Tiefe Hirnstimulation als Therapieoption für das Tourette-Syndrom

ZUSAMMENFASSUNG

Das Tourette-Syndrom (TS) ist eine neuropsychiatrische Erkrankung, die durch das Auftreten motorischer und vokaler Tics charakterisiert ist. Bei einem geringen Teil der Patienten sind die Symptome durch medikamentöse und behaviorale Therapie nicht ausreichend gut behandelbar. Hier kann eine Therapieeskalation erwogen werden. Die tiefe Hirnstimulation (THS) ist ein invasives Therapieverfahren, das bei bestimmten Bewegungsstörungen etabliert ist und für die Therapie des TS zunehmend an Bedeutung gewinnt. Der folgende Artikel fasst die aktuelle Evidenz zur Anwendung der THS beim TS zusammen. Die meiste Erfahrung liegt für die thalamische und pallidale Stimulation vor, wobei bisher keines der Zielgebiete deutlich überlegen war. Die Studienlage zeigt eine durchschnittliche Reduktion der Tic-Schwere unter THS von bis zu 40 % nach einem Jahr. Inwiefern die THS zu einer Besserung der oft begleitenden psychiatrischen Komorbiditäten führt, bleibt aufgrund der geringen Fallzahlen unsicher. Beim TS ist eine erhöhte Anzahl an postoperativen Infektionen aufgefallen, deren Ursache nicht geklärt wurde. Zusammenfassend zeigen die Studien, dass eine THS beim TS eine sichere Therapieoption zur Behandlung schwerer medikamentös nicht behandelbarer Tics darstellt. Die THS sollte an Zentren durchgeführt werden, in denen Expertise sowohl in der Behandlung von Tics als auch für THS vorliegt.

ABSTRACT

Tourette syndrome (TS) is a neurodevelopmental disorder characterized by the presence of motor and vocal tics. In a subset of patients pharmacological and behavioural therapy are not effective and deep brain stimulation should be considered. Deep brain stimulation (DBS) is an invasive therapy established for specific movement disorders that has been gaining relevance in the treatment of TS. This article aims to give an overview about the use of DBS in TS. Recent evidence reports on an average reduction in tic severity over 40 % after one year of DBS, but long-term data on efficacy are sparce. It remains to be elucidated if psychiatric comorbidities of TS improve with DBS. Even though there is most experience with thalamic and pallidal targets for DBS in TS, optimal target selection remains unclear. Stimulation associated side effects depend on the anatomical target. Hardware infections are more common adverse events in patients with TS than in other indications for DBS. Thus, DBS should be considered for patients with treatment-resistant TS that suffer from severe tics. Importantly, in cases evaluated for DBS, tics should be the predominant source of disability. The operation should be performed in centres with long-standing experience both in the treatment of tics and DBS.

