- Email: [email protected]
Stereotactic surgery for subthalamic nucleus stimulation under general anesthesia: A retrospective evaluation of Japanese patients with Parkinson's disease
ARTICLE IN PRESS
Parkinsonism and Related Disorders 13 (2007) 101–107 www.elsevier.com/locate/parkreldis
Stereotactic surgery for subthalamic nucleus stimulation under general anesthesia: A retrospective evaluation of Japanese patients with Parkinson’s disease Kazumichi Yamadaa,, Satoshi Gotoa, Jun-ichi Kuratsua, Kazuhito Matsuzakib, Tetsuya Tamurab, Shinji Nagahirob, Nagako Murasec, Hideki Shimazuc, Ryuji Kajic a
Department of Neurosurgery, Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Kumamoto City 860-8556, Kumamoto, Japan b Department of Neurological Surgery, Graduate School of Medicine, The University of Tokushima, Japan c Department of Clinical Neuroscience, Graduate School of Medicine, The University of Tokushima, Japan Received 10 April 2006; received in revised form 20 June 2006; accepted 12 July 2006
Abstract We compared retrospectively the outcome of bilateral subthalamic nucleus (STN) stimulation in 15 patients with Parkinson’s disease who underwent the procedure under general anesthesia (GA) with that achieved in 10 patients under local anesthesia (LA). At 3 months postoperatively, all cardinal parkinsonian motor symptoms, evaluated on Unified Parkinson’s Disease Rating Scale were significantly improved compared to preoperative baselines in both groups. The administration of GA did not adversely affect postoperative improvements in motor and daily activity scores, except for off-medication bradykinesia. Our results suggest that GA compares favorably with LA in surgical procedure for bilateral STN stimulation. r 2006 Elsevier Ltd. All rights reserved. Keywords: Anxiety; Deep brain stimulation; Drug-induced psychosis; General anesthesia; Parkinson’s disease; Subthalamic nucleus
1. Introduction Continuous high-frequency stimulation of the bilateral subthalamic nucleus (STN) is now widely accepted as a procedure that strikingly improves motor symptoms and levodopa-induced motor complications in patients with Parkinson’s disease (PD) [1–8]. Optimal patients selection [4,9–11] and precise targeting based on electrophysiological studies [12–14] are essential for a successful outcome of STN stimulation. The procedure is usually carried out with the patient under local anesthesia (LA) because intraoperative evaluation of clinical signs ensures optimal placement of the electrodes [15,16]. Although the effects of anesthetic agents on the Corresponding author. Tel.: +81 96 373 5219; fax: +81 96 371 8064. E-mail address: [email protected] (K. Yamada).
1353-8020/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2006.07.008
microelectrode recordings are of concern [17], patients with severe anxiety and/or drug-induced psychosis are often unable to tolerate the operation under LA [16]. Presumably due to the ethnic characteristics, many Japanese patients treated with anti-parkinsonian medication develop psychosis and/or non-motor side effects [18–21]. To reduce stress in patients with psychiatric symptoms, we prefer to administer general anesthesia (GA) although this may render targeting of the STN less precise. In this retrospective study, we compared the effects of general inhalation anesthesia and of LA on the postoperative outcome in Japanese PD patients treated with STN stimulation. 2. Methods 2.1. Patients selection Between September 2001 and December 2004, 30 consecutive patients (11 males and 19 females) with advanced PD
ARTICLE IN PRESS 102
K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
underwent bilateral deep brain stimulation (DBS) of the STN at our institutes. All manifested idiopathic PD and responded to levodopa according to the criteria of the Core Assessment Program for Intracerebral Transplantation criteria [22]. Patients with severe dementia who scored 4 on the Unified Parkinson’s Disease Rating Scale (UPDRS) Part I item 1, scored less than 20 on the Mini Mental Scale, manifested uncontrolled major psychiatric symptoms (UPDRS-I item 2 ¼ 4), or severe depression (UPDRS-I item 3 ¼ 4) were considered ineligible for surgery [2,3,7,23–25]. We did not intentionally exclude patients over 70 years [3], if their general physical and psychiatric status were acceptable for surgery. We also excluded 1 male and 3 female PD patients who, in addition to STN stimulation, had undergone another stereotactic procedure that targeted the thalamus and/or globus pallidus internus. During the early period (September 2001–August 2002), all of 7 patients (2 males and 5 females) underwent staged placement of DBS leads under local infiltrative anesthesia. In September 2002, a male (case 8) with a moderate degree of psychosis became extremely anxious during placement of an electrode on the left side under LA; the contra lateral procedure was therefore performed under GA. In the subsequent period (October 2002–December 2004), we used general inhalation anesthesia in all 15 patients (6 males, 9 females) with psychosis and/or anxiety if we suspected that they might develop difficulties in tolerating the procedure under LA; 1 male and 2 females without psychiatric symptoms underwent the procedure under LA. We excluded case 8 from the outcome evaluation; therefore, the study population was comprised of 25 patients.
neuronal activity of the STN could be recorded in all 15 of these patients (Fig. 1). In 9 patients under LA and 4 under GA, the electrodes were implanted in staged procedures; 1 patient under LA and 11 under GA underwent bilateral procedures in a single operative session. After several days of test-stimulation, pulse generators (Medtronic, Soletora Model 7426 IPG) were subcutaneously implanted on the subclavian portion. Most of the patients were treated with unipolar stimulation using the contact 1 or 0. The stimulation parameters were 130– 160 Hz frequency and a pulse width 60–90 m s on both sides. 2.3. Evaluations The patients were scored on the UPDRS and Schwab & England (S-E) activities of daily living (ADL) scale. With respect to parkinsonian motor symptoms, we individually analyzed bradykinesia (UPDRS-III items 23–26; 0–32), tremor (UPDRS-III items 20 and 21; 0–28), rigidity (UPDRS-III item 22; 0–20), and axial symptoms (UPDRS-II items 13–15 and UPDRS-III items 29 and 30; 0–20) [9]. The score after a drug-free period exceeding 12 h was defined as the practical worst ‘‘off’’ state; the score at 1–2 h after the administration of the usual morning medications as the practical ‘‘on’’ state. Assessments were performed by three independent observers from our departments several days before and 3 months after the procedure. The levodopa-equivalent daily dose (LEDD) was computed for each anti-parkinsonian medication, including levodopa, by multiplying the total daily dosage of each drug by its potency relative to a standard levodopa/decarboxylase inhibitor (DCI) preparation being assigned a value of 1. The conversion factors for bromocriptine and pergolide were 10 and 100, respectively [5,18,29].
