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Tremor is a common movement disorder that can have disabling effects on daily living, impact em-ployment, and reduce quality of life.7 Medical

management strategies are helpful for some patients, but many individuals either become unresponsive to medica-tion or derive no benefit from it. For decades, the VIM nucleus has been ablated to improve contralateral tremor, first using RFT and more recently using DBS, to provide effective and sustained control of essential or parkinso-

nian tremor.3–5 In the early years, target selection was based on indirect visualization of landmarks for the VIM using air or contrast encephalography. After 1980, many centers switched to using CT scanning to improve target selection. However, MRI has supplanted such techniques because of its enhanced contrast and spatial depiction.

Initial ablation of the target nucleus was performed using cryosurgery, hot wax, and agents such as phenol. Such exploratory methods evolved to the more wide-spread adoption of stereotactic RFT to create a controlled heat lesion of predictable volume. A trend to manage such patients with DBS emerged more than 15 years ago; more recently, the use of focused ultrasound has been promoted to create a heat lesion of the same target.

As the population ages, patients with tremor in whom

Gamma Knife thalamotomy for tremor in the magnetic resonance imaging era

Clinical articleAli KooshKAbAdi, M.d.,1 l. dAde lunsford, M.d.,1 dAniel ToneTTi, M.s.,1 John C. fliCKinger, M.d.,1,2 And douglAs KondziolKA, M.d., M.sC.1,2

Departments of 1Neurological Surgery and 2Radiation Oncology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania

Object. The surgical management of disabling tremor has gained renewed vigor with the availability of deep brain stimulation. However, in the face of an aging population of patients with increasing surgical comorbidities, noninvasive approaches for tremor management are needed. The authors’ purpose was to study the technique and results of stereotactic radiosurgery performed in the era of MRI targeting.

Methods. The authors evaluated outcomes in 86 patients (mean age 71 years; number of procedures 88) who underwent a unilateral Gamma Knife thalamotomy (GKT) for tremor during a 15-year period that spanned the era of MRI-based target selection (1996–2011). Symptoms were related to essential tremor in 48 patients (19 age ≥ 80 years and 3 age ≥ 90 years), Parkinson disease in 27 patients (11 age ≥ 80 years [1 patient underwent bilateral pro-cedures]), and multiple sclerosis in 11 patients (1 patient underwent bilateral procedures). A single 4-mm isocenter was used to deliver a maximum dose of 140 Gy to the posterior-inferior region of the nucleus ventralis intermedius. The Fahn-Tolosa-Marin clinical tremor rating scale was used to grade tremor, handwriting, and ability to drink. The median follow-up was 23 months.

Results. The mean tremor score was 3.28 ± 0.79 before and 1.81 ± 1.15 after (p < 0.0001) GKT; the mean hand-writing score was 2.78 ± 0.82 and 1.62 ± 1.04, respectively (p < 0.0001); and the mean drinking score was 3.14 ± 0.78 and 1.80 ± 1.15, respectively (p < 0.0001) . After GKT, 57 patients (66%) showed improvement in all 3 scores, 11 patients (13%) in 2 scores, and 2 patients (2%) in just 1 score. In 16 patients (19%) there was a failure to improve in any score. Two patients developed a temporary contralateral hemiparesis, 1 patient noted dysphagia, and 1 sustained facial sensory loss.

Conclusions. Gamma Knife thalamotomy in the MRI era was a safe and effective noninvasive surgical strategy for medically refractory tremor in the elderly or those with contraindications to deep brain stimulation or stereotactic radiofrequency (thermal) thalamotomy.(http://thejns.org/doi/abs/10.3171/2013.1.JNS121111)

Key Words      •      thalamotomy      •      tremor      •      Gamma Knife      •      multiple sclerosis      •      Parkinson disease      •      movement disorder      •      functional neurosurgery

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Abbreviations used in this paper: AC = anterior commissure; DBS = deep brain stimulation; ET = essential tremor; FTM = Fahn-Tolosa-Marin; GKT = Gamma Knife thalamotomy; MS = multiple sclerosis; PC = posterior commissure; PD = Parkinson disease; RFT = radiofrequency thalamotomy; VIM = ventralis intermedius.

