Brain, Vol. 122, No. 3, 417-425,
March 1999
© 1999 Oxford University Press
Article |
Reassessment of unilateral pallidotomy in Parkinson's disease
A 2-year follow-up study
Neurodegenerative Disorders Centre, Vancouver Hospital and Health Sciences Centre, Vancouver, BC, Canada
Correspondence to:
Dr Donald B. Calne, Neurodegenerative Disorders Centre, Vancouver Hospital and Health Sciences Centre, Purdy Pavilion, 2221, Wesbrook Mall, Vancouver, BC, Canada V6T 2B5
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Abstract |
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Unilateral pallidotomy has gained popularity in treating the motor symptoms of Parkinson's disease. We present the results of a 2-year post-pallidotomy follow-up study. Using the Unified Parkinson's Disease Rating Scale (UPDRS), the Goetz dyskinesia scale and the Purdue Pegboard Test (PPBT), we evaluated 20 patients at regular intervals both off and on medications for 2 years post-pallidotomy. There were no significant changes in the dosages of antiparkinsonian medications from 3 months pre-pallidotomy to 2 years post-pallidotomy. On the side contralateral to the operation, the improvements were preserved in `on'-state dyskinesia (83% reduction from pre-pallidotomy to 2 years post-pallidotomy, P < 0.001) and `off'-state tremor (90% reduction from pre-pallidotomy to 2 years post-pallidotomy, P = 0.005). There were no statistically significant differences between pre-pallidotomy scores and those at 2 years post-pallidotomy in ipsilateral dyskinesia, axial dyskinesia, `off'- or `on'-state PPBT, `off'-state Activities of Daily Living (ADL) and `off'-state gait and postural stability. After 2 years, the `on'-state ADL scores worsened by 75%, compared with pre-pallidotomy (P = 0.005). We conclude that 2 years after pallidotomy, the improvements in dyskinesia and tremor on the side contralateral to pallidotomy are preserved, while the initial improvements in most other deficits disappear, either because of progression of pathology or loss of the early efficacy achieved by surgery.
Parkinson's disease; pallidotomy; stereotaxic techniques; dyskinesia; tremor
ADL = Activities of Daily Living; GPi = globus pallidus internus; PPBT = Purdue Pegboard Test; UPDRS = Unified Parkinson's Disease Rating Scale
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Introduction |
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Unilateral pallidotomy has become a useful procedure in the treatment of patients with Parkinson's disease, when they encounter disabling side-effects from pharmacotherapy. In recent years, a number of investigators have reported variable degrees of benefit from pallidotomy (Laitinen et al., 1992
; Laitinen, 1994; Dogali et al., 1995; Iacono et al., 1995; Lozano et al., 1995; Sutton et al., 1995; Baron et al., 1996; Friedman et al., 1996; Shima et al., 1996; Fazzini et al., 1997; Johansson et al., 1997; Kazumata et al., 1997; Kishore et al., 1997;, Lang et al., 1997a, b; Uitti et al., 1997). Prospective studies have found that pallidotomy can improve tremor, bradykinesia, rigidity and dyskinesia (Laitinen et al., 1992; Dogali et al., 1995; Lozano et al., 1995; Baron et al., 1996; Shima et al., 1996; Fazzini et al., 1997; Kazumata et al., 1997; Kishore et al., 1997; Lang et al., 1997b). Dyskinesia can improve not only on the side contralateral to the surgery, but also on the ipsilateral side. Axial dyskinesia also responds to pallidotomy. In addition, many groups have reported significant improvements in activities of daily living (ADL) and levels of independence (Dogali et al., 1995; Baron et al., 1996; Kazumata et al., 1997; Kishore et al., 1997; Lang et al., 1997b; Uitti et al., 1997). However, carefully conducted, long-term follow-up studies on the effects of pallidotomy are scarce (Fazzini et al., 1997; Lang et al., 1997b). Fazzini et al. (1997) have reported preserved improvement up to 4 years after pallidotomy. Lang et al. (1997b) have reported sustained benefit in most of their patients 2 years after the operation. Kishore et al. (1997) reported significant benefits in 24 patients in the early post-operative period, 11 of whom were studied up to 1 year post-pallidotomy. We now report a follow-up study on 20 of the original 24 patients, who have been evaluated at regular intervals for at least 2 years. |
Methods |
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Subjects
The patient selection process, the exclusion criteria and the characteristics of the patients have been described in detail elsewhere (Kishore et al., 1997
). Briefly, 24 patients were selected by a neurologist (D.B.C.) experienced in movement disorders and a neurosurgeon (I.M.T.) experienced in stereotactic surgery. Twenty-two patients had motor fluctuations, with disabling dyskinesia, and two patients had severe tremor that had not responded to medications. The patients had been on stable antiparkinsonian medications for at least 3 months prior to surgery.