2.2. Surgery and anesthesia The procedure was carried out in accordance with good clinical practice after obtaining prior consent by the patients and their families. We used a magnetic resonance imaging (MRI)/microelectrode-guided technique with third ventriculography [26,27]. The tentative target site, determined by setting the coordinates, was 2 mm posterior to the midpoint of a line drawn between the anterior- and posterior commissures (AC– PC line) and 12 mm lateral, and 4 mm ventral to the AC–PC line. Semi-microelectrode recordings were obtained at all 1.0mm points along the trajectory toward the subthalamic target site to determine the relative physiologic position of the probe [28]. The trajectory that included more than four positive recording sites (4.0 mm) was chosen for placement of the DBS lead. Patients placed under LA (n ¼ 10) received electrical stimulation with a monopolar radiofrequency probe (diameter tip, 1 mm; uninsulated length, 2 mm) prior to placement of the DBS electrode (Medtronic, Model 3387). In the other patients (n ¼ 15), the entire procedure, except for placement of the head pins, was performed under endotracheal inhalation anesthesia. These patients were intubated under fiberscopic guidance and deeply anesthetized by the inhalation of a mixture of dinitrous oxide, oxygen, and sevoflurane (1.0–2.5%)(GOS); they also received fentanyl and/or propofol intravenously (i.v.). As in patients with LA, the characteristic
2.4. Statistics We used the paired Student’s t-test to compare parametric data and the Wilcoxon signed-rank test to compare UPDRS subscores and S-E scores before and after surgery. To compare the scores of the two groups we employed the Mann–Whitney U-test. All data were expressed as the mean7SD.
3. Results 3.1. Preoperative status of patients undergoing DBS under local or general As shown in Tables 1 and 2, the UPDRS-I psychiatric score was higher in the GA than the LA group, however, the difference was not statistically significant. There was no significant difference with respect to the age, UPDRS-II, III and the S-E ADL scores of the two groups. The individual motor symptoms in the GA group did not significantly differ from those in the LA group. However, the disease duration was longer and the UPDRS-IV score higher in the GA patients (po0.05).
ARTICLE IN PRESS K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
General Anesthesia
103
Local Anesthesia (Case 20)
(Case 18) -4 mm
ZI
-3 mm
-2 mm STN
STN -1 mm
SNr 0 mm
+1 mm
SNr 100 µV 100 msec
Fig. 1. Changes in the field potential along a trajectory through the subthalamic nucleus (STN) and surrounding structures. Representative cases under general- (patient 18) and local anesthesia (patient 20) are shown. The trajectory of the semi-microelectrode and the recording sites are drawn on a coronal brain section (nearest planes in the Schaltenbrand and Bailey atlas). Increased field potentials appear in both cases when the microelectrode probe passes through the zona incerta (ZI). At the substantia nigra pars reticulate (SNr), the field potential is significantly reduced. There is no specific difference between the two cases in the amplitude and pattern of discharge within the STN.
3.2. Peri-operative blood pressure changes in case 8 Preoperatively, this man had exhibited severe druginduced delusion. Reduced anti-parkinsonian medications and administration of quetiapine ameliorated his psychiatric symptoms, but a moderate degree of psychosis (UPDRS-I-2 ¼ 3) and depression (UPDRSI-3 ¼ 2) were remained. During DBS lead placement into the left STN under LA, he became severely anxious. As his systolic blood pressure exceeded 200 mm Hg at the start of the procedure, he received a continuous i.v. drip infusion of diltiazem (5–10 mg/kg/min) for the control of hypertension. Although his postoperative course was uneventful, we concluded that subsequent surgery to the contralateral side would be inadvisable without deep sedation. Under GA he remained normotensive and we were able to simultaneously implant DBS electrode in the right STN and the IPG. This patient was excluded from the retrospective assessment of treatment outcomes. 3.3. Postoperative findings Postoperatively, none of the patients exhibited permanent adverse effects such as motor weakness, sensory disturbance, oculomotor palsy, or cognitive decline. Transient effects were effectively treated by modifying their anti-parkinsonian medications, or by changing the
Table 1 Patient characteristics Characteristics
General anesthesia
Local anesthesia
Sex (number of patients) Male Female
6 9
3 7
Age (years) Mean7SD Range
65.277.0 50–73
65.678.6 51–71
Duration of disease (years) Mean7SD Range
11.175.0* 3–19
6.872.4* 3–11
Pre OP. medications (mg/day) Levodopa and DCI Mean7SD 320.77144.1 Range 100–600
400.07163.9 150–600
LEDD (mg) Mean7SD Range
425.07171.8 150–630
375.77195.6 100–750
LEDD—levodopa-equivalent daily dose; DCI—decarboxylase inhibitor; SD—standard deviations.*significantly different in two groups, po0.05, Student’s t-test.
