both’’. Recently updated consensus opinion erroneously interpreted to be psychogenic in origin, often classifies dystonias by two axes: clinical characteristics and termed ‘‘occupational neuroses.’’ In 1982, evidence for an etiology. The first axis, clinical characteristics, includes the organic etiology emerged from the work of Sheehy and age of onset, affected body region, temporal pattern, and Marsden. associated neurologic or systemic features. A subclas- In this review, we discuss the phenomenology and epi- sification includes focal task specific dystonias (FTSD), demiology of two of the most common forms of FTSD, which are a diverse group of focal dystonias affecting an writer’s cramp and musician’s dystonia. We then discuss isolated body part and are triggered, at least initially, by a emerging findings on the etiology, pathophysiology and specific action. treatment of FTSD. Background & Steven J. Frucht [email protected] FTSD typically begins in adulthood with symptom onset in 1 Icahn School of Medicine at Mount Sinai, 5 East 98th Street, the third to sixth decade. Unlike other adult onset primary Box 1138, First Floor, New York, NY 10029, USA focal dystonias, FTSD is more common in men, and it 123 J Neurol (2017) 264:1536–1541 1537 usually affects the arm, facial muscles or larynx. production of the desired air stream. Embouchure dystonias Overall prevalence estimates for FTSD in the general may be further classified by the pattern of abnormal population range from 7 to 69 per million [10, 11]. How- movements, including embouchure tremor, involuntary lip ever, prevalence has been estimated to be much higher in movements and jaw closure. selected groups; for instance, some studies have shown as many as 14% of patients seen at performing arts medical centers have FTSD [12, 13]. Advances in understanding FTSD typically presents as an insidious, painless loss of dexterity triggered by performance of a specific, often In recent years, much effort has focused on understanding over-practiced task. Symptoms progress over time to trig- the etiology, risk factors and pathophysiology of FTSD and ger uncontrolled activation of muscle groups, leading to potential therapeutic interventions. We will review these in abnormal postures and movements. Early in the disease turn. course, the dystonia typically is triggered only by the performance of a specific task, but over time spreads to Etiology involve other tasks, or even spreads to previously unaf- fected areas of the body. As with other types of dystonias, The etiology of FTSD remains unknown, although recent sensory tricks, or geste antagonistes, may temporarily lines of evidence suggest that both genetic and environ- reduce the dystonic symptoms of FTSD. mental factors are important. Examination of family members of patients with FTSD revealed up to 25% of patients with an affected family member [18, 19]. This is Writer’s cramp and musician’s dystonia consistent with a recent study of musician’s dystonia which found approximately 20% of patients with a similarly Writer’s cramp is characterized by involuntary cramping of affected family member. A recent genome-wide muscles of the hand, forearm, or upper arm selectively analysis has found an association with the arylsulfatase G triggered by writing. Typically, the distal muscles of the (ARSG) gene in both musician’s hand dystonia and wri- upper extremity are affected, but dystonia may progress to ter’s cramp, but to date, a specific causative mutation include more proximal muscle groups, may be triggered by within this gene has not been identified [21, 22]. Addi- other activities, and can even spread to the opposite non- tionally, in a study of musicians with FTSD of the hand, dominant hand. Average age of onset is in the fourth along with patients with writer’s cramp and their relatives, decade, and once present, symptoms rarely remit. reduced interhemispheric inhibition as measured by tran- FTSD seen in musicians, a group that may be at risk due scranial magnetic stimulation (TMS) was observed in to overly practiced fine motor tasks, typically manifests in individuals where there was a positive family history for two phenotypes based on the particular instrument: musi- dystonia. This finding suggests that reduced interhemi- cian’s hand dystonia or embouchure dystonia. Musician’s spheric inhibition may serve as a possible endophenotypic dystonia can occur in both amateur and professional marker of genetic susceptibility for developing FTSD. musicians, men are affected four times as often as women, In addition to repetitive, over-practicing of a motor task, and average symptom onset is in the fourth decade. other environmental factors may contribute to the risk Musician’s hand dystonia has been