Surgical procedure
Pallidotomy was performed contralateral to the side with the more pronounced dyskinesia, and if dyskinesia was not troublesome, contralateral to the more severe tremor. If the motor symptoms were symmetrical, the pallidotomy was performed on the side contralateral to the dominant hand. Before the operation, all antiparkinsonian medications were withheld for 8–12 h so that the motor symptoms were more apparent.
A Cosman–Roberts–Wells or Brown–Roberts–Wells (Radionics, Inc., Burlington, Mass., USA) ring and localizer were applied under local anaesthesia, and a CT scan obtained with slices at 2 mm intervals through the third ventricle and upper midbrain. The ring was fastened to the patient such that the cuts would be parallel to the intercommissural plane (Turnbull et al., 1985). The coordinates of a target where the 1.5 mm exposed tip of an electrode 1.8 mm in diameter would be placed in the posterolateral region of the medial globus pallidus, as described by Laitinen (1994), were recorded. This radiographic target was 5–6 mm below the intercommissural plane, 21–23 mm lateral to midline, and 2 mm anterior to the midpoint of the intercommissural plane.
A burr hole on the coronal suture at the same lateral distance as the target was drilled under local anaesthesia and the electrode introduced. Stimulation at 2 and 50 Hz at a point 6 mm short of the target on the electrode trajectory usually evoked no response. Experience has allowed us to determine the threshold for a motor and, occasionally sensory reponse that indicates that the electrode is too close to the internal capsule and needs to be moved to a target more anterior and lateral. Stimulation was carried out at loci 6, 4 and 2 mm above the target and then on the target, and 1 and 2 mm past the target in order to reach a position deep in the pallidum that did not evoke visual or other untoward responses. We have learned from our experience not to advance the electrode past the position where the phosphenes were first evoked and not to make the lesion <3 mm above that plane. We did not use intra-operative microelectrode recording. The first lesion was made at 80°C for 60 s after noting that no ill effects occurred from raising the temperature to 42°C and then to 60°C. Second and third lesions were made at 80°C after the electrode was withdrawn 3 mm and then 6 mm from the deepest lesion.
Clinical assessment
We used the Unified Parkinson's Disease Rating Scale (UPDRS) to rate activities of daily living (ADL) (subset II), motor performance (subset III) and complications of therapy (subset IV) (Fahn et al., 1987). We used the CAPIT (Core Assessment Program for Intracerebral Transplantation) for definitions of `off' and `on' states (Langston et al., 1992). For subset II, we asked the patients about their average ability to perform ADL during both the `off' and `on' states. For subset III, we examined the patients in both states. For the `off' state motor evaluation, we examined the patients between 08:00 and 09:00 in the morning following at least 12 h off all antiparkinsonian medication (18 h for controlled release levodopa/carbidopa). The patients were then given their usual first morning doses of antiparkinsonian medications, and they were examined 1–2 h later in their optimal `on' state. Most, but not all motor evaluations (UPDRS, subset III) were recorded on videotape.
We rated dyskinesia when the patients were in the optimal `on' state using the rating scale developed by Goetz et al. (1994). In addition, we evaluated the patients during both `off' and `on' states with the Purdue Pegboard Test (PPBT) (Hietanen et al., 1987). This test records the number of pegs inserted into a pegboard in 30 s unilaterally first with each hand separately, and then bilaterally with both hands simultaneously.