See the corresponding editorial in this issue, pp 711–712.

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there are high risks for surgical comorbidities such as long-term anticoagulation have been deemed ineligible for invasive surgical procedures. Stereotactic radiosurgi-cal treatment, or GKT, is an important option for tremor patients ineligible for other types of thalamic surgery be-cause of advanced age or surgical comorbidities.

Prior reports have shown GKT to be an effective treat-ment for ET, with clinical improvement rates between 70% and 80%, comparable to stereotactic RFT.2,4,9 The purpose of the present study was to expand the clinical outcome analysis in a series of patients with disabling tremor, in all of whom target selection had been performed since the in-corporation of MRI for target selection.

MethodsThis research was approved by the University of

Pittsburgh Institutional Review Board. There were no ex-ternal sources of funding for this study.

Patient CohortThe study group consisted of 86 patients (51 males

and 35 females) whose mean age was 71 years. Two pa-tients (one with ET and one with MS) underwent staged bilateral procedures, bringing the number of overall pro-cedures to 88. In the 48 patients with ET, the mean age was 74 years. In the 11 patients with a diagnosis of MS the mean age was 45 years, and in the 27 patients with PD the mean age was 76 years. All patients were referred for consideration of surgery because of progressive or un-responsive tremor refractory to medical management. In most patients with ET, trials of propranolol and Mysoline failed. In recent years, trials of topiramate and levetirace-tam also failed in most patients. Patients with other signs and symptoms of PD continued to be managed with stan-dard agents such as carbidopa/levodopa. In patients with MS-related tremor, the condition proved generally unre-sponsive to medical therapy for tremor. There were no specific indications for radiosurgical thalamotomy com-pared with other surgical options. It was considered in pa-tients thought to be poor candidates for DBS either due to health or diagnosis (that is, MS). Thus, exclusion criteria for other procedures raised the option of radiosurgery. In rare cases patient choice was the indication.

Patients were considered potential surgical candi-dates if their tremor resulted in significant limitations in activities of daily living including handwriting and eat-ing. Although some patients had bilateral tremor, they reported that the disability of their tremor was greatest in their dominant hand. Preoperative FTM tremor rating scale scores1 were obtained and showed a wide spectrum of tremor-related disability (Table 1).7

Stereotactic Radiosurgery TechniqueDuring stereotactic radiosurgery, the Leksell model

G stereotactic coordinate frame (Elekta AB) was secured to the patient’s head using a local anesthetic supplement-ed by brief conscious sedation using fentanyl and mid-azolam. High-resolution MR images were obtained us-ing a 1.5- or 3.0-T scanner. Contrast-enhanced volume

acquisition MRI (with images at 1-mm intervals) was performed for stereotactic targeting through the thala-mus and midbrain to identify the AC, PC, and the third ventricle. An axial fast inversion recovery sequence was then obtained to better identify the internal capsule and differentiate gray and white matter structures. The target was the posterior and inferior aspect of the VIM of the contralateral limb most affected by tremor. The VIM was targeted as follows: 1) x coordinate: laterality (50% of the width of the third ventricle + 11 mm from the AC-PC line); 2) y coordinate: anterior-posterior (25% of the AC-PC distance + 1 mm anterior to the PC); and 3) z coordi-nate: superior-inferior (isocenter placed 2.5 mm superior to the AC-PC line). The lateral position of the isocenter was adjusted to keep it medial to the internal capsule. The 20% isodose line of the 4-mm collimator was kept medial to the internal capsule. When the model B, C, 4C, or Per-fexion Gamma Knife was used, selective beam or sector blocking was performed to restrict the dose in the region of the internal capsule, which can be well visualized by MRI. Magnetic resonance imaging also allows accurate measurement of the thalamic width, which facilitates adjustment of the medial-lateral x coordinate. A gamma angle of 110° was used to create an isocenter volume that more closely matched the shape of the VIM in the anteri-or-posterior and superior-inferior coordinates. When the model U unit was used for radiosurgery, a gamma angle of 60°–70° was used and no beam blocking was neces-sary. A maximum dose of 130–140 Gy was delivered with a single 4-mm isocenter.

