Parkinsonism and Related Disorders 20 (2014) 1438e1439
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Letter to the Editor
The benefits of low-frequency pallidal deep brain stimulation in a patient with Tourette syndrome Keywords: Tourette syndrome Deep brain stimulation (DBS) Low frequency Globus pallidus internus
Tourette syndrome (TS) is a neuropsychiatric disorder characterized by uncontrolled motor and phonic tics, which is often comorbid with behavioral disorders. Deep brain stimulation (DBS) of the globus pallidus internus (GPi) has been proposed as a therapeutic option for patients with refractory TS. High-frequency (130e185 Hz) stimulation has been conventionally used. Herein, we describe the results of bilateral GPi-DBS in medically intractable TS. Beneficial effects were sustained after the stimulation frequency was reduced from 130 to 65 Hz. A 33-year-old man suffered from marked involuntary neck rotation, shoulder jerks and kicks since the age of 8 years. Coprolalia was present by the age of 9. Comorbidities included repetitive thoughts about a sentence of lyrics and compulsive picking of leaves. The patient was diagnosed with TS according to the criteria of DSM-IV. Tics symptoms seriously hampered his work and quality of life and caused secondary depression. He had been treated with haloperidol, clonidine and risperidone for tics with only mild transient benefit. The medication treatment was not effective and caused significant side effects (sedation, restlessness and blurred vision). After obtaining informed consent, the patient underwent DBS with MRI-guided stereotaxy in March 2011. Electrodes (Medtronic, model 3387; Medtronic, Minneapolis, MN, USA) were implanted bilaterally under local anesthesia and connected to a pulse generator (Kinetra, Medtronic) under general anesthesia. Different stimulation parameters were tried within 1 week after surgery. Stimulation parameters were chosen with a monopolar stimulation (2-, 6-; caseþ), amplitude of 2.8 V, pulse width of 90 ms, and frequency of 130 Hz for both sides. After 33 months (6 months before the final assessment), the stimulation frequency was changed from 130 to 65 Hz. The other parameters remained unchanged. The Yale Global Tic Severity Scale (YGTSS) and the Modified Rush Video-Based Tic Rating Scale (VTRS) were used to evaluate the patient's tics before and after DBS. Compulsion and psychological symptoms were also assessed with the YaleeBrown Obsessive Compulsive Scale (Y-BOCS), Hamilton Anxiety Scale (HAS), and Hamilton Depression Scale (HDS). Postoperatively, no obvious side effects were observed. Electrode positions were determined using MRI. The tips of the electrode were located in the posteroventral GPi. Substantial improvements in tics and comorbid symptoms were shown following 39 months of stimulation. The http://dx.doi.org/10.1016/j.parkreldis.2014.09.028 1353-8020/© 2014 Elsevier Ltd. All rights reserved.
patient did not take any medication after surgery. The reduction in tic severity was 92.9% (33 months) and 92.9% (39 months) in the total YGTSS after high- and low-frequency stimulation, respectively. Results of the VTRS were both 4 at the 33- and 39-month follow-up examinations. Relative to the preoperative assessment, the effects of both high- and low-frequency stimulation were stable and similar. Significant effects were shown in the comorbidity and psychological symptoms. The patient's compulsion disappeared. Depressive symptoms were improved. Preoperative and postoperative scores of the patient are presented in Table 1. The main reason for using GPi stimulation in the patient was because previous studies found that GPi DBS was more efficient than thalamic DBS and demonstrated significant therapeutic efficacy on tic-related obsessiveecompulsive disorder. Based on previous studies, it appears that high frequency stimulation may not be necessary to suppress movement disorder symptoms [1,2]. Martinez et al. accidentally found that stimulation at 3 Hz led to resolution of all tics of a TS patient [3]. The low parameter undoubtedly is well tolerated and could increase the therapeutic window between therapeutic effects and side effects. The exact mechanisms of the therapeutic effects of low-frequency stimulation remain unclear. It has been proposed that the minimum frequency necessary for symptom relief may vary across DBS targets and disease states [4]. The minimum effective stimulation frequency may relate to the mean firing rate of the target nucleus [1]. The mean firing rate of GPi neurons in TS was lower than Parkinson's disease and dystonia [5]. This could explain why 65 Hz was efficient in the Table 1 Chronic effects of GPi-DBS. Test
Tic severity (YGTSS) Motor tic severity Phonic tic severity Impairment Total score Tic severity (VTRS) OCD (Y-BOCS) Obsessions Compulsions Total Anxiety (HAS) Depression (HDS)
130 Hz
65 Hz
Baseline
Month 1
Month 3
Month 33
Month 39
16 0 40 56 11
8 0 20 28 7
8 0 0 8 7
4 0 0 4 4
4 0 0 4 4
11 7 18 3 11
0 0 0 2 2
0 0 0 2 0
0 0 0 1 0
0 0 0 1 0
YGTSS, Yale Global Tic Severity Scale. VTRS, Modified Rush Video-Based Tic Rating Scale. Y-BOCS, YaleeBrown Obsessive Compulsive Scale. HAS, Hamilton Anxiety Scale. HDS, Hamilton Depression Scale.