We kept detailed records of the patients' antiparkinsonian medications throughout the 2-year period. For the analysis, doses of 100 mg levodopa in standard Sinemet were regarded as equivalent to 130 mg levodopa in controlled release Sinemet. The doses of pergolide and ropinirole were expressed as equivalent doses of bromocriptine (1 mg pergolide = 10 mg bromocriptine, and 1 mg ropinirole = 2 mg bromocriptine). The exact dose conversion factor for ropinirole to bromocriptine is not known. However, the ratio of 1 : 2 for ropinirole to bromocriptine was derived from a recent study that directly compared the two drugs (Korczyn et al., 1998). In this study, the side-effect profile attributable to dopaminergic activity for the two drugs was similar, and the mean bromocriptine dose was approximately twice that of ropinirole.
All UPDRS evaluations and dyskinesia ratings were performed by two neurologists experienced in using these scales (A.K. and A.S.). The assessments done both before and after surgery, up to and including the 9-month follow-up evaluation were performed by examiner I (A.K.). At the 1 year post-operative follow-up, 11 patients were evaluated by examiner I, and 9 patients were evaluated by examiner II (A.S.). All the 18-month and 2-year evaluations were performed by examiner II. The PPBT assessments at all visits were conducted by the same nurse clinician who was experienced in conducting this test (S.Y.).
Statistical analysis
In order to adjust for potential inter-rater differences in motor scoring between the two examiners, we compared their scoring patterns on the same patients, using videotape recordings from the pre-pallidotomy and the 3 month post-pallidotomy assessments (recorded by examiner I). Examiner II reviewed these videotaped assessments, blinded to the scores assigned by examiner I, and provided motor scores using the UPDRS subset III (except for rigidity which cannot be assessed on videotape).
Using correlation analyses, the scores provided by examiner II (from videotape observations) were compared with the scores originally provided by examiner I (from direct patient observations). Whenever a significant correlation was noted for a particular measurement between the two examiners (P < 0.05), the missing observations of either examiner were imputed by regression analysis. Thus, the values from early evaluations not available on videotape were imputed for examiner II, and the values for the later evaluations were imputed for examiner I, only where there were significant correlations between the two examiners. We used the observed and the imputed values for UPDRS motor scores (subset III), for both examiners. The scores for ADL and complications of therapy depend predominantly on answers to standard questions that the patients provide, and the PPBT was performed on all patients by a single examiner throughout the study. Therefore, we did not perform correlation analysis on PPBT, ADL (UPDRS subset II) or complications of therapy (UPDRS subset IV) to compensate for inter-rater differences.
For each examiner, we carried out repeated measures analysis of variance on observed and imputed UPDRS motor scores, dyskinesia scores, as well as medication dosages, PPBT scores and ADL scores at pre-pallidotomy, and at 3 months, 18 months and 2 years post-pallidotomy. Comparisons between pre-pallidotomy scores and those from each of the post-pallidotomy evaluations, as well as analyses among the post-pallidotomy scores, were carried out by the method of multiple contrasts. Bonferroni's correction was used to adjust for mutiple comparisons. For all statistical analyses, an adjusted P-value of <0.05 was considered to be significant.
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Results |
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Subjects
Twenty of the original 24 patients were followed with evaluations at 1 year, 18 months and 2 years post-pallidotomy. One patient (a 70-year-old woman) died 2 weeks after her pallidotomy from an intracerebral bleed on the same side as the operation. It was not possible to determine from the autopsy whether the haemorrhage was related to the surgical track. Another patient (a 75-year-old man) died 17 months post-pallidotomy from cardiac illness. No autopsy was performed on this patient. One patient (a 40-year-old man) was lost to follow-up 1 year after pallidotomy when he moved to a long-term care facility too far away for follow-up. One patient (a 67-year-old man) who had no significant benefit from the first operation underwent a repeat pallidotomy on the same side 1 year after the original operation. The data from his evaluations were therefore excluded from the analysis.