DBS parameters. There were no infectious complications within the first 3 postoperative months although two patients in the LA group manifested skin erosion
ARTICLE IN PRESS 104
K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
Table 2 Parkinsonian symptoms at preoperative base line and 3 months after STN stimulation Scores
General anesthesia Baseline
Local anesthesia 3 months
Baseline
3 months
UPDRS-I
On Off
2.572.2 4.074.5
1.372.0** 1.372.0**
1.672.9 1.973.4
1.372.5 1.372.5
UPDRS-II
On Off
13.278.3 26.1710.3
5.374.4** 6.677.0**
12.077.1 20.479.3
3.374.1** 4.074.0**
UPDRS-III
On Off
30.4718.2 52.4719.0
9.975.3** 14.3715.4**
28.7710.6 45.9717.7
6.176.9** 7.177.0**
Bradykinesia
On Off
10.375.6 17.577.3
4.473.0** 6.575.4a,**
8.273.0 14.877.7
1.972.9* 1.972.9a,*
Tremor
On Off
3.973.7 7.174.9
0.971.2** 1.772.4**
6.875.3 9.276.4
1.070.9* 1.070.9*
Rigidity
On Off
6.074.7 9.774.9
0.771.8** 1.173.3**
6.072.8 8.974.8
0.170.3* 0.170.3*
Axial symptoms
On Off
7.975.1 16.075.0
2.972.8** 3.874.1**
6.274.7 11.476.0
1.973.2** 1.973.2**
UPDRS-IV
5.873.9b
1.871.1c,**
2.672.2b
0.671.3c,*
Dyskinesias
1.973.0
0.370.6*
0.571.0
0.170.3
d
d
Clinical fluctuations
3.572.0
0.771.0*
1.771.9
Nausea
0.070.0
0.070.0
0.070.0
0.070.0
Sleep disorders
0.570.5
0.570.5
0.270.4
0.070.0e
Orthostasis
0.170.3
0.170.3
0.270.4
0.070.0
S-E ADL
On Off
70.0717.7 42.7720.9
e
0.170.3*
87.378.8** 84.0716.8**
74.4713.3 56.7722.4
90.0715.0** 87.8714.8**
UPDRS—Unified Parkinson’s Disease Rating Scale; S-E—Schwab-England ADL scale.*Significantly different from scores at preoperative baseline, *po0.05,**po0.01, Wilcoxon signed-rank test. a, b, c, d, and e: significantly different in two groups, a, d, and e; po0.05, b and c; po0.01, Mann–Whitney U-test.
and subcutaneous abscess formation around the connector during the follow-up period. The anti-parkinsonian drug doses could be reduced significantly as the parkinsonian symptoms were ameliorated by chronic STN-DBS. At 3 months after the procedure, there was a significant reduction in the mean dosage of levodopa/DCI and LEDD in both groups (po0.05, Table 3). The levodopa dese-reduction was greater in the LA than GA group (38.2% vs. 16.6%). Compared to the preoperative baseline, at 3 months postoperatively, the UPDRS-II, III, and IV scores in both the ‘on’ and ‘off’ state were significantly lower in both groups, all aspects of motor symptoms including bradykinesia, tremor, rigidity, and axial symptoms were significantly improved as were the S-E scores in both the ‘on’ and ‘off’ state. There was no significant difference between the two groups with respect to postoperative UPDRS-I, II, and
III scores, all individual motor symptoms rated on the UPDRS, S-E ADL score, the levodopa dosage, and LEDD. UPDRS-IV continued to be higher in the GA group (Table 2) and the LA group showed greater improvements in bradykinesia, tremor, rigidity, and axial symptoms, however, except for bradykinesia in the ‘off’ state, the difference was not statistically significant (Fig. 2). In both groups, bilateral STN-DBS yielded almost the same degree of improvement in the S-E ADL and UPDRS-II score.
3.4. Stimulation amplitude at 3 months after the procedure Slightly higher amplitudes were used in the GA than LA group [2.3970.45 V (right), 2.3370.44 V (left) vs. 2.2470.57 V (right), 2.1270.65 V (left)], however, the difference was not statistically significant.
ARTICLE IN PRESS K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
105
Table 3 Pre- and 3 months postoperative treatments Treatments
General anesthesia
Local anesthesia
Pre OP.
3 months
Pre OP.
3 months
Levodopa/DCI (mg)
320.77144.1
260.07129.8*
400.07163.9
233.37147.9**
LEDD (mg)
375.77195.6
303.37164.7**
425.07171.8
261.17164.0**
Stimulating amplitude Rt. (V) Lt. (V)
— —
2.3970.45 2.3370.44
— —
2.2470.57 2.1270.65
*Significantly different from scores at preoperative Baseline; *po0.05, **po0.01, Student’s t-test.
200 ON
% Improvement
OFF
* 100 *
0 Bradykinesia Tremor
Rigidity
Axial Symptoms
S-E ADL
General Anesthesia Group
Bradykinesia Tremor
Rigidity
Axial Symptoms
S-E ADL
Local Anesthesia Group
Fig. 2. Improvements in the UPDRS motor score and S-E ADL scale 3 months after bilateral STN stimulation. While the improvement rate for bradykinesia, tremor, rigidity, and axial symptoms is somewhat better in the local anesthesia group, the difference was not statistically significant except for bradykinesia in ‘off’ state. The improvement rate of the S-E ADL scale in the ‘off’ state is rather higher in the general anesthesia group. However, the difference is not significant. Asterix: significantly different between the twp groups, *po0.05, Mann–Whitney U-test.
4. Discussion Of 26 Japanese patients reported here (including case 8), 18 experienced at least one drug-induced side effect such as psychosis, dyskinesia, or nausea, although the administered levodopa doses were markedly lower than those used in Western countries [2,3,5,7,8,25]. We speculate that their ethnic background might render Oriental less tolerant that Caucasians to anti-parkinsonian medications [18–20]. Compared to the LA group, the disease duration was longer in our GA patients and they had significantly higher scores for the side-effects of levodopa therapy (UPDRS-IV) and worse scores for psychiatric symptoms (UPDRS-I). This supports the hypothesis that long-term medical therapy may be one of the factors involved in the manifestation of psychiatric problems by PD patients [21].
Stereotactic functional surgery under LA may be inadvisable in patients with psychiatric problems. Our patient number 8 is a case in point. Although we were able to complete the procedure uneventfully under LA, anxiety-induced hypertension may increase the risk of perioperative complications such as intracranial hemorrhage. While adequate sedation reduces mental stress, we must always be aware of respiratory complications, as the presence of the Leksell frame may make the airway difficult to access during the operation [17]. From this perspective, endotracheal inhalation anesthesia may be the better alternative because the airway is secured and ventilation is stable during the stereotactic procedure. However, we should as well be cautious for complications of inhalation GA that affect on musculoskeletal, cardiovascular, or pulmonary systems.
