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Improvement in developmental stuttering following deep brain stimulation for Parkinson's disease
Parkinsonism and Related Disorders 19 (2013) 383–384
Contents lists available at SciVerse ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Letter to the Editor
Improvement in developmental stuttering following deep brain stimulation for Parkinson’s disease Keywords: Parkinson’s disease Deep brain stimulation Stuttering Dysarthria Speech
While bilateral subthalamic nucleus deep brain stimulation (STN-DBS) can dramatically improve the cardinal motor symptoms of Parkinson’s disease (PD), it may also worsen speech, verbal fluency or gait impairment. Developmental stuttering, defined as a disturbance of speech fluency usually appearing before the age of ten, with syllable repetitions, prolongations and blocks, differs from PD dysarthria, although a stuttering-like phenomenon may occasionally occur in PD [1]. The possible impact of STN-DBS for PD on coincident stuttering is unclear, although a worsening of stuttering following STN-DBS has been described in two patients [2,3]. Here we report the case of a PD patient whose developmental stuttering improved after STN-DBS. A right-handed man with a family history of stuttering had stuttered since childhood. Akineto-rigid PD, predominating on the right side, was diagnosed at the age of 46. Fluctuations and dyskinesia occurred following initiation of dopatherapy and persisted despite treatment optimization. Pre-operative evaluation showed a good response to acute levodopa challenge, normal cognition, and no specific abnormalities on brain MRI. The risk-benefit ratio of STN-DBS was discussed with the patient, notably with regard to a potential aggravation of his stuttering. The surgical procedure was finally performed 7 years after PD onset. Under general anesthesia, 2 electrodes (Medtronic, model 3389) were implanted in the STNs with MRI-guided target definition (Siemens, Germany) and micro-electrophysiological recordings. The electrodes were connected to a subcutaneous impulse generator (Medtronic, model Kinetra). Postoperative brain imaging confirmed the location of the electrodes in the right and left STNs (data not shown). Twelve months after surgery the levodopa-equivalent daily dose had been reduced from 2860 mg pre-operatively to 1270 mg (66% reduction). The motor score of the Unified Parkinson’s Disease Scale (UPDRS-III, maximum: 108), assessed while off medication, was respectively 24 and 14 with DBS switched off and on (42% improvement). Parameters included monopolar stimulation with contacts 2 and 6; amplitude 2.1 V on the right side and 2.3 V on the left side; 90 ms pulse width; and frequency 130 Hz. 1353-8020/$ – see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.parkreldis.2012.07.011
The patient’s speech improved following surgery. Three recording sessions of spontaneous speech and reading were performed while the patient was on medication: before surgery, 9 (M9 on-stim) and 13 months following surgery. At 13 months, three conditions were tested: on-stimulation (M13, on-stim), 1 h after stimulation was switched off (M13, off-stim) and 5 min after stimulation was switched on again (M13 on-stim 2). Each recording was transcripted. Stuttering was rated with fluency and efficacy of speaking (percentage of effective syllables among total syllables), and by a modified version of the systematic disfluency analysis (SDA). The SDA weighted score, which takes into account qualitative aspects of disfluencies for 200 efficient syllables, was used to establish six levels of stuttering (from normal (0) to highly severe (5)). Independently, nasality (a feature of the dysarthria) was rated by nasal airflow measurement. As expected, dysarthria worsened in on-stimulation conditions, but stuttering did not. Fluency, efficient fluency and efficacy of speaking improved after surgery (Table 1). The SDA scores (Table 1) indicated “moderate” stuttering before surgery and were “normal” after surgery: this score was 4 times lower on-stimulation than prior to surgery. The SDA scores were also lower off-stimulation than before surgery, but were 2.4 times higher than in on-stimulation conditions. This case shows that bilateral STN-DBS can improve developmental stuttering in advanced PD. Although stimulation substantially improved stuttering in acute testing conditions, stuttering was also improved in off-stimulation conditions relative to preoperative status. This effect might be attributed to a poststimulatory effect during the acute assessment or, to a lesser extent, to the persistence of an STN lesion effect. In addition, the reduction of dopaminergic intakes following STN stimulation might have played a significant role in off-stimulation performance and, more generally, in the observed post-surgical improvement in stuttering. Indeed, increased dopamine activity had been linked to stuttering, anti-dopaminergic treatment is known to reduce stuttering [4] and increasing of disfluencies in “on”’ periods has already been described in patients with both PD and developmental stuttering
384
Letter to the Editor / Parkinsonism and Related Disorders 19 (2013) 383–384
Table 1 Outcome of stuttering after STN-DBS in a patient with Parkinson’s disease. Assessment
Efficient Efficacy of SDA: fluency speech (efficient Weighted (efficient /total syllables) score syllables /min)
Stage of stuttering (0–5) established from SDA’s weighted score
Before surgery M9 on-stim M13 on-stim M13 off-stim M13 on-stim (2)
135 222 220 174 226
Stage Stage Stage Stage Stage
72% 92% 88% 83% 93%
192 42 48 116 55
3: 0: 0: 2: 0:
moderate normal normal mild normal
Financial disclosures Claire Thiriez has received travel funding from Biogen Idec, Orkyn, Novartis and UCB, and organizes a monthly meeting with the financial support of Biogen Idec. Gilles Fénelon serves on a scientific board of Boehringer Ingelheim and Novartis SA, and has received speaker honoraria and travel funding from Boehringer Ingelheim, Novartis SA, Teva, Lundbeck and UCB. Dr Gurruchaga has received travel funding from Medtronic, IRIS and UCB. Stéphane Palfi has received grants, speaker honoraria and travel funding from Oxford Biomedica, Medtronic and Boston Scientific.