Letter to the Editor / Parkinsonism and Related Disorders 20 (2014) 1438e1439
present study. To our knowledge, this study is the first case to compare the effects of low and high frequency GPi-DBS in a TS patient. Investigating the effects of different frequencies enables rational selection of stimulus parameters and helps to improve the efficacy and tolerability of DBS for the treatment of TS. This case indicates that low-frequency GPi-DBS stimulation may be an optional therapeutic strategy for treating symptoms in a subset of patients with TS. Whether low frequency DBS could be a broadly applicable treatment for TS, or is only effective on individual patients after long-term high frequency stimulation is currently unknown. A deficiency of the report is that no blinding of treatment was used. Future replication studies are needed to confirm the results observed in our patient. Conflict of interest All authors report no conflict of interest. Financial disclosure All the authors have no financial disclosure to claim. References [1] Alterman RL, Shils JL, Miravite J, Tagliati M. Lower stimulation frequency can enhance tolerability and efficacy of pallidal deep brain stimulation for dystonia. Mov Disord 2007;22:366e8.
1439
[2] Chen CC, Lin WY, Chan HL, Tu PH, Lee ST, Lu CS, et al. The impact of lowfrequency stimulation of subthalamic region on self-generated isometric contraction in patients with Parkinson's disease. Exp Brain Res 2013;227: 53e62. [3] Martinez-Fernandez R, Zrinzo L, Aviles-Olmos I, Hariz M, Martinez-Torres I, Joyce E, et al. Deep brain stimulation for Gilles de la Tourette syndrome: a case series targeting subregions of the globus pallidus internus. Mov Disord 2011;26:1922e30. [4] Birdno MJ, Grill WM. Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neurotherapeutics 2008;5:14e25. [5] Tang JK, Moro E, Mahant N, Hutchison WD, Lang AE, Lozano AM, et al. Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson's disease. J Neurophysiol 2007;98: 720e9.
Sheng Dong, Xiaohua Zhang, Jianyu Li, Yongjie Li* Beijing Institute of Functional Neurosurgery, Xuanwu Hospital, Capital Medical University, No. 45, Changchun Street, Xicheng, Beijing 100053, China *
Corresponding author. Tel.: þ86 01083199238; fax: þ86 01083163174. E-mail address: [email protected] (Y. Li). 10 June 2014
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Letter to the Editor
The benefits of low-frequency pallidal deep brain stimulation in a patient with Tourette syndrome Keywords: Tourette syndrome Deep brain stimulation (DBS) Low frequency Globus pallidus internus
Tourette syndrome (TS) is a neuropsychiatric disorder characterized by uncontrolled motor and phonic tics, which is often comorbid with behavioral disorders. Deep brain stimulation (DBS) of the globus pallidus internus (GPi) has been proposed as a therapeutic option for patients with refractory TS. High-frequency (130e185 Hz) stimulation has been conventionally used. Herein, we describe the results of bilateral GPi-DBS in medically intractable TS. Beneficial effects were sustained after the stimulation frequency was reduced from 130 to 65 Hz. A 33-year-old man suffered from marked involuntary neck rotation, shoulder jerks and kicks since the age of 8 years. Coprolalia was present by the age of 9. Comorbidities included repetitive thoughts about a sentence of lyrics and compulsive picking of leaves. The patient was diagnosed with TS according to the criteria of DSM-IV. Tics symptoms seriously hampered his work and quality of life and caused secondary depression. He had been treated with haloperidol, clonidine and risperidone for tics with only mild transient benefit. The medication treatment was not effective and caused significant side effects (sedation, restlessness and blurred vision). After obtaining informed consent, the patient underwent DBS with MRI-guided stereotaxy in March 2011. Electrodes (Medtronic, model 3387; Medtronic, Minneapolis, MN, USA) were implanted bilaterally under local anesthesia and connected to a pulse generator (Kinetra, Medtronic) under general anesthesia. Different stimulation parameters were tried within 1 week after surgery. Stimulation parameters were chosen with a monopolar stimulation (2-, 6-; caseþ), amplitude of 2.8 V, pulse width of 90 ms, and frequency of 130 Hz for both sides. After 33 months (6 months before the final assessment), the stimulation frequency was changed from 130 to 65 Hz. The other parameters remained unchanged. The Yale Global Tic Severity Scale (YGTSS) and the Modified Rush Video-Based Tic Rating Scale (VTRS) were used to evaluate the patient's tics before and after DBS. Compulsion and psychological symptoms were also assessed with the YaleeBrown Obsessive Compulsive Scale (Y-BOCS), Hamilton Anxiety Scale (HAS), and Hamilton Depression Scale (HDS). Postoperatively, no obvious side effects were observed. Electrode positions were determined using MRI. The tips of the electrode were located in the posteroventral GPi. Substantial improvements in tics and comorbid symptoms were shown following 39 months of stimulation. The http://dx.doi.org/10.1016/j.parkreldis.2014.09.028 1353-8020/© 2014 Elsevier Ltd. All rights reserved.