ARTICLE IN PRESS 106
K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
We found that in our two groups, with the exception of bradykinesia in the ‘off’ state, there was no significant difference in the postoperative improvement rate (%) of the UPDRS motor scores. Moreover, the use of GA had no negative effect on the postoperative S-E ADL scores, whereas amplitude of STN stimulation was not significantly different between two groups. Our method of delivering GA did not interfere with the identification of the dorsal and ventral margins of the STN by microelectrode recordings (Fig. 1), which is necessary for the precise placement of the DBS electrode and the achievement of a favorable outcome. On the other hand, GA renders intraoperative clinical evaluation impossible and this may have a worse effect on post-procedure improvement of bradykinesia in ‘off’ state [16]. Houeto et al. [15] reported that the improvement of segmental akinesia provoked by intraoperative stimulation was significantly correlated with the postoperative improvement of akinesia, although it was not a predictor of the postoperative outcome with respect to axial symptoms. The intraoperative evaluation of axial features is highly limited even under LA, because recumbent patients are fixed to the stereotactic frame and the adaptive headrest. Therefore, we suggest that with respect to axial symptoms, intraoperative assessment may not play a significant role in the postoperative outcome. Our results suggest that GA compares favorably with LA with respect to both safety and effectiveness in bilateral STN-DBS procedures. While prospective studies on larger patient groups are needed to elucidate the benefits and risks of each anesthetic method, GA is a viable option in patients undergoing stereotactic surgery for STN stimulation, especially patients with psychiatric problems.
Acknowledgment This work was supported by a Grant-in-Aid for Scientific Research (15500240) and by a Center of Excellence grant (16101J-1) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. References [1] Houeto JL, Damier P, Bejjani PB, Staedler C, Bonnet AM, Arnulf I, et al. Subthalamic stimulation in Parkinson disease: a multidisciplinary approach. Arch Neurol 2000;57:461–5. [2] Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Eng J Med 1998;339:1105–11. [3] Krack P, Batir A, van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Eng J Med 2003;349:1925–34.
[4] Moro E, Esselink RJA, Benabid AL, Pollak P. Response to levodopa in parkinsonian patients with bilateral subthalamic nucleus stimulation. Brain 2002;125:2408–17. [5] Moro E, Scerrati M, Romito LMA, Roselli R, Tonali P, Albanese A. Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease. Neurology 1999;53:85. [6] Østergaard K, Sunde N, Dupont E. Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson’s disease and motor fluctuations. Movement Disord 2002;17:693–700. [7] The deep-brain stimulation for Parkinson’s disease study group. Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus Pallidus in Parkinson’s disease. N Eng J Med 2001;345:956–63. [8] Vingerhoets FJG, Villemure J-G, Temperli P, Pollo C, Pralong E, Ghika J. Subthalamic DBS replaces levodopa in Parkinson’s disease. Two-year follow-up. Neurology 2002;58:396–401. [9] Charles PD, Van Blercom N, Krack P, Lee SL, Xie J, Besson G, et al. Predictors of effective bilateral subthalamic nucleus stimulation for PD. Neurology 2002;59:932–4. [10] Kleiner-Fisman G, Fisman DN, Sime E, Saint-Cyr JA, Lozano AM, Lang AE. Long-term follow up of bilateral deep brain stimulation of the subthalamic nucleus in patients with advanced Parkinson disease. J Neurosurg 2003;99:489–95. [11] Welter ML, Houeto JL, Tezenas du Montcel S, Mesnage V, Bonnet AM, Pillon B, et al. Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 2002;125: 575–83. [12] Bejjani BP, Dormont D, Pidoux B, Yelnik J, Damier P, Arnulf I, et al. Bilateral subthalamic stimulation for Parkinson’s disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 2000;92:615–25. [13] Hutchison WD, Allan RJ, Opitz H, Levy R, Dostrovsky JO, Lang AE, et al. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease. Ann Neurol 1998;44: 622–8. [14] Rodriguez-Oroz MC, Rodriguez M, Guridi J, Mewes K, Chockkman V, Vitek J, et al. The subthalamic nucleus in Parkinson’s disease: somatotopic organization and physiological characteristics. Brain 2001;124:1777–90. [15] Houeto JL, Welter ML, Bejjani PB, Tezenas du Montcel S, Bonnet AM, Mesnage V, et al. Subthalamic stimulation in Parkinson Disease. intraoperative predictive factors. Arch Neurol 2003;60:690–4. [16] Malteˆte D, Navarro S, Welter M-L, Roche S, Bonnet A-M, Houeto J-L, et al. Subthalamic stimulation in Parkinson disease. with or without anesthesia? Arch Neurol 2004;61:390–2. [17] Venkatraghavan L, Manninen P, Mak P, Lukitto K, Hodaie M, Lozano A. Anesthesia for functional neurosurgery. Review of complications. J Neurosurg Anesthesiol 2006;18:64–7. [18] Katayama Y, Kasai M, Oshima H, Fukaya C, Yamamato T, Ogawa K, et al. Subthalamic nucleus stimulation for Parkinson disease: benefits observed in levodopa-intolerant patients. J Neurosurg 2001;95:213–21. [19] Rivera-Calimlim L, Reilly DK. Difference in erythrocyte catechol-O-methyltransferase activity between Orentals and Caucasians: difference in levodopa tolerance. Clin Pharmacol Ther 1984;35:804–9. [20] Yamada K, Goto S, Ushio Y. GPi pallidotomy for Parkinson’s disease with drug-induced psychosis. Parkinsonism Relat Disord 2003;10:35–40. [21] Poewe W. Psychosis in Parkinson’s disease. Movement Disord 2003;18(Suppl 6):S80–7. [22] Langston JW, Widner H, Goetz CG, Brooks D, Fahn S, Freeman T, et al. Core assessment program for intracerebral transplantation (CAPIT). Movement Disord 1992;7:2–13.
ARTICLE IN PRESS K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107 [23] Saint-Cyr JA, Tre´panier LL, Kumar R, Lozano AM, Lang AE. Neuropsychological consequence of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain 2000;123: 2091–108. [24] Limousin-Dowsey P, Pollak P, Van Blercom N. Thalamic, subthalamic nucleus and internal pallidum stimulation in Parkinson’s disease. J Neurol 1999;246(Suppl 2): II42–5. [25] Simuni T, Jaggi JL, Mulholland H, Hurtig H, Colcher A, Siderowf AD, et al. Bilateral stimulation of the subthalamic nucleus in patients with Parkinson’s disease: a study of efficacy and safety. J Neurosurg 2002;96:666–72.