Schlüsselwörter

Tourette-Syndrom - tiefe Hirnstimulation - Neuromodulation - Neuropsychiatrie

Key words

Tourette syndrome - deep brain stimulation - neuromodulation - neuropsychiatry

• Literatur

• 1 American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders: DSM-5. Arlington: VA; 2013
• 2 Knight T, Steeves T, Day L. et al Prevalence of tic disorders: a systematic review and meta-analysis. Pediatric neurology 2012; 47 (02) 77-90
• 3 Bloch MH, Peterson BS, Scahill L. et al Adulthood Outcome of Tic and Obsessive-Compulsive Symptom Severity in Children With Tourette Syndrome. Archives of Pediatrics & Adolescent Medicine 2006; 160 (01) 65
• 4 Pringsheim T, Okun MS, Müller-Vahl K. et al Practice guideline recommendations summary: Treatment of tics in people with Tourette syndrome and chronic tic disorders. Neurology 2019; 92 (19) 896-906
• 5 Deuschl G, Schade-Brittinger C, Krack P. et al A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 2006; 355 (09) 896-908
• 6 Volkmann J, Wolters A, Kupsch A. et al Pallidal deep brain stimulation in patients with primary generalised or segmental dystonia: 5-year follow-up of a randomised trial. The Lancet Neurology 2012; 11 (12) 1029-38
• 7 Volkmann J, Mueller J, Deuschl G. et al Pallidal neurostimulation in patients with medication-refractory cervical dystonia: a randomised, sham-controlled trial. The Lancet Neurology 2014; 13 (09) 875-84
• 8 Kühn AA, Kupsch A, Schneider GH. et al Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in Parkinson’s disease. Eur J Neurosci 2006; 23 (07) 1956-60
• 9 Kühn AA, Kempf F, Brücke C. et al High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson’s disease in parallel with improvement in motor performance. J Neurosci 2008; 28 (24) 6165-73
• 10 Kühn AA, Volkmann J. Innovations in deep brain stimulation methodology. Movement Disorders 2017; 32 (01) 11-9
• 11 Neumann W-J, Huebl J, Brücke C. et al Pallidal and thalamic neural oscillatory patterns in tourette’s syndrome. Annals of Neurology 2018; 84 (04) 505-14
• 12 Hariz MI, Blomstedt P, Zrinzo L. Deep brain stimulation between 1947 and 1987 the untold story. Neurosurg Focus 2010; 29 (02) E1
• 13 Schnitzler A, Gross J. Normal and pathological oscillatory communication in the brain. Nature Reviews Neuroscience 2005; 6 (04) 285-96
• 14 Lozano AM, Lipsman N, Bergman H. et al Deep brain stimulation: current challenges and future directions. Nature Reviews Neurology 2019 E-pub
• 15 Hariz M, Blomstedt P, Zrinzo L. Future of brain stimulation: new targets, new indications, new technology. Movement Disorders 2013; 28 (13) 1784-92
• 16 Mink JW. Basal ganglia dysfunction in Tourette’s syndrome: a new hypothesis. Pediatric Neurology 2001; 25 (03) 190-8
• 17 Albin RL, Mink JW. Recent advances in Tourette syndrome research. Trends in Neurosciences 2006; 29 (03) 175-82
• 18 Cheng B, Braass H, Ganos C. et al Altered intrahemispheric structural connectivity in Gilles de la Tourette syndrome. NeuroImage: Clinical 2014; 4: 174-81
• 19 Worbe Y, Marrakchi-Kacem L, Lecomte S. et al Altered structural connectivity of cortico-striato-pallido-thalamic networks in Gilles de la Tourette syndrome. Brain 2015; 138 (02) 472-82
• 20 Worbe Y, Malherbe C, Hartmann A. et al Functional immaturity of cortico-basal ganglia networks in Gilles de la Tourette syndrome. Brain 2012; 135 (06) 1937-46
• 21 Wang Z, Maia TV, Marsh R. et al The Neural Circuits That Generate Tics in Tourette’s Syndrome. American Journal of Psychiatry 2011; 168 (12) 1326-37
• 22 Neumann W-J, Schroll H, de Almeida Marcelino AL. et al Functional segregation of basal ganglia pathways in Parkinson’s disease. Brain 2018; 141 (09) 2655-69
• 23 de Almeida Marcelino AL, Horn A, Krause P. et al Subthalamic neuromodulation improves short-term motor learning in Parkinson’s disease. Brain 2019; 142 (08) 2198-206
• 24 Singer HS, Szymanski S, Giuliano J. et al Elevated Intrasynaptic Dopamine Release in Tourette’s Syndrome Measured by PET. American Journal of Psychiatry 2002; 159 (08) 1329-36
• 25 Wong DF, Brašić JR, Singer HS. et al Mechanisms of Dopaminergic and Serotonergic Neurotransmission in Tourette Syndrome: Clues from an In Vivo Neurochemistry Study with PET. Neuropsychopharmacology 2008; 33 (06) 1239-51
• 26 Vernaleken I, Kuhn J, Lenartz D. et al Bithalamical Deep Brain Stimulation in Tourette Syndrome Is Associated with Reduction in Dopaminergic Transmission. Biological Psychiatry 2009; 66 (10) e15-7
