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Case report
Combined deep brain stimulation and thalamotomy for tremor-dominant Parkinson’s disease Akimaro Kojoh a, Rei Enatsu a,⇑, Mayumi Kitagawa b, Takeshi Mikami a, Ayaka Sasagawa a, Tomoyoshi Kuribara a, Tsukasa Hirano a, Masayasu Arihara a, Nobuhiro Mikuni a a b
Department of Neurosurgery, Sapporo Medical University School of Medicine, Sapporo, Japan Department of Neurology, Sapporo Teishinkai Hospital, Sapporo, Japan
a r t i c l e
i n f o
Article history: Received 16 December 2019 Accepted 10 February 2020 Available online xxxx Keywords: Deep brain stimulation Thalamotomy Tremor Parkinson’s disease, tolerance
a b s t r a c t Although deep brain stimulation (DBS) is an established treatment for Parkinson’s disease, the long-term suppression of tremor is still a challenging issue. We report two patients with tremor-dominant Parkinson’s disease (PD) treated with unilateral thalamotomy of the ventralis intermedius nucleus (Vim) combined with the subthalamic nucleus (STN)-DBS or the posterior subthalamic area (PSA)-DBS. One year after the surgery, thalamotomy of the area from the Vim to the PSA showed improvement not only in tremor but also in rigidity and akinesia. PSA- or STN-DBS with low intensity stimulation eliminated residual PD symptoms. Combined DBS and thalamotomy may provide long-term improvement of the majority of PD symptoms using lower therapeutic stimulation voltages. Ó 2020 Published by Elsevier Ltd.
1. Introduction
2. Case reports
Deep brain stimulation (DBS) targeting the subthalamic nucleus (STN), globus pallidus internas (GPi), the ventral intermediate nucleus of the thalamus (Vim), the caudal zona incerta (cZI), and posterior subthalamic area (PSA) has been reported to be effective for severe tremor in patients with Parkinson’s disease (PD) [1–5]. DBS has the benefit of being able to program adjustments to minimize stimulation-related complications; however, long-term improvement of tremor does not always persist [6]. Progressively increasing stimulation intensity may cause stimulation-induced side effects. Thalamotomy is a historical approach to ameliorate medication-refractory tremor. Although previous studies have reported residual tremor, recurrence of tremor, and surgical complications after thalamotomy [2], a recent study found that long-term effective and safe tremor control could be achieved by superselective thalamotomy [7]. A combination of thalamotomy and DBS may provide long-term improvement without stimulation-induced side effects. We here report the effectiveness of STN-DBS or PSA-DBS combined with thalamotomy in two PD patients with severe tremor.
2.1. Case 1
⇑ Corresponding author at: Department of Neurosurgery, Sapporo Medical University, South 1, West 16, Chuo-ku, Sapporo 060-8543, Japan. E-mail address:
[email protected] (R. Enatsu).
A 74-year-old woman with a 1-year history of tremor-dominant PD was referred to our department for surgical treatment. She had been treated with L-dopa/carbidopa, dopamine agonist/ropinirole, and zonisamide, but right hand tremor was medication refractory and affected her daily life. Preoperatively, her Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) motor score (part 3) and tremor subscore (3.15–3.17) during OFF-medication were 72 and 8, respectively (Table 1). Left-sided PSA–DBS implantation (10 mm lateral, 6 mm posterior, and 4 mm inferior to the mid-commissure point) combined with Vim thalamtomy (14 mm lateral, 5 mm posterior, and on the vertical plane to the mid-commissure point) was planned using the MRI/ CT image fusion software, BrainLAB system (Brainlab, Feldkirchen, Germany) (Fig. 1a). After microrecording through the tract that Vim would target under an awake state, intraoperative stimulation was performed to confirm the therapeutic effects and to check for adverse responses. Thermal coagulation (70 °C for 60 s) was performed using a monopolar radiofrequency probe. Tremor and rigidity on the right side of the body disappeared during coagulation, and no adverse event occurred. Thereafter, DBS electrode 3389 (Medtronic, Minneapolis, MN, USA) was inserted in the left PSA. On postoperative MRI, coagulation changes and edema
https://doi.org/10.1016/j.jocn.2020.02.014 0967-5868/Ó 2020 Published by Elsevier Ltd.