Follow-UpWe reviewed the medical and imaging records of

86 patients who underwent GKT for treatment of their tremor during the recent 15-year era of MRI-based tar-get selection (1996–2011). Postradiosurgery imaging was conducted routinely at 4 months. Three functional items from the FTM clinical tremor rating scale includ-ing tremor amplitude, handwriting ability, and ability to drink from a cup were evaluated in all patients both preoperatively and during follow-up appointments. The clinical ratings were derived from chart notes recorded by the study neurosurgeon or referring neurologist, detailing the amplitude of tremor, ability to drink, and handwriting ability in the form of a handwriting sample. The tremor rating score used was validated by blinded comparison of reviewer scores. However, use of this rating scale during a telephone discussion was believed to be less reliable. We compared the 3 tremor subscores before and after radiosurgery for individual patients and compared group scores among the 3 tremor etiologies.

A p value of 0.05 was set for statistical comparison among tremor types.

ResultsThe median follow-up after GKT was 11.5 months

(range 1–152 months). All reported patients had pre- and postoperative testing. We excluded those without any follow-up appointments and/or those who died prior to a follow-up appointment; 86 patients remained after these

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exclusions. Of 97 total patients managed with GKT for tremor between 1996 and 2011, we excluded 11 patients who lacked both a follow-up appointment and were un-reachable later by phone, leaving 86 patients for our anal-ysis. Of the 17 patients for whom we recorded phone fol-low-up data points, only 2 (12%) had no in-person evalua-tions. Therefore, for these 2 patients information recorded via phone call is the only follow-up data we have. One of these patients was evaluated at 5 years. The remaining 15 patients (88%) who were phoned had their scores used to track changes in functional ability, to update data since the last office-based assessment.

The FTM clinical tremor rating scale was used to as-sess pre- and postoperative tremor, handwriting, and abil-ity to drink from a cup (Fig. 1). Overall, the preoperative and postoperative mean tremor scores were 3.3 ± 0.8 and 1.8 ± 1.2, respectively (p < 0.00001). The mean handwrit-ing scores were 2.8 ± 0.8 and 1.6 ± 1.0, respectively (p < 0.00001). The mean preoperative drinking scores were 3.1 ± 0.8 and 1.8 ± 1.1, respectively (p < 0.00001) (Table 1). After radiosurgery, 57 patients (66%) exhibited im-provement in all 3 assessed scores, 11 patients (13%) in 2 scores, 2 patients (2%) in just 1 score, and 16 patients (19%) had no improvement in any of the assessed scores. Thirty-five patients (40%) demonstrated either no tremor or a slight, barely perceivable tremor after GKT. The clin-ical benefit of radiosurgery for any indication occurred at an average of 2 months (range 1 week to 8 months).

Among the 48 patients with ET, the mean preopera-tive FTM writing score was 2.7 ± 0.8 and mean postop-erative writing score was 1.4 ± 1.1 (p < 0.00001). The tremor score was 3.3 ± 0.8 preoperatively and 1.8 ± 1.2 postoperatively (p < 0.00001). The water-drinking score improved from 3.1 ± 0.8 before GKT to 1.7 ± 1.2 at the most recent follow-up (p < 0.00001) (Table 2). Of those

patients diagnosed with ET, 20 (42%) demonstrated either complete resolution or a barely perceivable tremor after GKT. One patient with ET underwent insertion of a con-tralateral DBS system 2 years later and did well.