All patients were taking levodopa/carbidopa (controlled release, standard or a combination). Twenty-one patients were originally on bromocriptine and two were on pergolide. One patient who was not originally taking a dopamine agonist began taking ropinirole a few weeks before the 2-year evaluation, and another patient switched from bromocriptine to ropinirole a few weeks before the 2-year evaluation. Overall, there were no significant changes in the dosages of antiparkinsonian medications from 3 months pre-pallidotomy to 2 years post-pallidotomy. Figure 1 shows the dosages of antiparkinsonian medications, expressed as controlled-release levodopa or bromocriptine equivalents, at pre-pallidotomy and at 3 months, 18 months and 2 years post-pallidotomy.
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Correlation analyses
The scoring patterns for dyskinesia (using the Goetz scale), and tremor, gait and stability (using the motor UPDRS) correlated well in the two examiners. We therefore compared the tremor, gait and postural stability components of the UPDRS motor examination, as well as the dyskinesia scores by imputing expected values for both examiners. Tests for limb bradykinesia and rigidity yielded inconsistent results in the two examiners, so these measures were not considered sufficiently robust to analyse. Table 1
summarizes the results of the correlation analysis between the motor scores provided by the two examiners.
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`Off'-state changes
On the side contralateral to the pallidotomy, improvements in `off'-state resting tremor were preserved after 2 years. There was a 90% reduction in contralateral resting tremor at 2 years post-pallidotomy when compared with pre-pallidotomy (P = 0.005, adjusted for multiple comparisons). On the side ipsilateral to the pallidotomy, the improvement seen in resting tremor 3 months post-operatively reported by Kishore et al. (1997) disappeared by 18 months (Fig. 2
). The `off'-state PPBT scores in the limb contralateral to the operation showed a trend towards preserved improvement at 18 months and 2 years, but once corrected for multiple comparisons, this trend did not reach statistical significance (Fig. 3A). The `off'-state PPBT scores in the upper limb ipsilateral to the operation, or both upper limbs performing simultaneously were not significantly different at 18 months or 2 years post-pallidotomy when compared with pre-pallidotomy or 3 months post-pallidotomy (Fig. 3A). The `off'-state gait scores showed a trend towards worsening at 2 years when compared with pre-pallidotomy (Fig. 4A), but this trend did not reach statistical significance after the correction for multiple comparisons (from P = 0.010 to P = 0.060). The `off'-state gait scores at 2 years were significantly worse than those at 3 months post-pallidotomy (P = 0.003, adjusted for multiple comparisons). There was no significant change in postural stability at 18 months or 2 years, compared with pre-pallidotomy or 3 months post-pallidotomy (Fig. 4A).
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`On'-state changes
On the side contralateral to the pallidotomy, improvements in `on'-state dyskinesia were preserved after 2 years. There was a 83% reduction in contralateral dyskinesia at 2 years post-pallidotomy when compared with pre-pallidotomy (P < 0.001, adjusted for multiple comparisons). There was no significant difference in axial dyskinesia or ipsilateral limb dyskinesia between pre-pallidotomy and 18 months or 2 years post-pallidotomy (Fig. 5
). This suggests that the early improvements in ipsilateral and axial dyskinesia reported by Kishore et al. (1997) had disappeared by 18 months. The `on'-state PPBT scores (Fig. 3B
), postural stability and gait scores (Fig. 4B) were not significantly different from pre-pallidotomy to 3 months, 18 months or 2 years post-pallidotomy.
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UPDRS subset II (ADL) and subset IV (complications of therapy)
The `off'-state total ADL scores at 18 months and 2 years were not significantly different from the pre-pallidotomy scores, but were significantly worse than the 3 month post-pallidotomy scores (P < 0.001 for both, adjusted for multiple comparisons). This suggests that the initial improvements reported by Kishore et al. (1997) had disappeared by 18 months. After 2 years, the `on'-state ADL scores had worsened by 75%, compared with pre-pallidotomy (P = 0.005, adjusted for multiple comparisons), suggesting that disease progression had occurred (Fig. 6
). There was no significant change in either UPDRS subset IV-A (dyskinesia rated by the patient), or subset IV-B (motor fluctuations rated by the patient) between pre-pallidotomy and 18 months or 2 years post-pallidotomy. Again, this suggests that the improvements in subset IV scores in the early post-operative period reported by Kishore et al. (1997) had disappeared by 18 months (Fig. 7). Pallidotomy did not change the proportion of `off' time (UPDRS-IV, item 39) during the waking day (Fig. 8). At 3 months post-pallidotomy, the proportion of the waking day during which dyskinesia occurred (UPDRS-IV, item 32) was reduced compared with pre-pallidotomy (P < 0.05), but this improvement disappeared by 18 months (Fig. 8).