• 27 Vandewalle V, van der Linden C, Groenewegen HJ. et al Stereotactic treatment of Gilles de la Tourette syndrome by high frequency stimulation of thalamus. The Lancet 1999; 353 9154 724
• 28 Hassler R, Dieckmann G. [Stereotaxic treatment of tics and inarticulate cries or coprolalia considered as motor obsessional phenomena in Gilles de la Tourette’s disease]. Revue neurologique 1970; 123 (02) 89-100
• 29 Rickards H, Wood C, Cavanna AE. Hassler and Dieckmann’s seminal paper on stereotactic thalamotomy for Gilles de la Tourette syndrome: Translation and critical reappraisal. Movement Disorders 2008; 23 (14) 1966-72
• 30 Schrock LE, Mink JW, Woods DW. et al Tourette syndrome deep brain stimulation: A review and updated recommendations. Movement Disorders 2015; 30 (04) 448-71
• 31 Martinez-Ramirez D, Jimenez-Shahed J, Leckman JF. et al Efficacy and Safety of Deep Brain Stimulation in Tourette Syndrome. JAMA Neurology 2018; 75 (03) 353
• 32 Baldermann JC, Schüller T, Huys D. et al Deep Brain Stimulation for Tourette-Syndrome: A Systematic Review and Meta-Analysis. Brain Stimulation 2016; 9 (02) 296-304
• 33 Ackermans L, Duits A, van der Linden C. et al Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. Brain 2011; 134 (03) 832-44
• 34 Kefalopoulou Z, Zrinzo L, Jahanshahi M. et al Bilateral globus pallidus stimulation for severe Tourette’s syndrome: a double-blind, randomised crossover trial. The Lancet Neurology 14 (06) 595-605
• 35 Welter M-L, Houeto J-L, Thobois S. et al Anterior pallidal deep brain stimulation for Tourette’s syndrome: a randomised, double-blind, controlled trial. The Lancet Neurology 2017; 16 (08) 610-9
• 36 Houeto JL, Karachi C, Mallet L. et al Tourette’s syndrome and deep brain stimulation. Journal of neurology, neurosurgery, and psychiatry 2005; 76 (07) 992-5
• 37 Welter M-L, Mallet L, Houeto J-L. et al Internal Pallidal and Thalamic Stimulation in Patients With Tourette Syndrome. Archives of Neurology 2008; 65 (07) 952-7
• 38 Maciunas RJ, Maddux BN, Riley DE. et al Prospective randomized double-blind trial of bilateral thalamic deep brain stimulation in adults with Tourette syndrome. Journal of neurosurgery 2007; 107 (05) 1004-14
• 39 Rodriguez-Oroz MC, Obeso JA, Lang AE. et al Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain 2005; 128 Pt 10 2240-9
• 40 Hirschtritt ME, Lee PC, Pauls DL. et al Lifetime Prevalence, Age of Risk, and Genetic Relationships of Comorbid Psychiatric Disorders in Tourette Syndrome. JAMA Psychiatry 2015; 72 (04) 325
• 41 Porta M, Brambilla A, Cavanna AE. et al Thalamic deep brain stimulation for treatment-refractory Tourette syndrome: two-year outcome. Neurology 2009; 73 (17) 1375-80
• 42 Johnson KA, Fletcher PT, Servello D. et al Image-based analysis and long-term clinical outcomes of deep brain stimulation for Tourette syndrome: a multisite study. Journal of neurology, neurosurgery, and psychiatry 2010; 90 (10) 1078-90
• 43 Bajwa RJ, de Lotbinière AJ, King RA. et al Deep brain stimulation in Tourette’s syndrome. Movement Disorders 2007; 22 (09) 1346-50
• 44 Smeets AYJM, Duits AA, Leentjens AFG. et al Thalamic Deep Brain Stimulation for Refractory Tourette Syndrome: Clinical Evidence for Increasing Disbalance of Therapeutic Effects and Side Effects at Long-Term Follow-Up. Neuromodulation: Technology at the Neural Interface 2018; 21 (02) 197-202
• 45 Hariz MI. Complications of deep brain stimulation surgery. Movement Disorders 2002; 17 S3 S162-6
• 46 Servello D, Sassi M, Gaeta M. et al Tourette syndrome (TS) bears a higher rate of inflammatory complications at the implanted hardware in deep brain stimulation (DBS). Acta Neurochirurgica 2011; 153 (03) 629-32
• 47 Servello D, Sassi M, Brambilla A. et al Long-Term, Post-Deep Brain Stimulation Management of a Series of 36 Patients Affected With Refractory Gilles de la Tourette Syndrome. Neuromodulation: Technology at the Neural Interface 2010; 13 (03) 187-94
• 48 Krack P, Hariz MI, Baunez C. et al Deep brain stimulation: from neurology to psychiatry?. Trends in Neurosciences 2010; 33 (10) 474-84
• 49 Vandewalle V, van der Linden C, Groenewegen H. et al Stereotactic treatment of Gilles de la Tourette syndrome by high frequency stimulation of thalamus. The Lancet 1999; 353 9154 724
• 50 Cannon E, Silburn P, Coyne T. et al Deep Brain Stimulation of Anteromedial Globus Pallidus Interna for Severe Tourette’s Syndrome. American Journal of Psychiatry 2012; 169 (08) 860-6