107
[26] Goto S, Yamada K, Ushio Y. Subthalamic nucleus stimulation in a parkinsonian patient with previous bilateral thalamotomy. J Neurol Neurosurg Psychiat 2004;75:163–71. [27] Yamada K, Goto S. Bilateral subthalamic nucleus stimulation results in reversal of alopecia in Parkinson’s disease. Parkinsonism Relat Disord 2004;10:353–5. [28] Benazzouz A, Breit S, Koudsie A, Pollak P, Krack P, Benabid AL. Intraoperative microrecordings of the subthalamic nucleus in Parkinson’s disease. Movement Disord 2002;17(Suppl 3):S145–9. [29] Romito LM, Scerrati M, Contarino MF, Bentivoglio AR, Tonali P, Albanese A. Long-term follow up of subthalamic nucleus stimulation in Parkinson’s disease. Neurology 2002;58:1546–50.
Parkinsonism and Related Disorders 13 (2007) 101–107 www.elsevier.com/locate/parkreldis
Stereotactic surgery for subthalamic nucleus stimulation under general anesthesia: A retrospective evaluation of Japanese patients with Parkinson’s disease Kazumichi Yamadaa,, Satoshi Gotoa, Jun-ichi Kuratsua, Kazuhito Matsuzakib, Tetsuya Tamurab, Shinji Nagahirob, Nagako Murasec, Hideki Shimazuc, Ryuji Kajic a
Department of Neurosurgery, Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Kumamoto City 860-8556, Kumamoto, Japan b Department of Neurological Surgery, Graduate School of Medicine, The University of Tokushima, Japan c Department of Clinical Neuroscience, Graduate School of Medicine, The University of Tokushima, Japan Received 10 April 2006; received in revised form 20 June 2006; accepted 12 July 2006
Abstract We compared retrospectively the outcome of bilateral subthalamic nucleus (STN) stimulation in 15 patients with Parkinson’s disease who underwent the procedure under general anesthesia (GA) with that achieved in 10 patients under local anesthesia (LA). At 3 months postoperatively, all cardinal parkinsonian motor symptoms, evaluated on Unified Parkinson’s Disease Rating Scale were significantly improved compared to preoperative baselines in both groups. The administration of GA did not adversely affect postoperative improvements in motor and daily activity scores, except for off-medication bradykinesia. Our results suggest that GA compares favorably with LA in surgical procedure for bilateral STN stimulation. r 2006 Elsevier Ltd. All rights reserved. Keywords: Anxiety; Deep brain stimulation; Drug-induced psychosis; General anesthesia; Parkinson’s disease; Subthalamic nucleus
1. Introduction Continuous high-frequency stimulation of the bilateral subthalamic nucleus (STN) is now widely accepted as a procedure that strikingly improves motor symptoms and levodopa-induced motor complications in patients with Parkinson’s disease (PD) [1–8]. Optimal patients selection [4,9–11] and precise targeting based on electrophysiological studies [12–14] are essential for a successful outcome of STN stimulation. The procedure is usually carried out with the patient under local anesthesia (LA) because intraoperative evaluation of clinical signs ensures optimal placement of the electrodes [15,16]. Although the effects of anesthetic agents on the Corresponding author. Tel.: +81 96 373 5219; fax: +81 96 371 8064. E-mail address: [email protected] (K. Yamada).
1353-8020/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2006.07.008
microelectrode recordings are of concern [17], patients with severe anxiety and/or drug-induced psychosis are often unable to tolerate the operation under LA [16]. Presumably due to the ethnic characteristics, many Japanese patients treated with anti-parkinsonian medication develop psychosis and/or non-motor side effects [18–21]. To reduce stress in patients with psychiatric symptoms, we prefer to administer general anesthesia (GA) although this may render targeting of the STN less precise. In this retrospective study, we compared the effects of general inhalation anesthesia and of LA on the postoperative outcome in Japanese PD patients treated with STN stimulation. 2. Methods 2.1. Patients selection Between September 2001 and December 2004, 30 consecutive patients (11 males and 19 females) with advanced PD
ARTICLE IN PRESS 102
K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
underwent bilateral deep brain stimulation (DBS) of the STN at our institutes. All manifested idiopathic PD and responded to levodopa according to the criteria of the Core Assessment Program for Intracerebral Transplantation criteria [22]. Patients with severe dementia who scored 4 on the Unified Parkinson’s Disease Rating Scale (UPDRS) Part I item 1, scored less than 20 on the Mini Mental Scale, manifested uncontrolled major psychiatric symptoms (UPDRS-I item 2 ¼ 4), or severe depression (UPDRS-I item 3 ¼ 4) were considered ineligible for surgery [2,3,7,23–25]. We did not intentionally exclude patients over 70 years [3], if their general physical and psychiatric status were acceptable for surgery. We also excluded 1 male and 3 female PD patients who, in addition to STN stimulation, had undergone another stereotactic procedure that targeted the thalamus and/or globus pallidus internus. During the early period (September 2001–August 2002), all of 7 patients (2 males and 5 females) underwent staged placement of DBS leads under local infiltrative anesthesia. In September 2002, a male (case 8) with a moderate degree of psychosis became extremely anxious during placement of an electrode on the left side under LA; the contra lateral procedure was therefore performed under GA. In the subsequent period (October 2002–December 2004), we used general inhalation anesthesia in all 15 patients (6 males, 9 females) with psychosis and/or anxiety if we suspected that they might develop difficulties in tolerating the procedure under LA; 1 male and 2 females without psychiatric symptoms underwent the procedure under LA. We excluded case 8 from the outcome evaluation; therefore, the study population was comprised of 25 patients.
neuronal activity of the STN could be recorded in all 15 of these patients (Fig. 1). In 9 patients under LA and 4 under GA, the electrodes were implanted in staged procedures; 1 patient under LA and 11 under GA underwent bilateral procedures in a single operative session. After several days of test-stimulation, pulse generators (Medtronic, Soletora Model 7426 IPG) were subcutaneously implanted on the subclavian portion. Most of the patients were treated with unipolar stimulation using the contact 1 or 0. The stimulation parameters were 130– 160 Hz frequency and a pulse width 60–90 m s on both sides. 2.3. Evaluations The patients were scored on the UPDRS and Schwab & England (S-E) activities of daily living (ADL) scale. With respect to parkinsonian motor symptoms, we individually analyzed bradykinesia (UPDRS-III items 23–26; 0–32), tremor (UPDRS-III items 20 and 21; 0–28), rigidity (UPDRS-III item 22; 0–20), and axial symptoms (UPDRS-II items 13–15 and UPDRS-III items 29 and 30; 0–20) [9]. The score after a drug-free period exceeding 12 h was defined as the practical worst ‘‘off’’ state; the score at 1–2 h after the administration of the usual morning medications as the practical ‘‘on’’ state. Assessments were performed by three independent observers from our departments several days before and 3 months after the procedure. The levodopa-equivalent daily dose (LEDD) was computed for each anti-parkinsonian medication, including levodopa, by multiplying the total daily dosage of each drug by its potency relative to a standard levodopa/decarboxylase inhibitor (DCI) preparation being assigned a value of 1. The conversion factors for bromocriptine and pergolide were 10 and 100, respectively [5,18,29].