See text for a description of the study parameters.
Acknowledgments [5]. However, neither our patient nor the medical staff observed any difference in the intensity of stuttering according to his on/off medication state. Furthermore, the stuttering improved more markedly when stimulation was switched on, suggesting a direct stimulation effect. A chronic and/or acute placebo effect cannot be ruled out, even if both the patient and his physicians expected a worsening rather than an improvement. However, 13 months is considered to be beyond the placebo range. Finally, as emotion is a key factor in stuttering intensity, behavioral motor recovery following STN stimulation may also have contributed to the improvement in stuttering. Speech difficulties associated with PD differ from developmental stuttering, but stuttering-like disfluencies, such as palilalia and logoclonia can also occur during the course of PD [1] .Our patient displayed a typical developmental stuttering, with a familial history of stuttering and occurrence during childhood, which was not worsened by the coincident PD. His speech impairment included disfluencies that can be seen in speech difficulties associated with both PD and developmental stuttering, such as sound repetitions, prolongation or blocks; but it also included features more specific to developmental stuttering, such as reformulations, unfinished words or filling words. All these features improved following DBS. Although the neural basis of stuttering remains unknown, several lines of evidence point to the involvement of the basal ganglia [4]. Indeed, acquired stuttering has been described following basal ganglia lesions [4]; improvements in stuttering have been described after thalamic DBS; and recurrence of childhood stuttering has been reported following PD onset [1]. Cerebral blood flow studies using positron emission tomography (PET) have shown an improvement in cerebellar activation, associated with the disappearance of abnormal superior premotor cortex activation, after stutter rehabilitation. Similar PET findings have been described in parkinsonian patients whose dysarthria improved following STN-DBS [6]. The impact of STN-DBS on stuttering in PD patients has rarely been reported. In one case, developmental stuttering worsened after the onset of PD and further deteriorated after bilateral STN-DBS [2]. Two other patients, one with re-emergent childhood stuttering and the other with acquired stuttering, also worsened after bilateral STN-DBS [3]. The unexpected improvement observed here might have been due to different kind of speech troubles; it might also have been due to a different anatomical location of stimulation and/or to different stimulator settings. However, a significant motor benefit was observed in all reported cases, suggesting appropriate lead locations within the motor STN, and the parameters setting were comparable. In conclusion, since this patient’s developmental stuttering was not systematically worsened by STN-DBS, the presence of developmental stuttering may not be an absolute contraindication for this procedure; however, patients with a history of stuttering need to be advised about the possible benefits and risks of this procedure on their speech fluency.