reported with a vari- factors of developing FTSD. Possible risk factors include ety of instruments, including piano, violin, guitar, flute, personality traits, such as perfectionism and anxiety, clarinet, horn and tabla, among others. Dystonia typically anatomical factors, such as hand size and joint mobility, as occurs in the hand that performs the more demanding tasks, well as delayed onset of age of musical training such as the right hand in pianists and the left hand in vio- [17, 24, 25]. linists. The specific pattern of abnormal muscle acti- vation varies by instrument. For example, abnormal flexion Pathophysiology of the fingers is typically seen in pianists and violinists, while in woodwind or brass players, extension due to lum- The pathophysiology of FTSD has been linked to abnor- brical activation can occur. FTSD may be exquisitely malities in inhibition, plasticity, and motor networks. In task specific, triggered by playing one instrument, but 1995, experiments first demonstrated decreased short sparing the hand when a patient plays a different instrument. intracortical inhibition (SICI) in FTSD patients compared Embouchure dystonia may affect brass and woodwind to healthy controls using TMS. Interestingly, this players, with age of onset in the fourth decade. The abnormality was found in the bilateral hemispheres of embouchure is the critical interplay of the lips and facial patients, despite unilateral symptoms. Recent research has muscles with the instrument’s mouthpiece that controls the therefore postulated that decreased SICI may not directly 123 1538 J Neurol (2017) 264:1536–1541 cause abnormal motor activation but rather facilitate the have reported increased cerebellar activity in patients with development of FTSD through other mechanisms [27, 28]. writer’s cramp [47–49], while others have demonstrated Specifically, one suggested mechanism, found in several decreased activity in the cerebellum during hand activation studies of FTSD patients, is the development of impaired in FTSD [50, 51]. Further research is warranted to under- surround inhibition, a neural inhibitory mechanism stand the precise network abnormalities; however, evidence responsible for the selective recruitment and activation of of aberrant connections between the basal ganglia and muscles necessary for a particular task with inactivation of cerebellum leading to dystonia is supported by research the neighboring muscles that are unnecessary [27, 29, 30]. demonstrating that interruption of this connection leads to Consistent with the hypothesis of decreased SICI and improvement of the dystonic symptoms. impaired surround inhibition, multiple studies have shown a loss of dexterity and impaired independent movement of Treatment fingers of patients with either writer’s cramp or musician’s dystonia [31–33]. Current treatment modalities for FTSD include oral medi- Another interesting abnormality that may contribute to cation, chemodenervation, surgery and physical therapy. FTSD pathology is maladaptive neural plasticity. While Anticholinergic agents like trihexyphenidyl, as well as plasticity is believed to be critical to the processes of other medications, such as primidone, baclofen, and learning and memory, maladaptive neuroplastic responses phenytoin have been tried with inconsistent responses and in both the motor and sensory cortices have been examined frequent intolerable side effects [53–55]. Chemodenerva- in conditioning protocols using repetitive stimuli from tion with botulinum neurotoxin (BoNT) type A has been TMS. Patients with writer’s cramp exhibited abnormal the mainstay of treatment for FTSD. responses to paired associative stimulation of the median Each of the seven known BoNT serotypes (types A–G) nerve and primary motor cortex. Such abnormalities targets a specific SNARE protein for degradation in included increased facilitation with spread to non-median peripheral cholinergic neurons, thereby preventing the nerve innervated muscles in addition to the absence of a downstream release of acetylcholine into the neuromus- typical cortical silent period. More recently, experi- cular junction. As a result, chemodenervation and subse- ments demonstrated a decreased short latency afferent quent muscle paralysis occur and persist for several months inhibition following 1-Hz repetitive TMS in writer’s until the eventual degradation of BoNT and regeneration of cramp, but not in normal controls. SNARE proteins. While the inhibition of acetylcholine Furthermore, in both musician’s dystonia and writer’s release at the neuromuscular junction is believed to be a cramp, functional neuroimaging experiments have major component of BoNT’s mechanism of action, there is demonstrated abnormal cortical representations