2.2. Surgery and anesthesia The procedure was carried out in accordance with good clinical practice after obtaining prior consent by the patients and their families. We used a magnetic resonance imaging (MRI)/microelectrode-guided technique with third ventriculography [26,27]. The tentative target site, determined by setting the coordinates, was 2 mm posterior to the midpoint of a line drawn between the anterior- and posterior commissures (AC– PC line) and 12 mm lateral, and 4 mm ventral to the AC–PC line. Semi-microelectrode recordings were obtained at all 1.0mm points along the trajectory toward the subthalamic target site to determine the relative physiologic position of the probe [28]. The trajectory that included more than four positive recording sites (4.0 mm) was chosen for placement of the DBS lead. Patients placed under LA (n ¼ 10) received electrical stimulation with a monopolar radiofrequency probe (diameter tip, 1 mm; uninsulated length, 2 mm) prior to placement of the DBS electrode (Medtronic, Model 3387). In the other patients (n ¼ 15), the entire procedure, except for placement of the head pins, was performed under endotracheal inhalation anesthesia. These patients were intubated under fiberscopic guidance and deeply anesthetized by the inhalation of a mixture of dinitrous oxide, oxygen, and sevoflurane (1.0–2.5%)(GOS); they also received fentanyl and/or propofol intravenously (i.v.). As in patients with LA, the characteristic
2.4. Statistics We used the paired Student’s t-test to compare parametric data and the Wilcoxon signed-rank test to compare UPDRS subscores and S-E scores before and after surgery. To compare the scores of the two groups we employed the Mann–Whitney U-test. All data were expressed as the mean7SD.
3. Results 3.1. Preoperative status of patients undergoing DBS under local or general As shown in Tables 1 and 2, the UPDRS-I psychiatric score was higher in the GA than the LA group, however, the difference was not statistically significant. There was no significant difference with respect to the age, UPDRS-II, III and the S-E ADL scores of the two groups. The individual motor symptoms in the GA group did not significantly differ from those in the LA group. However, the disease duration was longer and the UPDRS-IV score higher in the GA patients (po0.05).
ARTICLE IN PRESS K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
General Anesthesia
103
Local Anesthesia (Case 20)
(Case 18) -4 mm
ZI
-3 mm
-2 mm STN
STN -1 mm
SNr 0 mm
+1 mm
SNr 100 µV 100 msec
Fig. 1. Changes in the field potential along a trajectory through the subthalamic nucleus (STN) and surrounding structures. Representative cases under general- (patient 18) and local anesthesia (patient 20) are shown. The trajectory of the semi-microelectrode and the recording sites are drawn on a coronal brain section (nearest planes in the Schaltenbrand and Bailey atlas). Increased field potentials appear in both cases when the microelectrode probe passes through the zona incerta (ZI). At the substantia nigra pars reticulate (SNr), the field potential is significantly reduced. There is no specific difference between the two cases in the amplitude and pattern of discharge within the STN.
3.2. Peri-operative blood pressure changes in case 8 Preoperatively, this man had exhibited severe druginduced delusion. Reduced anti-parkinsonian medications and administration of quetiapine ameliorated his psychiatric symptoms, but a moderate degree of psychosis (UPDRS-I-2 ¼ 3) and depression (UPDRSI-3 ¼ 2) were remained. During DBS lead placement into the left STN under LA, he became severely anxious. As his systolic blood pressure exceeded 200 mm Hg at the start of the procedure, he received a continuous i.v. drip infusion of diltiazem (5–10 mg/kg/min) for the control of hypertension. Although his postoperative course was uneventful, we concluded that subsequent surgery to the contralateral side would be inadvisable without deep sedation. Under GA he remained normotensive and we were able to simultaneously implant DBS electrode in the right STN and the IPG. This patient was excluded from the retrospective assessment of treatment outcomes. 3.3. Postoperative findings Postoperatively, none of the patients exhibited permanent adverse effects such as motor weakness, sensory disturbance, oculomotor palsy, or cognitive decline. Transient effects were effectively treated by modifying their anti-parkinsonian medications, or by changing the
Table 1 Patient characteristics Characteristics
General anesthesia
Local anesthesia
Sex (number of patients) Male Female
6 9
3 7
Age (years) Mean7SD Range
65.277.0 50–73
65.678.6 51–71
Duration of disease (years) Mean7SD Range
11.175.0* 3–19
6.872.4* 3–11
Pre OP. medications (mg/day) Levodopa and DCI Mean7SD 320.77144.1 Range 100–600
400.07163.9 150–600
LEDD (mg) Mean7SD Range
425.07171.8 150–630
375.77195.6 100–750
LEDD—levodopa-equivalent daily dose; DCI—decarboxylase inhibitor; SD—standard deviations.*significantly different in two groups, po0.05, Student’s t-test.