We thank the patient for his kind cooperation, Cécile Delbende and Clarisse Hillion for their help in assessing the patient, Pierre Brugières for assessing the right positioning of electrodes by the fused computed tomography/MRI, and David Young and Richard Harrington for editorial assistance. References [1] Benke T, Hohenstein C, Poewe W, Butterworth B. Repetitive speech phenomena in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2000;69:319–24. [2] Burghaus L, Hilker R, Thiel A, Galldiks N, Lehnhardt FG, Zaro-Weber O, et al. Deep brain stimulation of the subthalamic nucleus reversibly deteriorates stuttering in advanced Parkinson’s disease. J Neural Transm 2006;113:625–31. [3] Toft M, Dietrichs E. Aggravated stuttering following subthalamic deep brain stimulation in Parkinson’s disease–two cases. BMC Neurol 2011;11:44. [4] Alm PA. Stuttering and the basal ganglia circuits: a critical review of possible relations. J Commun Disord 2004;37:325–69. [5] Anderson JM, Hughes JD, Rothi LJ Gonzalez, Crucian GP, Heilman KM. Developmental stuttering and Parkinson’s disease: the effects of levodopa treatment. J Neurol Neurosurg Psychiatry 1999;66:776–8. [6] Pinto S, Thobois S, Costes N, Le Bars D, Benabid AL, Broussole E, et al. Subthalamic nucleus stimulation and dysarthria in Parkinson’s disease: a PET study. Brain 2004;127(Pt3):602–15.
Claire Thiriez* AP-HP, Service de Neurologie, Groupe Hospitalier Henri Mondor, 51 Avenue du Maréchal de Lattre de Tassigny, 94010 Créteil Cedex, France Université Paris-est Créteil, Faculté de médecine, 94 010 Créteil cedex, France Bernard Roubeau AP-HP, Département d’oto-rhino-laryngologie, Hôpital Tenon, Paris, France Naoufel Ouerchefani, Jean-Marc Gurruchaga AP-HP, Unité de neurochirurgie fonctionnelle, Groupe Hospitalier Henri Mondor, Créteil, France Stéphane Palfi AP-HP, Unité de neurochirurgie fonctionnelle, Groupe Hospitalier Henri Mondor, Créteil, France Université Paris-est Créteil, Faculté de médecine, 94 010 Créteil cedex, France Gilles Fénelon AP-HP, Service de Neurologie, Groupe Hospitalier Henri Mondor, 51 Avenue du Maréchal de Lattre de Tassigny, 94010 Créteil Cedex, France * Corresponding author. Service de Neurologie, Hôpital Henri Mondor, 51 Avenue du Maréchal de Lattre de Tassigny, 94010 Créteil Cedex, France. Tel.: þ33 1 49814301; fax: þ33 1 49812306. E-mail address: [email protected] (C. Thiriez) 16 April 2012
Contents lists available at SciVerse ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Letter to the Editor
Improvement in developmental stuttering following deep brain stimulation for Parkinson’s disease Keywords: Parkinson’s disease Deep brain stimulation Stuttering Dysarthria Speech
While bilateral subthalamic nucleus deep brain stimulation (STN-DBS) can dramatically improve the cardinal motor symptoms of Parkinson’s disease (PD), it may also worsen speech, verbal fluency or gait impairment. Developmental stuttering, defined as a disturbance of speech fluency usually appearing before the age of ten, with syllable repetitions, prolongations and blocks, differs from PD dysarthria, although a stuttering-like phenomenon may occasionally occur in PD [1]. The possible impact of STN-DBS for PD on coincident stuttering is unclear, although a worsening of stuttering following STN-DBS has been described in two patients [2,3]. Here we report the case of a PD patient whose developmental stuttering improved after STN-DBS. A right-handed man with a family history of stuttering had stuttered since childhood. Akineto-rigid PD, predominating on the right side, was diagnosed at the age of 46. Fluctuations and dyskinesia occurred following initiation of dopatherapy and persisted despite treatment optimization. Pre-operative evaluation showed a good response to acute levodopa challenge, normal cognition, and no specific abnormalities on brain MRI. The risk-benefit ratio of STN-DBS was discussed with the patient, notably with regard to a potential aggravation of his stuttering. The surgical procedure was finally performed 7 years after PD onset. Under general anesthesia, 2 electrodes (Medtronic, model 3389) were implanted in the STNs with MRI-guided target definition (Siemens, Germany) and micro-electrophysiological recordings. The electrodes were connected