Combination of thalamic Vim stimulation and GPi pallidotomy synergistically abolishes Holmes’ tremor
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《神经病学神经外科学杂志》
Department of Neurosurgery, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan
Correspondence to:
S Goto MD PhD
Department of Neurosurgery, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan; sgoto@kaiju.medic.kumamoto-u.ac.jp
Keywords: Holmes’ tremor; deep brain stimulation; pallidotomy
The recent report of Kim et al,1 who demonstrated that stereotactic surgical ablation of the thalamic nucleus ventrointermedius (Vim) markedly improved Holmes’ tremor in a patient with midbrain tumour, corroborated our earlier findings.2 In their patient, Vim thalamotomy alleviated tremor in both the distal and proximal segments of the upper extremity.1 However, controversy continues to surround the advisability of using this procedure for proximal tremors because the placement of larger lesions carries increased risks and the somatotopy of the proximal or truncal muscles remains obscure in the human Vim.3–5 Here we present a patient with a pontine haemorrhage in whom the combination of thalamic Vim deep brain stimulation (DBS) and globus pallidus internus (GPi) pallidotomy abolished Holmes’ tremor.
This 53 year old right-handed man with a history of essential hypertension suddenly developed right hemiparesis and cerebellar ataxia in February 2000. He was admitted to a hospital where radiological examinations showed a left upper brainstem haemorrhage (fig 1A). His neurological state gradually improved. However, in October 2001 a coarse, slowly progressive tremor arose in his right upper extremity. It was severely disabling and he could not use his right arm. He was admitted to our hospital in December 2001.
Figure 1 (A) Computed tomography (CT) scan showing a haematoma in the pontine tegmentum. (B, C) Axial views of T2-weighted magnetic resonance images at chronic stage (22 months after onset) demonstrating a haemosiderin ring around the lesion in the pontine tegmentum (B, arrow) and a high signal intensity area in the left inferior olivary nucleus indicating hypertrophic olivary degeneration (C). (D, E) Location of the electrode superimposed on the frontal (D) and lateral (E) view of a selective third ventriculography. The target point is indicated by the asterisk. (F) CT scan demonstrating the coagulative lesion made by the left GPi pallidotomy (arrow). The CT scan was carried out 10 days after pallidotomy. AC, anterior commissure; PC, posterior commissure; ML, midline.
On admission, he was alert and oriented. His speech was mildly dysarthric and slurred. There was palatal tremor. Mild hemiparesis with increased stretch reflexes and Babinski sign were noted on the right side. There were mild deficits of position, vibratory sense, and superficial sensation of light touch and pain in his right upper and lower extremities. Dysmetria was more pronounced on the right. Because of severe truncal and gait ataxia, he could not remain upright without support; he was unable to walk even with assistance. There was coarse and severe tremor in the right upper extremity. It persisted at rest and its amplitude increased during maintenance of a fixed posture and intentional voluntary movements. It rendered the right arm useless and prevented him from feeding and caring for himself. He was exhausted because of the severe tremor that persisted throughout his waking hours. Surface electromyograms showed rhythmic grouping discharges of 3.6 Hz in the right forearm muscles. His preoperative score on the Tremor Rating Scale (TRS)6 for his right upper extremity (Part A, score 5) was 11. Magnetic resonance imaging (MRI) study (December 2001) showed a haemosiderin ring around the lesion in the left pontine tegmentum (fig 1B). On T2-weighted images, a high signal lesion was seen in the left inferior olive, as consistent with the hypertrophic olivary degeneration (fig 1C). As sequential pharmacotherapy using clonazepam (3x0.5 mg/day) and benserazide/levodopa (3x25/100 mg per day) was only slightly effective, he was referred for surgery. Prior informed consent was obtained from the patient and his family.
In January 2002, a quadripolar DBS electrode (Model 3387; Medtronic Inc., Minneapolis, MN, USA) was implanted in the left thalamic Vim nucleus with the aid of MRI, third ventriculography, and microelectrode guidance, as previously described.2 The optimal target was determined to be 7 mm posterior and 14.5 mm lateral to the midpoint of the anterior to posterior commissure (AC–PC) line, and on the AC–PC line. The most ventral contact was placed precisely on the target point (fig 1D, E). As stimulation tests, performed for 5 days, confirmed the beneficial effects of DBS, a programmable pulse generator (Soletra, Model 7426; Medtronic Inc.) was implanted. His postoperative course was uneventful.