DBS parameters. There were no infectious complications within the first 3 postoperative months although two patients in the LA group manifested skin erosion
ARTICLE IN PRESS 104
K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
Table 2 Parkinsonian symptoms at preoperative base line and 3 months after STN stimulation Scores
General anesthesia Baseline
Local anesthesia 3 months
Baseline
3 months
UPDRS-I
On Off
2.572.2 4.074.5
1.372.0** 1.372.0**
1.672.9 1.973.4
1.372.5 1.372.5
UPDRS-II
On Off
13.278.3 26.1710.3
5.374.4** 6.677.0**
12.077.1 20.479.3
3.374.1** 4.074.0**
UPDRS-III
On Off
30.4718.2 52.4719.0
9.975.3** 14.3715.4**
28.7710.6 45.9717.7
6.176.9** 7.177.0**
Bradykinesia
On Off
10.375.6 17.577.3
4.473.0** 6.575.4a,**
8.273.0 14.877.7
1.972.9* 1.972.9a,*
Tremor
On Off
3.973.7 7.174.9
0.971.2** 1.772.4**
6.875.3 9.276.4
1.070.9* 1.070.9*
Rigidity
On Off
6.074.7 9.774.9
0.771.8** 1.173.3**
6.072.8 8.974.8
0.170.3* 0.170.3*
Axial symptoms
On Off
7.975.1 16.075.0
2.972.8** 3.874.1**
6.274.7 11.476.0
1.973.2** 1.973.2**
UPDRS-IV
5.873.9b
1.871.1c,**
2.672.2b
0.671.3c,*
Dyskinesias
1.973.0
0.370.6*
0.571.0
0.170.3
d
d
Clinical fluctuations
3.572.0
0.771.0*
1.771.9
Nausea
0.070.0
0.070.0
0.070.0
0.070.0
Sleep disorders
0.570.5
0.570.5
0.270.4
0.070.0e
Orthostasis
0.170.3
0.170.3
0.270.4
0.070.0
S-E ADL
On Off
70.0717.7 42.7720.9
e
0.170.3*
87.378.8** 84.0716.8**
74.4713.3 56.7722.4
90.0715.0** 87.8714.8**
UPDRS—Unified Parkinson’s Disease Rating Scale; S-E—Schwab-England ADL scale.*Significantly different from scores at preoperative baseline, *po0.05,**po0.01, Wilcoxon signed-rank test. a, b, c, d, and e: significantly different in two groups, a, d, and e; po0.05, b and c; po0.01, Mann–Whitney U-test.
and subcutaneous abscess formation around the connector during the follow-up period. The anti-parkinsonian drug doses could be reduced significantly as the parkinsonian symptoms were ameliorated by chronic STN-DBS. At 3 months after the procedure, there was a significant reduction in the mean dosage of levodopa/DCI and LEDD in both groups (po0.05, Table 3). The levodopa dese-reduction was greater in the LA than GA group (38.2% vs. 16.6%). Compared to the preoperative baseline, at 3 months postoperatively, the UPDRS-II, III, and IV scores in both the ‘on’ and ‘off’ state were significantly lower in both groups, all aspects of motor symptoms including bradykinesia, tremor, rigidity, and axial symptoms were significantly improved as were the S-E scores in both the ‘on’ and ‘off’ state. There was no significant difference between the two groups with respect to postoperative UPDRS-I, II, and
III scores, all individual motor symptoms rated on the UPDRS, S-E ADL score, the levodopa dosage, and LEDD. UPDRS-IV continued to be higher in the GA group (Table 2) and the LA group showed greater improvements in bradykinesia, tremor, rigidity, and axial symptoms, however, except for bradykinesia in the ‘off’ state, the difference was not statistically significant (Fig. 2). In both groups, bilateral STN-DBS yielded almost the same degree of improvement in the S-E ADL and UPDRS-II score.
3.4. Stimulation amplitude at 3 months after the procedure Slightly higher amplitudes were used in the GA than LA group [2.3970.45 V (right), 2.3370.44 V (left) vs. 2.2470.57 V (right), 2.1270.65 V (left)], however, the difference was not statistically significant.
ARTICLE IN PRESS K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
105
Table 3 Pre- and 3 months postoperative treatments Treatments
General anesthesia
Local anesthesia
Pre OP.
3 months
Pre OP.
3 months
Levodopa/DCI (mg)
320.77144.1
260.07129.8*
400.07163.9
233.37147.9**
LEDD (mg)
375.77195.6
303.37164.7**
425.07171.8
261.17164.0**
Stimulating amplitude Rt. (V) Lt. (V)
— —
2.3970.45 2.3370.44
— —
2.2470.57 2.1270.65
*Significantly different from scores at preoperative Baseline; *po0.05, **po0.01, Student’s t-test.
200 ON
% Improvement
OFF
* 100 *
0 Bradykinesia Tremor
Rigidity
Axial Symptoms
S-E ADL
General Anesthesia Group
Bradykinesia Tremor
Rigidity
Axial Symptoms
S-E ADL
Local Anesthesia Group
Fig. 2. Improvements in the UPDRS motor score and S-E ADL scale 3 months after bilateral STN stimulation. While the improvement rate for bradykinesia, tremor, rigidity, and axial symptoms is somewhat better in the local anesthesia group, the difference was not statistically significant except for bradykinesia in ‘off’ state. The improvement rate of the S-E ADL scale in the ‘off’ state is rather higher in the general anesthesia group. However, the difference is not significant. Asterix: significantly different between the twp groups, *po0.05, Mann–Whitney U-test.
4. Discussion Of 26 Japanese patients reported here (including case 8), 18 experienced at least one drug-induced side effect such as psychosis, dyskinesia, or nausea, although the administered levodopa doses were markedly lower than those used in Western countries [2,3,5,7,8,25]. We speculate that their ethnic background might render Oriental less tolerant that Caucasians to anti-parkinsonian medications [18–20]. Compared to the LA group, the disease duration was longer in our GA patients and they had significantly higher scores for the side-effects of levodopa therapy (UPDRS-IV) and worse scores for psychiatric symptoms (UPDRS-I). This supports the hypothesis that long-term medical therapy may be one of the factors involved in the manifestation of psychiatric problems by PD patients [21].
Stereotactic functional surgery under LA may be inadvisable in patients with psychiatric problems. Our patient number 8 is a case in point. Although we were able to complete the procedure uneventfully under LA, anxiety-induced hypertension may increase the risk of perioperative complications such as intracranial hemorrhage. While adequate sedation reduces mental stress, we must always be aware of respiratory complications, as the presence of the Leksell frame may make the airway difficult to access during the operation [17]. From this perspective, endotracheal inhalation anesthesia may be the better alternative because the airway is secured and ventilation is stable during the stereotactic procedure. However, we should as well be cautious for complications of inhalation GA that affect on musculoskeletal, cardiovascular, or pulmonary systems.