to a subcutaneous impulse generator (Medtronic, model Kinetra). Postoperative brain imaging confirmed the location of the electrodes in the right and left STNs (data not shown). Twelve months after surgery the levodopa-equivalent daily dose had been reduced from 2860 mg pre-operatively to 1270 mg (66% reduction). The motor score of the Unified Parkinson’s Disease Scale (UPDRS-III, maximum: 108), assessed while off medication, was respectively 24 and 14 with DBS switched off and on (42% improvement). Parameters included monopolar stimulation with contacts 2 and 6; amplitude 2.1 V on the right side and 2.3 V on the left side; 90 ms pulse width; and frequency 130 Hz. 1353-8020/$ – see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.parkreldis.2012.07.011
The patient’s speech improved following surgery. Three recording sessions of spontaneous speech and reading were performed while the patient was on medication: before surgery, 9 (M9 on-stim) and 13 months following surgery. At 13 months, three conditions were tested: on-stimulation (M13, on-stim), 1 h after stimulation was switched off (M13, off-stim) and 5 min after stimulation was switched on again (M13 on-stim 2). Each recording was transcripted. Stuttering was rated with fluency and efficacy of speaking (percentage of effective syllables among total syllables), and by a modified version of the systematic disfluency analysis (SDA). The SDA weighted score, which takes into account qualitative aspects of disfluencies for 200 efficient syllables, was used to establish six levels of stuttering (from normal (0) to highly severe (5)). Independently, nasality (a feature of the dysarthria) was rated by nasal airflow measurement. As expected, dysarthria worsened in on-stimulation conditions, but stuttering did not. Fluency, efficient fluency and efficacy of speaking improved after surgery (Table 1). The SDA scores (Table 1) indicated “moderate” stuttering before surgery and were “normal” after surgery: this score was 4 times lower on-stimulation than prior to surgery. The SDA scores were also lower off-stimulation than before surgery, but were 2.4 times higher than in on-stimulation conditions. This case shows that bilateral STN-DBS can improve developmental stuttering in advanced PD. Although stimulation substantially improved stuttering in acute testing conditions, stuttering was also improved in off-stimulation conditions relative to preoperative status. This effect might be attributed to a poststimulatory effect during the acute assessment or, to a lesser extent, to the persistence of an STN lesion effect. In addition, the reduction of dopaminergic intakes following STN stimulation might have played a significant role in off-stimulation performance and, more generally, in the observed post-surgical improvement in stuttering. Indeed, increased dopamine activity had been linked to stuttering, anti-dopaminergic treatment is known to reduce stuttering [4] and increasing of disfluencies in “on”’ periods has already been described in patients with both PD and developmental stuttering
384
Letter to the Editor / Parkinsonism and Related Disorders 19 (2013) 383–384
Table 1 Outcome of stuttering after STN-DBS in a patient with Parkinson’s disease. Assessment
Efficient Efficacy of SDA: fluency speech (efficient Weighted (efficient /total syllables) score syllables /min)
Stage of stuttering (0–5) established from SDA’s weighted score
Before surgery M9 on-stim M13 on-stim M13 off-stim M13 on-stim (2)
135 222 220 174 226
Stage Stage Stage Stage Stage
72% 92% 88% 83% 93%
192 42 48 116 55
3: 0: 0: 2: 0:
moderate normal normal mild normal
Financial disclosures Claire Thiriez has received travel funding from Biogen Idec, Orkyn, Novartis and UCB, and organizes a monthly meeting with the financial support of Biogen Idec. Gilles Fénelon serves on a scientific board of Boehringer Ingelheim and Novartis SA, and has received speaker honoraria and travel funding from Boehringer Ingelheim, Novartis SA, Teva, Lundbeck and UCB. Dr Gurruchaga has received travel funding from Medtronic, IRIS and UCB. Stéphane Palfi has received grants, speaker honoraria and travel funding from Oxford Biomedica, Medtronic and Boston Scientific.
See text for a description of the study parameters.