of digits increasing evidence that BoNT also acts peripherally at and reorganization of the sensory homunculus in the sen- gamma motor neurons to reduce afferent sensory input sory cortex [37–39]. Such aberrant somatotopy may be from muscle spindles to the central nervous system and to reversible with associated improved fine motor control alter sensorimotor pathways [57–61]. Treatment of limb using constraint-induced therapy [40–42]. However, dystonia with BoNT has demonstrated transient increased another study of somatotopic mapping discovered bilateral intracortical inhibition on par with normal levels of inhi- misrepresentation of digits despite unilateral dystonic bition as measured by transcranial magnetic stimulation symptoms, suggesting that the disturbed somatotopy is an. Furthermore, recent research suggests that BoNT may endophenotype for vulnerability to develop FTSD. additionally have non-SNARE cellular targets involved in Regardless of the etiology of the aberrant somatotopy, the wide-ranging activities, such as cell division and apoptosis, evidence suggests that maladaptive plasticity of FTSD neuritogenesis and gene expression. impairs sensorimotor integration. Of the seven BoNT serotypes, only serotype A and to a Finally, results from recent investigations have suggested lesser extent serotype B are available for clinical use, with a network disorder leading to FTSD, whereby involvement specific formulations of each serotype characterized by of the entire sensorimotor network contributes to dystonia different potency, immunogenicity, preparation, compound. Hyperactivation of the basal ganglia has been stability and heat tolerance. Notably, BoNT type B is only demonstrated in fMRI studies of writer’s cramp. Fur- formally approved for the treatment of cervical dystonia, ther aberrant basal ganglia function has been demonstrated while BoNT type A has approved indications in the treat- by PET studies, which have shown decreased release of ment of both neurologic and non-neurologic conditions striatal dopamine during hand activation in patients with. Multiple studies have demonstrated long-lasting writer’s cramp. Cerebellar dysfunction has also been treatment benefits of BoNT in FTSD, but there is a delicate suggested to contribute to FTSD, although the specific balance between reducing dystonic symptoms without abnormality is not well understood. Some investigations inducing concurrent residual weakness resulting in loss of 123 J Neurol (2017) 264:1536–1541 1539 motor function [53, 65–68]. Even with treatment, many The triggering activity can be associated with one’s occu- affected musicians are no longer able to play profession- pation, leading to the disorder’s further classification as an ally, due to the high level of fine motor skill required for occupational dystonia. The development of such a condi- continued professional performance. tion can impact one’s livelihood, particularly if symptoms In recent years, emerging studies have investigated the are severe. While progress has been made in recent years in role of surgery and sensorimotor retraining as therapeutic understanding the etiology, risk factors and pathophysiol- options. Thalamotomies have been performed as treatment ogy of FTSD, improved therapeutic options are needed. of a variety of movement disorders since the 1950s. In what was the largest published case series of patients with Compliance with ethical standards writer’s cramp undergoing stereotactic ventro-oral thala- Conflicts of interest The authors have no conflict of interest to motomy, eleven of twelve patients reported almost com- report. plete resolution of symptoms with sustained benefit for over one year after surgery. Based on its benefit for Open Access This article is distributed under the terms of the writer’s cramp, stereotactic ventro-oral thalamotomy was Creative Commons Attribution 4.0 International License (http://crea tivecommons.org/licenses/by/4.0/), which permits unrestricted use, demonstrated to improve medically refractory musician’s distribution, and reproduction in any medium, provided you give dystonia with long-term benefit. More recently in appropriate credit to the original author(s) and the source, provide a 2016, treatment with noninvasive gamma knife ventro-oral link to the Creative Commons license, and indicate if changes were thalamotomy was shown to be effective in a case of made. refractory musician’s dystonia for a patient who was deemed too high-risk for conventional stereotactic thala- motomy. However, larger long-term follow-up studies will be necessary to evaluate the lasting efficacy of this References intervention. Additionally, a small case series has investi- 1. 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