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Discussion |
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In 1987, the UPDRS was developed to provide a comprehensive scale for mental, motor and functional evaluation of patients with Parkinson's disease (Fahn et al., 1987
). The overall reliability of UPDRS has been tested and deemed adequate (Martinez-Martin et al., 1994; Richards et al., 1994; Goetz et al., 1995; Louis et al., 1996). However, different components of the UPDRS show different degrees of inter-rater agreement. For example, in one study, it was found that resting tremor and gait scores had excellent inter-rater reliability, while rigidity and bradykinesia ratings had moderate, and speech ratings had poor inter-rater reliability (Richards et al., 1994).
We used videotapes from prior examinations to compare the scoring patterns of the two examiners. We found good correlation in most categories of motor scoring with the exception of limb bradykinesia, which includes finger tapping, fist closure/opening, alternating pronation/supination and foot tapping. Therefore, we eliminated limb bradykinesia from the analysis. However, an adequate assessment of limb bradykinesia could still be achieved because the PPBT provided an index of this deficit (Hietanen et al., 1987; Vingerhoets et al., 1997). Since we could not determine whether or not there was an adequate correlation in rigidity scoring (which could not be assessed by reviewing videotapes) between the two examiners, we also eliminated this component of the UPDRS motor examination from the analysis. We compared the dyskinesia scoring patterns using the scale provided by Goetz et al. (1994), and we found good correlation between the two examiners here.
We found that only improvements in tremor and dyskinesia in the limbs contralateral to the pallidotomy were preserved after 2 years. Kishore et al. (1997) reported improvements in axial and ipsilateral limb dyskinesia in the early post-operative period, which according to our results, had disappeared by 18 months. The same was true for UPDRS subset IV scores (motor fluctuations and dyskinesia ratings) provided by the patients.
The dyskinesia scores by self-assessment (UPDRS-IV) paralleled the observations on axial and ipsilateral dyskinesia, in that they were improved early in the post-pallidotomy period, but the improvements disappeared by 18 months. This is because the dyskinesia segment of the UPDRS-IV does not differentiate between the two sides or axial dyskinesia. Therefore, from the patients' standpoint, the persistent improvement in contralateral dyskinesia was insufficient to compensate for the deterioration in axial and ipsilateral dyskinesia or in the proportion of waking day during which dyskinesia occured.
The improvements in the `off'-state ADL scores had also disappeared by 18 months. The `on'-state ADL scores had actually worsened by 2 years post-pallidotomy. This could be due to either disease progression or possible deterioration secondary to the pallidotomy itself. The `off'-state PPBT scores in the contralateral limb that had improved 3 months post-operatively, were not significantly different (once corrected for multiple comparisons) at 18 months or 2 years, compared with pre-pallidotomy. Since `off'-state PPBT is a measure of limb bradykinesia (Hietanen et al., 1987; Vingerhoets et al., 1997), this suggests that the improvements in contralateral limb bradykinesia also disappeared by 18 months.
The earlier pallidotomy studies reported various degrees of improvement in bradykinesia, tremor, speech, levodopa-induced dyskinesia, gait and even mental performance (Laitinen et al., 1992; Laitinen, 1994; Dogali et al., 1995; Iacono et al., 1995; Lozano et al., 1995; Sutton et al., 1995; Shima et al., 1996). More extensive studies followed patients for longer periods at regular intervals using standardized comprehensive tests (Baron et al., 1996; Fazzini et al., 1997; Johansson et al., 1997; Kazumata et al., 1997; Kishore et al., 1997;, Lang et al., 1997b; Uitti et al., 1997; Biousse et al., 1998).