After extensive trials, stimulation was carried out using contacts 0 and 1 (fig 1D, E). The optimal stimulation parameters were determined to be 160 Hz frequency, 90 μsec pulse width, and 2.9 V and 3.4 V amplitude at the first and final session. Stimulation with amplitude exceeding 3.4 V induced unpleasant electrical paraesthesia on the right side of his face and right upper extremity. Under optimal stimulation, the tremor was markedly alleviated in the distal part of his right arm: the TRS score for his upper extremity tremor (Part A, score 5) was reduced to 6. Upon discontinuation of stimulation, the distal tremor reappeared immediately and returned to the preoperative state. The proximal tremor of his right arm was unresolved.
After discharge, he visited our outpatient department once a month. In January 2003, he complained of gradual worsening of the remaining proximal tremor; the distal tremor remained completely suppressed by thalamic Vim stimulation. We discussed GPi pallidotomy5 and obtained informed consent prior to the procedure.
In April 2003, left GPi pallidotomy was performed according to the method we described previously.7 The optimal target for the posteroventral part of the GPi was determined to be 2 mm anterior and 20 mm lateral to the midpoint of the AC–PC line, and 1 mm dorsal to the floor of the third ventricle. After creating a test lesion (42 °C, 60 sec), a permanent anatomical lesion was made by heating the electrode tip to 72 °C for up to 70 sec. The electrode was moved in 2 mm increments in the medial, lateral, and dorsal directions, and the lesioning process was repeated to increase the overall size of the lesion (fig 1F). GPi pallidotomy completely abolished his proximal tremor. However, it produced only a small effect on his distal tremor and discontinuation of Vim stimulation resulted in its reappearance at almost the preoperative level. Without stimulation, the TRS score for his upper extremity tremor (Part A, score 5) was 5. The combination of Vim stimulation and GPi pallidotomy had synergistic effects in abolishing Holmes’ tremor in our patient. The therapeutic benefits remain unchanged at the time of writing and the TRS score for his upper extremity tremor (Part A, score 5) is 0. His palatal tremor did not respond to Vim stimulation and pallidotomy and remains unresolved.
Stereotactic Vim surgery, either thalamotomy or thalamic stimulation, is a mainstay in the surgical treatment of parkinsonian or essential tremors.8 Its efficacy in tremor suppression is superior to that of pallidotomy in parkinsonian patients. However, as evidenced by our case, it does not always produce satisfactory results in patients with Holmes’ tremors, particularly with respect to their proximal tremors. The basal ganglia outflow pathway from the GPi exerts a direct influence on not only the thalamus but also the brainstem motor centres such as the pedunculopontine nucleus related to the mesencephalic tegmental field that controls the axial and proximal appendicular musculature via the descending reticulospinal tract. Therefore, unlike thalamic surgery, which interrupts the thalamocortical output that controls distal appendicular musculature via descending corticospinal and corticobulbar tracts, GPi pallidal surgery influences the control of otherwise inaccessible axial and proximal muscles. This may be the reason why GPi pallidotomy produced a marked alleviation of the proximal tremor in our patient. Due to the limited efficacy of thalamic Vim surgery on proximal tremors, the use of other or additional surgeries with greater effects—for example, pallidal surgery5 or subthalamic area stimulation,9 should be considered for the treatment of Holmes’ tremor.
References
Kim M-C , Son BC, Miyagi Y, et al. Vim thalamotomy for Holmes’ tremor secondary to midbrain tumour. J Neurol Neurosurg Psychiatry 2002;73:453–5.
Kudo M , Goto S, Nishikawa S, et al. Bilateral thalamic stimulation for Holmes’ tremor caused by unilateral brainstem lesion. Mov Disord 2001;16:170–4.
Hirai T , Miyazaki M, Nakajima H, et al. The correlation between tremor characteristics and the predicted volume of effective lesions in stereotaxic nucleus ventralis intermedius thalamotomy. Brain 1983;106:1001–18.
Nguyen JP, Degas JD. Thalamic stimulation and proximal tremor: a specific target in the nucleus ventrointermedius thalami. Arch Neurol 1993;50:498–500.
Miyagi Y , Shima F, Ishido K, et al. Posteroventral pallidotomy for midbrain tremor after a pontine hemorrhage. J Neurosurg 1999;91:885–8.
Fahn S , Tolosa E, Marin C. Clinical rating scale for tremor. In: Jankovic J, Tolosa E, eds. Parkinson’s Disease and Movement Disorders. Baltimore, Munich: Urban & Schwarzenberg, 1988:225–34.
Goto S , Hamasaki T, Nishikawa S, et al. Temporal sequence of response to unilateral GPi pallidotomy of motor symptoms in Parkinson’s disease. Stereotact Funct Neurosurg 2000;75:160–6.
Schuurman PR, Bosch DA, Bossuyt PM, et al. A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N Engl J Med 2000;342:461–8.