Acknowledgments [5]. However, neither our patient nor the medical staff observed any difference in the intensity of stuttering according to his on/off medication state. Furthermore, the stuttering improved more markedly when stimulation was switched on, suggesting a direct stimulation effect. A chronic and/or acute placebo effect cannot be ruled out, even if both the patient and his physicians expected a worsening rather than an improvement. However, 13 months is considered to be beyond the placebo range. Finally, as emotion is a key factor in stuttering intensity, behavioral motor recovery following STN stimulation may also have contributed to the improvement in stuttering. Speech difficulties associated with PD differ from developmental stuttering, but stuttering-like disfluencies, such as palilalia and logoclonia can also occur during the course of PD [1] .Our patient displayed a typical developmental stuttering, with a familial history of stuttering and occurrence during childhood, which was not worsened by the coincident PD. His speech impairment included disfluencies that can be seen in speech difficulties associated with both PD and developmental stuttering, such as sound repetitions, prolongation or blocks; but it also included features more specific to developmental stuttering, such as reformulations, unfinished words or filling words. All these features improved following DBS. Although the neural basis of stuttering remains unknown, several lines of evidence point to the involvement of the basal ganglia [4]. Indeed, acquired stuttering has been described following basal ganglia lesions [4]; improvements in stuttering have been described after thalamic DBS; and recurrence of childhood stuttering has been reported following PD onset [1]. Cerebral blood flow studies using positron emission tomography (PET) have shown an improvement in cerebellar activation, associated with the disappearance of abnormal superior premotor cortex activation, after stutter rehabilitation. Similar PET findings have been described in parkinsonian patients whose dysarthria improved following STN-DBS [6]. The impact of STN-DBS on stuttering in PD patients has rarely been reported. In one case, developmental stuttering worsened after the onset of PD and further deteriorated after bilateral STN-DBS [2]. Two other patients, one with re-emergent childhood stuttering and the other with acquired stuttering, also worsened after bilateral STN-DBS [3]. The unexpected improvement observed here might have been due to different kind of speech troubles; it might also have been due to a different anatomical location of stimulation and/or to different stimulator settings. However, a significant motor benefit was observed in all reported cases, suggesting appropriate lead locations within the motor STN, and the parameters setting were comparable. In conclusion, since this patient’s developmental stuttering was not systematically worsened by STN-DBS, the presence of developmental stuttering may not be an absolute contraindication for this procedure; however, patients with a history of stuttering need to be advised about the possible benefits and risks of this procedure on their speech fluency.
We thank the patient for his kind cooperation, Cécile Delbende and Clarisse Hillion for their help in assessing the patient, Pierre Brugières for assessing the right positioning of electrodes by the fused computed tomography/MRI, and David Young and Richard Harrington for editorial assistance. References [1] Benke T, Hohenstein C, Poewe W, Butterworth B. Repetitive speech phenomena in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2000;69:319–24. [2] Burghaus L, Hilker R, Thiel A, Galldiks N, Lehnhardt FG, Zaro-Weber O, et al. Deep brain stimulation of the subthalamic nucleus reversibly deteriorates stuttering in advanced Parkinson’s disease. J Neural Transm 2006;113:625–31. [3] Toft M, Dietrichs E. Aggravated stuttering following subthalamic deep brain stimulation in Parkinson’s disease–two cases. BMC Neurol 2011;11:44. [4] Alm PA. Stuttering and the basal ganglia circuits: a critical review of possible relations. J Commun Disord 2004;37:325–69. [5] Anderson JM, Hughes JD, Rothi LJ Gonzalez, Crucian GP, Heilman KM. Developmental stuttering and Parkinson’s disease: the effects of levodopa treatment. J Neurol Neurosurg Psychiatry 1999;66:776–8. [6] Pinto S, Thobois S, Costes N, Le Bars D, Benabid AL, Broussole E, et al. Subthalamic nucleus stimulation and dysarthria in Parkinson’s disease: a PET study. Brain 2004;127(Pt3):602–15.
Claire Thiriez* AP-HP, Service de Neurologie, Groupe Hospitalier Henri Mondor, 51 Avenue du Maréchal de Lattre de Tassigny, 94010 Créteil Cedex, France Université Paris-est Créteil, Faculté de médecine, 94 010 Créteil cedex, France Bernard Roubeau AP-HP, Département d’oto-rhino-laryngologie, Hôpital Tenon, Paris, France Naoufel Ouerchefani, Jean-Marc Gurruchaga AP-HP, Unité de neurochirurgie fonctionnelle, Groupe Hospitalier Henri Mondor, Créteil, France Stéphane Palfi AP-HP, Unité de neurochirurgie fonctionnelle, Groupe Hospitalier Henri Mondor, Créteil, France Université Paris-est Créteil, Faculté de médecine, 94 010 Créteil cedex, France Gilles Fénelon AP-HP, Service de Neurologie, Groupe Hospitalier Henri Mondor, 51 Avenue du Maréchal de Lattre de Tassigny, 94010 Créteil Cedex, France * Corresponding author. Service de Neurologie, Hôpital Henri Mondor, 51 Avenue du Maréchal de Lattre de Tassigny, 94010 Créteil Cedex, France. Tel.: þ33 1 49814301; fax: þ33 1 49812306. E-mail address: [email protected] (C. Thiriez) 16 April 2012