Although most investigators report improvements in `off'-state bradykinesia and rigidity, there are two studies that have reported no improvement (Sutton et al., 1995; Johansson et al., 1997). Sutton et al. (1995) found no overall functional improvement post-pallidotomy, but peak-dose dyskinesia was significantly ameliorated contralateral to the operation. Johansson et al. (1997) found bradykinesia to be unchanged post-operatively, but contralateral dyskinesia and tremor were significantly improved, with some reduction in axial and ipsilateral dyskinesia. The only symptom that is invariably improved in all pallidotomy series is levodopa-induced dyskinesia on the side contralateral to the operation, with contralateral tremor being the next most consistent improvement. Neither of these two groups used microelectrode recordings to delineate the lesion site.
Two long-term studies have reported persistent benefit in overall function after pallidotomy (Fazzini et al., 1997; Lang et al., 1997b). Fazzini et al. (1997) reported 4-year results in five patients. They found that the improvements in the `off'-state timed tests of pronation–supination, finger dexterity and hand/arm movement were still preserved after 4 years in the upper limb contralateral to the pallidotomy. Lang et al. (1997b) reported 2-year results in 11 patients. They found that the improvements in `off'-state contralateral bradykinesia and rigidity were sustained at 2 years. The improvement in tremor was not sustained after 2 years, probably because of the correction for multiple comparisons and a small sample size. The improvement in contralateral dyskinesia was sustained at 2 years, but was lost in ipsilateral dyskinesia by the second year. Our results, together with those of Fazzini et al. (1997) and Lang et al. (1997b), suggest that the long-term relief of contralateral dyskinesia is the most enduring benefit of pallidotomy. The other early post-operative benefits have variable longevity depending on the study.
Most investigators agree that the lesion site should be in the ventroposterior or ventroposterolateral segment of globus pallidus internus (GPi), contralateral to the more symptomatic side. Some centres use intraoperative microelectrode recordings to delineate the GPi prior to making a permanent lesion (Hutchison et al., 1994; Dogali et al., 1995; Lozano et al., 1995; Baron et al., 1996; Shima et al., 1996; Fazzini et al., 1997; Kazumata et al., 1997; Lang et al., 1997b; Uitti et al., 1997), while others (including our centre) do not (Laitinen et al., 1992; Laitinen, 1994; Iacono et al., 1995; Sutton et al., 1995; Johansson et al., 1997; Kishore et al., 1997). The location of the lesion in operations where microelectrode recording is carried out depends on the neuronal firing pattern within the pallidum, as well as the results of microstimulation to identify sensitive structures such as the internal capsule and the optic tract. At centres that do not use microelectrode recording, the lesion site depends on accurate stereotactic localization of the intended target, as well as microstimulation to identify sensitive structures. Differences in microelectrode recording techniques, microstimulation frequencies, and stereotactic techniques are bound to produce different lesion sites and sizes.
With the advent of deep brain stimulation, it has been possible to stimulate different structures in the basal ganglia and the thalamus, and render them temporarily dysfunctional through high frequency simulation, thus mimicking a lesion without permanency (Benabid et al., 1991; Siegfried and Lippitz, 1994; Limousin et al., 1995; Davis et al., 1997; Troster et al., 1997). Two recent studies have found that stimulating different sites in the pallidum had different outcomes (Bejjani et al., 1997; Krack et al., 1998). Bejjani et al. (1997) found that in the `off'-state, stimulating the dorsal GP improved gait, bradykinesia and rigidity, and could induce dyskinesia, while stimulating the posteroventral GP worsened gait and bradykinesia, but still reduced rigidity. In the `on'-state, stimulating the posteroventral GP reduced dyskinesia, and worsened gait and bradykinesia, thus `cancelling out' the effect of levodopa. Krack et al. (1998) found very similar results. They also found that stimulating a zone intermediate between the two extreme positions led to a `good compromise' between these opposite effects, similar to the results seen after pallidotomy. These varying responses from dorsal and ventral pallidal stimulation, together with differences in microelectrode recording and stereotactic techniques may help to explain the different outcomes reported.
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Acknowledgments |
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We wish to thank Susan Calne for skilful editing. We also wish to thank the Medical Research Council of Canada, The Parkinson Foundation of Canada, The Pacific Parkinson Research Institute and The National Parkinson Foundation for supporting this study.
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Received June 4, 1998. Revised September 21, 1998. Accepted October 21, 1998.
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