• 51 Diederich NJ, Kalteis K, Stamenkovic M. et al Efficient internal pallidal stimulation in Gilles de la Tourette syndrome: A case report. Movement Disorders 2005; 20 (11) 1496-9
• 52 Shahed J, Poysky J, Kenney C. et al GPi deep brain stimulation for Tourette syndrome improves tics and psychiatric comorbidities. Neurology 2007; 68 (02) 159-60
• 53 Dehning S, Feddersen B, Cerovecki A. et al Globus pallidus internus-deep brain stimulation in Tourette’s syndrome: Can clinical symptoms predict response?. Movement Disorders 2011; 26 (13) 2440-1
• 54 Piedimonte F, Andreani JCM, Piedimonte L. et al Behavioral and Motor Improvement After Deep Brain Stimulation of the Globus Pallidus Externus in a Case of Tourette’s Syndrome. Neuromodulation: Technology at the Neural Interface 2013; 16 (01) 55-8
• 55 Kuhn J, Lenartz D, Mai JK. et al Deep brain stimulation of the nucleus accumbens and the internal capsule in therapeutically refractory Tourette-syndrome. Journal of Neurology 2007; 254 (07) 963-5
• 56 Flaherty AW, Williams ZM, Amirnovin R. et al Deep Brain Stimulation of the Anterior Internal Capsule for the Treatment of Tourette Syndrome: Technical Case Report. Operative Neurosurgery 2005; 57 (Suppl. 04) E403
• 57 Neuner I, Podoll K, Lenartz D. et al Deep Brain Stimulation in the Nucleus Accumbens for Intractable Tourette’s Syndrome: Follow-Up Report of 36 Months. Biological Psychiatry 2009; 65 (04) e5-6
• 58 Martinez-Torres I, Hariz MI, Zrinzo L. et al Improvement of tics after subthalamic nucleus deep brain stimulation. Neurology 2009; 72 (20) 1787-9
• 59 Fraint A, Pal G. Deep Brain Stimulation in Tourette’s Syndrome. Frontiers in Neurology 2010; 6: 170
• 60 Ackermans L, Temel Y, Cath D. et al Deep brain stimulation in Tourette’s syndrome: Two targets?. Movement Disorders 2006; 21 (05) 709-13
• 61 Visser-Vandewalle V, Temel Y, Boon P. et al Chronic bilateral thalamic stimulation: a new therapeutic approach in intractable Tourette syndrome. Journal of Neurosurgery 2003; 99 (06) 1094-100
• 62 Kaido T, Otsuki T, Kaneko Y. et al Deep brain stimulation for Tourette syndrome: a prospective pilot study in Japan. Neuromodulation 2011; 14 (02) 123-8
• 63 Martínez-Fernández R, Zrinzo L, Aviles-Olmos I. et al Deep brain stimulation for Gilles de la Tourette syndrome: A case series targeting subregions of the globus pallidus internus. Movement Disorders 2011; 26 (10) 1922-30
• 64 Horn A, Kühn AA, Merkl A. et al Probabilistic conversion of neurosurgical DBS electrode coordinates into MNI space. NeuroImage 2017; 150: 395-404
• 65 Ewert S, Plettig P, Li N. et al Toward defining deep brain stimulation targets in MNI space: A subcortical atlas based on multimodal MRI, histology and structural connectivity. NeuroImage 2018; 170: 271-82
• 66 Edlow BL, Mareyam A, Horn A. et al 7 Tesla MRI of the ex vivo human brain at 100 micron resolution. Scientific data 2019; 6 (01) 244
• 67 Servello D, Sassi M, Brambilla A. et al De novo and rescue DBS leads for refractory Tourette syndrome patients with severe comorbid OCD: a multiple case report. Journal of Neurology 2009; 256 (09) 1533-9
• 68 Motlagh MG, Smith M, Landeros-Weisenberger A. et al Lessons Learned from Open-label Deep Brain Stimulation for Tourette Syndrome: Eight Cases over 7 Years. Tremor and Other Hyperkinetic. Movements 2013: 3 tre-03-170-4428-1
• 69 Ganos C, Martino D, Espay AJ. et al Tics and functional tic-like movements: Can we tell them apart? Neurology. NLM (Medline) 2019; 93 (17) 750-8
• 70 Müller-Vahl K, Dodel I, Müller N. et al Health-related quality of life in patients with Gilles de la Tourette’s syndrome. Movement Disorders 2010; 25 (03) 309-14
• 71 Schuepbach WMM, Rau J, Knudsen K. et al Neurostimulation for Parkinson’s Disease with Early Motor Complications. New England Journal of Medicine 2013; 368 (07) 610-22
• 72 Horn A, Reich M, Vorwerk J. et al Brain Stimulation Outcome in Parkinson Disease. 2017: 67-78
• 73 Marceglia S, Rosa M, Servello D. et al Adaptive Deep Brain Stimulation (aDBS) for Tourette Syndrome. Brain Sciences 2017; 8 (01) 4
• 74 Molina R, Okun MS, Shute JB. et al Report of a patient undergoing chronic responsive deep brain stimulation for Tourette syndrome: proof of concept. Journal of neurosurgery 2018; 129 (02) 308-14
• 75 Okun MS, Foote KD, Wu SS. et al A Trial of Scheduled Deep Brain Stimulation for Tourette Syndrome. JAMA Neurology 2013; 70 (01) 85
• 76 Rossi PJ, Opri E, Shute JB. et al Scheduled, intermittent stimulation of the thalamus reduces tics in Tourette syndrome. Parkinsonism & Related Disorders 2016; 29: 35-41