Please cite this article as: A. Kojoh, R. Enatsu, M. Kitagawa et al., Combined deep brain stimulation and thalamotomy for tremor-dominant Parkinson’s disease, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.02.014
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Table 1 Contralateral MDS-UPDRS motor subscores (part 3) during medicaiton off. Case 1 Preope
Rigidity (3.3) Akinesia (3.4–3.8) Postural tremor (3.15) Action tremor (3.16) Resting tremor (3.17) UPDRS part 3 total
6 15 3 1 4 72
Case 2 1 year after
Preope
DBS off
DBS on
3 8 1 2 0 59
1 0 0 2 0 30
formation spread from the thalamus to the PSA, and a DBS electrode was implanted in the PSA (Fig. 1b). Postoperatively, rightsided tremor disappeared and rigidity and akinesia improved without DBS. Ten days after the surgery, DBS was used for further improvement. One year after the surgery, remarkable improvement of tremor, rigidity and akinesia was observed during OFF-DBS/OFF-medication (Table 1). PSA-DBS at low-intensity stimulation (130 Hz, 60 ls, and 1.0 V) further improved postural tremor, rigidity, and akinesia. 2.2. Case 2 A 59-year-old man with a 5-year history of PD exhibited from medication-refractory left-hand tremor, and requested neurosurgical treatment to reduce hand tremor. Right STN-DBS (12 mm lateral, 3 mm posterior, and 4 mm inferior to the mid-commissure point) and right Vim thalamotomy (13 mm lateral, 5 mm posterior, and on the vertical plane to the mid-commissure point) were planned (Fig. 1c). Tremor and rigidity on the left side of the body disappeared during coagulation, and no adverse event was observed. A DBS electrode was implanted in the right STN. Postoperative MRI showed a coagulation/edema-like signal that spread from the thalamus to the PSA. The size of the edema-like signal in the PSA was thin and small (Fig. 1d). One month after surgery, left-hand tremor recurred. STN-DBS (130 Hz, 60 ls, and 1.0 V) alleviated tremor; however, this improvement faded within a month. On-demand use of DBS and DBS with cycle mode (10 s on, 1 s off) were useful to maintain the stimulation effect of DBS. One year after surgery, improvement in rigidity and akinesia on the left side was observed during OFF-DBS/OFF-medication, but the severity of tremor returned to the preoperative level. STN-DBS at relatively low-intensity stimulation (130 Hz, 60 ls, and 1.6 V) alleviated action, postural, and resting tremor (Table 1).
2 6 3 2 6 31
1 year after DBS off
DBS on
0 0 2 2 5 13
0 0 0 0 1 3
tremor at low-intensity stimulation, for one year. Previous studies have reported the effectiveness of PSA-DBS on akinesia [4]. Therefore, coagulation spread from the Vim to the PSA may be associated with long-term improvement in akinesia. In Case 2, the smaller size of the coagulated lesion in the PSA may be related to tremor recurrence and early tolerance to DBS. The PSA is located anterolaterally of the red nucleus, posteromedial of the STN, and anteromedially of the posterior limb of the internal capsule. Because some previous studies have reported severe complications, such as choreo-ballistic movement following subthalamotomy [8,9], DBS may be the preferred surgical procedure for targeting the PSA. Both PSA-DBS and STN-DBS alleviated residual and recurrent PD symptoms after thalamotomy; however, Case 2 developed habituation to STN-DBS. Previous studies have reported the usefulness of a DBS holiday or on-demand DBS to prevent habituation to DBS in patients with essential tremor [10,11]. In Case 2, DBS with on-demand and with cycle mode (10 s on, 1 s off) was useful to maintain the stimulation effect of STN-DBS. The new treatment system based on real-time behavioral assesment would contribute long-term improvement [12]. For combined DBS and thalamotomy, several technical issues should be noted. First, DBS electrode placement may be distorted by tracts from a prior thalamotomy. Second, microelectrode recordings may be influenced by coagulation and edema induced by prior thalamotomy. Third, electrode placement through coagulated tissues may cause hemorrhagic complications. Despite several limitations, we suggest that DBS combined with Vim thalamotomy is a useful technique for stable control of tremor in patients who are more likely to develop tolerance to DBS. Declaration of Competing Interest
3. Discussion In both our cases, combined thalamotomy and DBS improved the majority of PD symptoms, including severe
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
" Fig. 1. (a) Preoperative planning of case 1. Two targets were set using MRI/CT imaging fusion software (Left Vim: 14 mm lateral, 5 mm posterior, and on the vertical plane to the mid-commissure point; Left PSA: 10 mm lateral, 6 mm posterior, and 4 mm inferior to the mid-commissure point). (b) Postoperative MRI showing the inserted electrode and coagulated lesion. (c) Preoperative planning of case 2 (Right Vim: 13 mm lateral, 5 mm posterior, and on the vertical plane to the mid-commissure point; Right STN: 12 mm lateral, 3 mm posterior, and 4 mm inferior to the mid-commissure point). (d) Postoperative MRI showing the inserted electrode, stimulation site and coagulated lesion. DBS: deep brain stimulation, GP: globus pallidus, IC: internal capsule, PSA: posterior subthalamic area, RN: red nucleus, STN: subthalamic nucleus, Vim: the ventral intermediate nucleus of the thalamus, Postop: postoperative, Preop: preoperative.
Please cite this article as: A. Kojoh, R. Enatsu, M. Kitagawa et al., Combined deep brain stimulation and thalamotomy for tremor-dominant Parkinson’s disease, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.02.014
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Please cite this article as: A. Kojoh, R. Enatsu, M. Kitagawa et al., Combined deep brain stimulation and thalamotomy for tremor-dominant Parkinson’s disease, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.02.014
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Please cite this article as: A. Kojoh, R. Enatsu, M. Kitagawa et al., Combined deep brain stimulation and thalamotomy for tremor-dominant Parkinson’s disease, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.02.014