Kitagawa M , Murata J, Kikuchi S, et al. Deep brain stimulation of subthalamic area for severe proximal tremor. Neurology 2000;55:114–16.(S Goto and K Yamada)
Correspondence to:
S Goto MD PhD
Department of Neurosurgery, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan; sgoto@kaiju.medic.kumamoto-u.ac.jp
Keywords: Holmes’ tremor; deep brain stimulation; pallidotomy
The recent report of Kim et al,1 who demonstrated that stereotactic surgical ablation of the thalamic nucleus ventrointermedius (Vim) markedly improved Holmes’ tremor in a patient with midbrain tumour, corroborated our earlier findings.2 In their patient, Vim thalamotomy alleviated tremor in both the distal and proximal segments of the upper extremity.1 However, controversy continues to surround the advisability of using this procedure for proximal tremors because the placement of larger lesions carries increased risks and the somatotopy of the proximal or truncal muscles remains obscure in the human Vim.3–5 Here we present a patient with a pontine haemorrhage in whom the combination of thalamic Vim deep brain stimulation (DBS) and globus pallidus internus (GPi) pallidotomy abolished Holmes’ tremor.
This 53 year old right-handed man with a history of essential hypertension suddenly developed right hemiparesis and cerebellar ataxia in February 2000. He was admitted to a hospital where radiological examinations showed a left upper brainstem haemorrhage (fig 1A). His neurological state gradually improved. However, in October 2001 a coarse, slowly progressive tremor arose in his right upper extremity. It was severely disabling and he could not use his right arm. He was admitted to our hospital in December 2001.
Figure 1 (A) Computed tomography (CT) scan showing a haematoma in the pontine tegmentum. (B, C) Axial views of T2-weighted magnetic resonance images at chronic stage (22 months after onset) demonstrating a haemosiderin ring around the lesion in the pontine tegmentum (B, arrow) and a high signal intensity area in the left inferior olivary nucleus indicating hypertrophic olivary degeneration (C). (D, E) Location of the electrode superimposed on the frontal (D) and lateral (E) view of a selective third ventriculography. The target point is indicated by the asterisk. (F) CT scan demonstrating the coagulative lesion made by the left GPi pallidotomy (arrow). The CT scan was carried out 10 days after pallidotomy. AC, anterior commissure; PC, posterior commissure; ML, midline.
On admission, he was alert and oriented. His speech was mildly dysarthric and slurred. There was palatal tremor. Mild hemiparesis with increased stretch reflexes and Babinski sign were noted on the right side. There were mild deficits of position, vibratory sense, and superficial sensation of light touch and pain in his right upper and lower extremities. Dysmetria was more pronounced on the right. Because of severe truncal and gait ataxia, he could not remain upright without support; he was unable to walk even with assistance. There was coarse and severe tremor in the right upper extremity. It persisted at rest and its amplitude increased during maintenance of a fixed posture and intentional voluntary movements. It rendered the right arm useless and prevented him from feeding and caring for himself. He was exhausted because of the severe tremor that persisted throughout his waking hours. Surface electromyograms showed rhythmic grouping discharges of 3.6 Hz in the right forearm muscles. His preoperative score on the Tremor Rating Scale (TRS)6 for his right upper extremity (Part A, score 5) was 11. Magnetic resonance imaging (MRI) study (December 2001) showed a haemosiderin ring around the lesion in the left pontine tegmentum (fig 1B). On T2-weighted images, a high signal lesion was seen in the left inferior olive, as consistent with the hypertrophic olivary degeneration (fig 1C). As sequential pharmacotherapy using clonazepam (3x0.5 mg/day) and benserazide/levodopa (3x25/100 mg per day) was only slightly effective, he was referred for surgery. Prior informed consent was obtained from the patient and his family.
In January 2002, a quadripolar DBS electrode (Model 3387; Medtronic Inc., Minneapolis, MN, USA) was implanted in the left thalamic Vim nucleus with the aid of MRI, third ventriculography, and microelectrode guidance, as previously described.2 The optimal target was determined to be 7 mm posterior and 14.5 mm lateral to the midpoint of the anterior to posterior commissure (AC–PC) line, and on the AC–PC line. The most ventral contact was placed precisely on the target point (fig 1D, E). As stimulation tests, performed for 5 days, confirmed the beneficial effects of DBS, a programmable pulse generator (Soletra, Model 7426; Medtronic Inc.) was implanted. His postoperative course was uneventful.
After extensive trials, stimulation was carried out using contacts 0 and 1 (fig 1D, E). The optimal stimulation parameters were determined to be 160 Hz frequency, 90 μsec pulse width, and 2.9 V and 3.4 V amplitude at the first and final session. Stimulation with amplitude exceeding 3.4 V induced unpleasant electrical paraesthesia on the right side of his face and right upper extremity. Under optimal stimulation, the tremor was markedly alleviated in the distal part of his right arm: the TRS score for his upper extremity tremor (Part A, score 5) was reduced to 6. Upon discontinuation of stimulation, the distal tremor reappeared immediately and returned to the preoperative state. The proximal tremor of his right arm was unresolved.