Among 27 patients with PD, the mean FTM writ-ing score changed from 2.4 ± 0.6 preoperatively to 1.3 ± 0.9 postoperatively (p < 0.0001). The mean tremor score was 3.0 ± 0.8 before GKT and 1.5 ± 1.1 after GKT (p < 0.0001), and the mean water-drinking score was 2.9 ± 0.8 before treatment and after treatment 1.5 ± 1.0 (p < 0.0001) (Table 3). Analysis of the results for the 11 patients with MS showed mean writing scores of 3.7 ± 0.5 before GKT and 2.4 ± 0.8 after GKT (p < 0.003). Mean tremor scores were 3.9 ± 0.3 preoperatively and 2.5 ± 0.9 postopera-tively (p < 0.001). Mean FTM drinking scores were 3.9 ± 0.3 before treatment and 2.5 ± 1.0 at the most recent follow-up (p < 0.003) (Table 4). Patients in each tremor subset showed similar improvements in functional scores post-GKT. Improvements in FTM score after treatment for all scores (writing, tremor, and drinking) and tremor subsets (ET, PD, or MS) varied from 1.1 to 1.5, with simi-lar scores before and after radiosurgery for the ET and PD subsets. Patients with MS had significantly higher preoperative scores, but analysis demonstrated a similar FTM score improvement after GKT—an improvement of 1.3 in writing score, 1.4 in tremor score, and 1.4 in the drinking score.

Two patients experienced temporary contralateral hemiparesis 6 months after GKT, 1 patient experienced dysphagia after 8 months, and 1 patient described a peri-oral burning sensation with left-sided facial numbness.

The thalamotomy lesion that developed in patients was visible on the first MRI study (obtained as early as 3 months). The effect was a well-circumscribed contrast-enhanced lesion with central hypointensity. Postradiosur-

TABLE 1: Summary of FTM tremor scores in 86 patients who underwent 88 GKT procedures*

Period No. of ProceduresFTM Category

Writing Tremor Drinking

all 88 preop 2.8 ± 0.8 3.3 ± 0.8 3.1 ± 0.8 postop 1.6 ± 1.0 1.8 ± 1.2 1.8 ± 1.1 Wilcoxon p value <1E-10 <1E-10 <1E-10ET 48 preop 2.7 ± 0.8 3.3 ± 0.8 3.1 ± 0.8 postop 1.4 ± 1.1 1.8 ± 1.2 1.7 ± 1.2 Wilcoxon p value <1.191E-7 <8.075E-8 <1.525E-7PD 29 preop 2.4 ± 0.6 3.0 ± 0.8 2.9 ± 0.8 postop 1.3 ± 0.9 1.5 ± 1.1 1.5 ± 1.0 Wilcoxon p value <6.414E-5 <2.891E-5 <2.891E-5MS 11 preop 3.7 ± 0.5 3.9 ± 0.3 3.9 ± 0.3 postop 2.4 ± 0.8 2.5 ± 0.9 2.5 ± 1.0 Wilcoxon p value ≤0.002217 ≤0.0009805 ≤0.002217

* Values represent means ± SD unless otherwise noted.

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gery images were obtained routinely at 4 months. The mean contrast-enhanced short–echo time MRI-measured lesion diameter was 5 mm. When contrast-enhanced CT was used for follow-up, a similar lesion size was iden-tified. Surrounding changes on FLAIR imaging were seen in all patients with MRI. Few patients underwent MRI after 1 year, but persistent contrast-enhanced le-sions could be seen within Years 1–2, with regression of enhancement after Year 2. Magnetic resonance imaging was requested 4 months following radiosurgery and was not routinely repeated unless new symptoms developed, because in an early cohort of patients the observed lesions remained stable for 2 years and then decreased in size. The patients who experienced any complication had the onset of symptoms beginning at 6 months after thalamot-omy. Imaging performed at that time showed evidence of larger contrast-enhancing lesions due to blood-brain bar-rier disruption with inflammation. These changes later regressed over the next year.