patient did not take any medication after surgery. The reduction in tic severity was 92.9% (33 months) and 92.9% (39 months) in the total YGTSS after high- and low-frequency stimulation, respectively. Results of the VTRS were both 4 at the 33- and 39-month follow-up examinations. Relative to the preoperative assessment, the effects of both high- and low-frequency stimulation were stable and similar. Significant effects were shown in the comorbidity and psychological symptoms. The patient's compulsion disappeared. Depressive symptoms were improved. Preoperative and postoperative scores of the patient are presented in Table 1. The main reason for using GPi stimulation in the patient was because previous studies found that GPi DBS was more efficient than thalamic DBS and demonstrated significant therapeutic efficacy on tic-related obsessiveecompulsive disorder. Based on previous studies, it appears that high frequency stimulation may not be necessary to suppress movement disorder symptoms [1,2]. Martinez et al. accidentally found that stimulation at 3 Hz led to resolution of all tics of a TS patient [3]. The low parameter undoubtedly is well tolerated and could increase the therapeutic window between therapeutic effects and side effects. The exact mechanisms of the therapeutic effects of low-frequency stimulation remain unclear. It has been proposed that the minimum frequency necessary for symptom relief may vary across DBS targets and disease states [4]. The minimum effective stimulation frequency may relate to the mean firing rate of the target nucleus [1]. The mean firing rate of GPi neurons in TS was lower than Parkinson's disease and dystonia [5]. This could explain why 65 Hz was efficient in the Table 1 Chronic effects of GPi-DBS. Test
Tic severity (YGTSS) Motor tic severity Phonic tic severity Impairment Total score Tic severity (VTRS) OCD (Y-BOCS) Obsessions Compulsions Total Anxiety (HAS) Depression (HDS)
130 Hz
65 Hz
Baseline
Month 1
Month 3
Month 33
Month 39
16 0 40 56 11
8 0 20 28 7
8 0 0 8 7
4 0 0 4 4
4 0 0 4 4
11 7 18 3 11
0 0 0 2 2
0 0 0 2 0
0 0 0 1 0
0 0 0 1 0
YGTSS, Yale Global Tic Severity Scale. VTRS, Modified Rush Video-Based Tic Rating Scale. Y-BOCS, YaleeBrown Obsessive Compulsive Scale. HAS, Hamilton Anxiety Scale. HDS, Hamilton Depression Scale.
Letter to the Editor / Parkinsonism and Related Disorders 20 (2014) 1438e1439
present study. To our knowledge, this study is the first case to compare the effects of low and high frequency GPi-DBS in a TS patient. Investigating the effects of different frequencies enables rational selection of stimulus parameters and helps to improve the efficacy and tolerability of DBS for the treatment of TS. This case indicates that low-frequency GPi-DBS stimulation may be an optional therapeutic strategy for treating symptoms in a subset of patients with TS. Whether low frequency DBS could be a broadly applicable treatment for TS, or is only effective on individual patients after long-term high frequency stimulation is currently unknown. A deficiency of the report is that no blinding of treatment was used. Future replication studies are needed to confirm the results observed in our patient. Conflict of interest All authors report no conflict of interest. Financial disclosure All the authors have no financial disclosure to claim. References [1] Alterman RL, Shils JL, Miravite J, Tagliati M. Lower stimulation frequency can enhance tolerability and efficacy of pallidal deep brain stimulation for dystonia. Mov Disord 2007;22:366e8.
1439
[2] Chen CC, Lin WY, Chan HL, Tu PH, Lee ST, Lu CS, et al. The impact of lowfrequency stimulation of subthalamic region on self-generated isometric contraction in patients with Parkinson's disease. Exp Brain Res 2013;227: 53e62. [3] Martinez-Fernandez R, Zrinzo L, Aviles-Olmos I, Hariz M, Martinez-Torres I, Joyce E, et al. Deep brain stimulation for Gilles de la Tourette syndrome: a case series targeting subregions of the globus pallidus internus. Mov Disord 2011;26:1922e30. [4] Birdno MJ, Grill WM. Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neurotherapeutics 2008;5:14e25. [5] Tang JK, Moro E, Mahant N, Hutchison WD, Lang AE, Lozano AM, et al. Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson's disease. J Neurophysiol 2007;98: 720e9.
Sheng Dong, Xiaohua Zhang, Jianyu Li, Yongjie Li* Beijing Institute of Functional Neurosurgery, Xuanwu Hospital, Capital Medical University, No. 45, Changchun Street, Xicheng, Beijing 100053, China *
Corresponding author. Tel.: þ86 01083199238; fax: þ86 01083163174. E-mail address: [email protected] (Y. Li). 10 June 2014