After discharge, he visited our outpatient department once a month. In January 2003, he complained of gradual worsening of the remaining proximal tremor; the distal tremor remained completely suppressed by thalamic Vim stimulation. We discussed GPi pallidotomy5 and obtained informed consent prior to the procedure.
In April 2003, left GPi pallidotomy was performed according to the method we described previously.7 The optimal target for the posteroventral part of the GPi was determined to be 2 mm anterior and 20 mm lateral to the midpoint of the AC–PC line, and 1 mm dorsal to the floor of the third ventricle. After creating a test lesion (42 °C, 60 sec), a permanent anatomical lesion was made by heating the electrode tip to 72 °C for up to 70 sec. The electrode was moved in 2 mm increments in the medial, lateral, and dorsal directions, and the lesioning process was repeated to increase the overall size of the lesion (fig 1F). GPi pallidotomy completely abolished his proximal tremor. However, it produced only a small effect on his distal tremor and discontinuation of Vim stimulation resulted in its reappearance at almost the preoperative level. Without stimulation, the TRS score for his upper extremity tremor (Part A, score 5) was 5. The combination of Vim stimulation and GPi pallidotomy had synergistic effects in abolishing Holmes’ tremor in our patient. The therapeutic benefits remain unchanged at the time of writing and the TRS score for his upper extremity tremor (Part A, score 5) is 0. His palatal tremor did not respond to Vim stimulation and pallidotomy and remains unresolved.
Stereotactic Vim surgery, either thalamotomy or thalamic stimulation, is a mainstay in the surgical treatment of parkinsonian or essential tremors.8 Its efficacy in tremor suppression is superior to that of pallidotomy in parkinsonian patients. However, as evidenced by our case, it does not always produce satisfactory results in patients with Holmes’ tremors, particularly with respect to their proximal tremors. The basal ganglia outflow pathway from the GPi exerts a direct influence on not only the thalamus but also the brainstem motor centres such as the pedunculopontine nucleus related to the mesencephalic tegmental field that controls the axial and proximal appendicular musculature via the descending reticulospinal tract. Therefore, unlike thalamic surgery, which interrupts the thalamocortical output that controls distal appendicular musculature via descending corticospinal and corticobulbar tracts, GPi pallidal surgery influences the control of otherwise inaccessible axial and proximal muscles. This may be the reason why GPi pallidotomy produced a marked alleviation of the proximal tremor in our patient. Due to the limited efficacy of thalamic Vim surgery on proximal tremors, the use of other or additional surgeries with greater effects—for example, pallidal surgery5 or subthalamic area stimulation,9 should be considered for the treatment of Holmes’ tremor.
References
Kim M-C , Son BC, Miyagi Y, et al. Vim thalamotomy for Holmes’ tremor secondary to midbrain tumour. J Neurol Neurosurg Psychiatry 2002;73:453–5.
Kudo M , Goto S, Nishikawa S, et al. Bilateral thalamic stimulation for Holmes’ tremor caused by unilateral brainstem lesion. Mov Disord 2001;16:170–4.
Hirai T , Miyazaki M, Nakajima H, et al. The correlation between tremor characteristics and the predicted volume of effective lesions in stereotaxic nucleus ventralis intermedius thalamotomy. Brain 1983;106:1001–18.
Nguyen JP, Degas JD. Thalamic stimulation and proximal tremor: a specific target in the nucleus ventrointermedius thalami. Arch Neurol 1993;50:498–500.
Miyagi Y , Shima F, Ishido K, et al. Posteroventral pallidotomy for midbrain tremor after a pontine hemorrhage. J Neurosurg 1999;91:885–8.
Fahn S , Tolosa E, Marin C. Clinical rating scale for tremor. In: Jankovic J, Tolosa E, eds. Parkinson’s Disease and Movement Disorders. Baltimore, Munich: Urban & Schwarzenberg, 1988:225–34.
Goto S , Hamasaki T, Nishikawa S, et al. Temporal sequence of response to unilateral GPi pallidotomy of motor symptoms in Parkinson’s disease. Stereotact Funct Neurosurg 2000;75:160–6.
Schuurman PR, Bosch DA, Bossuyt PM, et al. A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N Engl J Med 2000;342:461–8.
Kitagawa M , Murata J, Kikuchi S, et al. Deep brain stimulation of subthalamic area for severe proximal tremor. Neurology 2000;55:114–16.(S Goto and K Yamada)