DiscussionRationale for Radiosurgical Thalamotomy

Currently, thalamic DBS may be the commonest sur-gical procedure for medically refractory essential or par-kinsonian tremor where it is available. The value of DBS in MS-related tremor is not clear because tremor relief is modest and often not lasting.10,12 Stereotactic RFT is still performed where DBS may not be available or affordable. Both procedures are rarely performed in patients older than 80 years or those with medical comorbidities in whom RFT is thought to be associated with unacceptable risk. For such patients, stereotactic radiosurgical thalamotomy us-ing the Gamma Knife is an important option. Prior studies,

although few in number, have demonstrated a significant improvement in tremor control.13 However, this procedure remains underutilized. During the last 15 years, target se-lection has improved as MRI technologies have advanced.

However, it is not just the ability to perform radio-surgery in older patients or those with significant addi-tional risk factors that makes such a minimally invasive strategy attractive. The radiobiological effect of the radio-surgical lesion is unique. The effect consists of a limited central target necrosis (3–4 mm in diameter) where the highest dose is delivered. This central zone is surrounded by a nonnecrotic peripheral or halo effect that may also provide therapeutic benefit to thalamic cells generating tremor. This peripheral effect, which consists of astrocy-tosis and mild vascular changes (hyalinization of blood vessels), has been well characterized in subhuman pri-mate models of radiosurgery.4,5 Indeed, we think that this regional effect allows radiosurgical targeting to result in a larger therapeutic volume than that obtained during radiofrequency or other heat lesioning techniques. This benefit largely addresses the primary criticism of tremor ablative radiosurgery—that is, the lack of intraoperative electrophysiology target confirmation.

Importance of MRI-Based TargetingAs with the majority of functional neurosurgery pro-

cedures, precision of anatomical targets is key to success-ful interventions and avoidance of complications. The critical anatomical structures near the VIM nucleus must be avoided, and with higher-definition MRI sequences, accurate targeting of this region can be performed safely. Computed tomography targeting, however, is still per-formed today in patients who have pacemakers or other contraindications to MRI. The accuracy of their VIM

Fig. 1. Preoperative and the most recent follow-up writing (A), tremor (B), and water-drinking (C) scores for all patients who underwent GKT.

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targeting is inherently less than it is with MRI, but the thalamotomy can still be performed with relative safety.

Critical Analysis of Results of Radiosurgical ThalamotomyIn the present study, GKT in the modern era of MRI-

based targeting proved to be effective in improving medi-cally refractory tremor associated with ET, PD, and MS. In 70 patients (81%), at least one of the assessed scores was improved following GKT. Of these 70 patients, the median follow-up duration before improvement was 4 months.

A previous series of 26 patients with ET undergo-ing GKT showed that 90% of patients had some degree of tremor improvement, with 50% showing either no or only slight intermittent tremor after GKT.5 The authors of a smaller series of 8 cases in which patients with ET underwent GKT noted an 87.5% rate of clinical improve-ment (62.5% complete tremor arrest, 25% nearly tremor free).11 A recent prospective multicenter study from Japan of 72 patients (with PD or MS) found that 81% of patients had excellent or good results.8 Results from each of these studies are comparable to those of the present study, in which 81% of the patients demonstrated some degree of clinically significant tremor improvement.

One study of 18 patients (with ET and PD) using doses of 130–140 Gy found significant improvements in FTM scores for activities of daily living but not tremor.6

In each disease subset, GKT provided statistically significant improvements in FTM writing, tremor, and drinking scores. Similar results were seen in patients with ET and PD. Interestingly, patients with MS who underwent GKT had preoperative scores notably higher than those of the ET and PD patients, indicating that the tremor was more severe at the time of referral. Most MS patients had a coarse, jerking tremor, causing them to of-ten bang their arm and hand against a wheelchair armrest or bedrail. Despite this difference, we found that MS pa-tients had FTM scoring improvements similar to the ET and PD subsets of patients. However, the clinical signifi-cance of the MS score reductions, from a range of 3.7–3.9 preoperatively to one of 2.4–2.5 post-GKT, is perhaps not as important to the patient functionally as the scor-ing improvements seen in ET and PD patients (for whom the final post-GKT scores were in the range of 1.2–1.5). The severity of tremor was lessened, but the ability for the patient to perform tasks was variable depending on other MS-related deficits.

Complication Assessment and AvoidanceThe complications we observed in this patient series,

though few, raise several issues with regard to GKT. The radiation effect of GKT in some patients caused a larger than required response that led to inflammation and local mass effect on the internal capsule, with subsequent mo-tor or sensory deficits. These deficits were not permanent and responded to a course of high-dose corticosteroids. There was no obvious flaw in technique in any of these patients, but the presence of a larger lesion was only noted after clinical manifestations were observed. It is possible that other patients had such transient expansion of the ra-diobiological effect but remained asymptomatic.

Maintenance of Tremor ReliefWe studied the maintenance of tremor relief over

time. In the current study 5 patients (6%) experienced improved symptoms and tremor scores at initial follow-up but the initial benefit waned over time. The median initial follow-up time to improved scores was 4 months, while the median time that scores later worsened was 23 months. These patients included a 70-year-old man, an 85-year-old man, a 90-year-old woman, a 57-year-old woman, and a 71-year-old man. Four such patients had ET and one had MS. These patients represented a unique group who experienced short-term improvement of trem-or symptoms after GKT but who did not sustain that level of improvement. At their most recent follow-up, statuses in 3 of these patients had returned entirely to their pre-GKT scores, while scores in the other 2 patients were maintained and were better than those determined before radiosurgery. We think that radiosurgery provides tremor control that is longer lasting than that seen after RFT. Some patients who undergo RFT develop early symptom recurrence once the perilesional edema effect resolves. Indeed, the final thermal lesion may be too small. In DBS-treated patients, the need to increase the stimulation energy over time is common. The biology of the radio-surgical effect may be the reason why cells involved in tremor remain controlled.

Limitations of the Present StudyThe limitations are related to a variability in outcome

documentation, because many patients lived at a distance and not all maintained follow-up at our center. This study used patients as their own controls and did not include an additional control group such as best medical therapy or DBS.

ConclusionsIn the era of MRI, we found that GKT for tremor in

a group of patients who are elderly or high risk if treated with DBS or RFT can have significant benefit. Further clinical experience in the use of GKT for medically re-fractory tremor is warranted. One question to evaluate is whether a higher dose (for example, 150 Gy) may im-prove or sustain tremor relief. At present we believe that GKT is an underutilized approach, appropriate for elderly patients with disabling tremor and those with other in-creased surgical risk factors.

Disclosure

Dr. Kondziolka is a consultant for Elekta AB, and Dr. Lunsford is consultant for and shareholder in Elekta AB.

Author contributions to the study and manuscript prepara-tion include the following. Conception and design: all authors. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Kondziolka. Statistical analysis: all authors. Administrative/technical/material support: Kondziolka, Kooshkabadi, Lunsford, Tonetti. Study supervision: Kondziolka.

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Manuscript submitted June 1, 2012.Accepted January 8, 2013.Please include this information when citing this paper: pub-

lished online February 1, 2013; DOI: 10.3171/2013.1.JNS121111.Address correspondence to: Douglas Kondziolka, M.D., Depart-

ment of Neurosurgery, NYU Langone Medical Center, 530 First Avenue, Suite 8R, New York, New York 10016. email: douglas.kondziolka@nyumc.org.