ARTICLE IN PRESS 106
K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107
We found that in our two groups, with the exception of bradykinesia in the ‘off’ state, there was no significant difference in the postoperative improvement rate (%) of the UPDRS motor scores. Moreover, the use of GA had no negative effect on the postoperative S-E ADL scores, whereas amplitude of STN stimulation was not significantly different between two groups. Our method of delivering GA did not interfere with the identification of the dorsal and ventral margins of the STN by microelectrode recordings (Fig. 1), which is necessary for the precise placement of the DBS electrode and the achievement of a favorable outcome. On the other hand, GA renders intraoperative clinical evaluation impossible and this may have a worse effect on post-procedure improvement of bradykinesia in ‘off’ state [16]. Houeto et al. [15] reported that the improvement of segmental akinesia provoked by intraoperative stimulation was significantly correlated with the postoperative improvement of akinesia, although it was not a predictor of the postoperative outcome with respect to axial symptoms. The intraoperative evaluation of axial features is highly limited even under LA, because recumbent patients are fixed to the stereotactic frame and the adaptive headrest. Therefore, we suggest that with respect to axial symptoms, intraoperative assessment may not play a significant role in the postoperative outcome. Our results suggest that GA compares favorably with LA with respect to both safety and effectiveness in bilateral STN-DBS procedures. While prospective studies on larger patient groups are needed to elucidate the benefits and risks of each anesthetic method, GA is a viable option in patients undergoing stereotactic surgery for STN stimulation, especially patients with psychiatric problems.
Acknowledgment This work was supported by a Grant-in-Aid for Scientific Research (15500240) and by a Center of Excellence grant (16101J-1) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. References [1] Houeto JL, Damier P, Bejjani PB, Staedler C, Bonnet AM, Arnulf I, et al. Subthalamic stimulation in Parkinson disease: a multidisciplinary approach. Arch Neurol 2000;57:461–5. [2] Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Eng J Med 1998;339:1105–11. [3] Krack P, Batir A, van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Eng J Med 2003;349:1925–34.
[4] Moro E, Esselink RJA, Benabid AL, Pollak P. Response to levodopa in parkinsonian patients with bilateral subthalamic nucleus stimulation. Brain 2002;125:2408–17. [5] Moro E, Scerrati M, Romito LMA, Roselli R, Tonali P, Albanese A. Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease. Neurology 1999;53:85. [6] Østergaard K, Sunde N, Dupont E. Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson’s disease and motor fluctuations. Movement Disord 2002;17:693–700. [7] The deep-brain stimulation for Parkinson’s disease study group. Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus Pallidus in Parkinson’s disease. N Eng J Med 2001;345:956–63. [8] Vingerhoets FJG, Villemure J-G, Temperli P, Pollo C, Pralong E, Ghika J. Subthalamic DBS replaces levodopa in Parkinson’s disease. Two-year follow-up. Neurology 2002;58:396–401. [9] Charles PD, Van Blercom N, Krack P, Lee SL, Xie J, Besson G, et al. Predictors of effective bilateral subthalamic nucleus stimulation for PD. Neurology 2002;59:932–4. [10] Kleiner-Fisman G, Fisman DN, Sime E, Saint-Cyr JA, Lozano AM, Lang AE. Long-term follow up of bilateral deep brain stimulation of the subthalamic nucleus in patients with advanced Parkinson disease. J Neurosurg 2003;99:489–95. [11] Welter ML, Houeto JL, Tezenas du Montcel S, Mesnage V, Bonnet AM, Pillon B, et al. Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 2002;125: 575–83. [12] Bejjani BP, Dormont D, Pidoux B, Yelnik J, Damier P, Arnulf I, et al. Bilateral subthalamic stimulation for Parkinson’s disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 2000;92:615–25. [13] Hutchison WD, Allan RJ, Opitz H, Levy R, Dostrovsky JO, Lang AE, et al. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease. Ann Neurol 1998;44: 622–8. [14] Rodriguez-Oroz MC, Rodriguez M, Guridi J, Mewes K, Chockkman V, Vitek J, et al. The subthalamic nucleus in Parkinson’s disease: somatotopic organization and physiological characteristics. Brain 2001;124:1777–90. [15] Houeto JL, Welter ML, Bejjani PB, Tezenas du Montcel S, Bonnet AM, Mesnage V, et al. Subthalamic stimulation in Parkinson Disease. intraoperative predictive factors. Arch Neurol 2003;60:690–4. [16] Malteˆte D, Navarro S, Welter M-L, Roche S, Bonnet A-M, Houeto J-L, et al. Subthalamic stimulation in Parkinson disease. with or without anesthesia? Arch Neurol 2004;61:390–2. [17] Venkatraghavan L, Manninen P, Mak P, Lukitto K, Hodaie M, Lozano A. Anesthesia for functional neurosurgery. Review of complications. J Neurosurg Anesthesiol 2006;18:64–7. [18] Katayama Y, Kasai M, Oshima H, Fukaya C, Yamamato T, Ogawa K, et al. Subthalamic nucleus stimulation for Parkinson disease: benefits observed in levodopa-intolerant patients. J Neurosurg 2001;95:213–21. [19] Rivera-Calimlim L, Reilly DK. Difference in erythrocyte catechol-O-methyltransferase activity between Orentals and Caucasians: difference in levodopa tolerance. Clin Pharmacol Ther 1984;35:804–9. [20] Yamada K, Goto S, Ushio Y. GPi pallidotomy for Parkinson’s disease with drug-induced psychosis. Parkinsonism Relat Disord 2003;10:35–40. [21] Poewe W. Psychosis in Parkinson’s disease. Movement Disord 2003;18(Suppl 6):S80–7. [22] Langston JW, Widner H, Goetz CG, Brooks D, Fahn S, Freeman T, et al. Core assessment program for intracerebral transplantation (CAPIT). Movement Disord 1992;7:2–13.
ARTICLE IN PRESS K. Yamada et al. / Parkinsonism and Related Disorders 13 (2007) 101–107 [23] Saint-Cyr JA, Tre´panier LL, Kumar R, Lozano AM, Lang AE. Neuropsychological consequence of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain 2000;123: 2091–108. [24] Limousin-Dowsey P, Pollak P, Van Blercom N. Thalamic, subthalamic nucleus and internal pallidum stimulation in Parkinson’s disease. J Neurol 1999;246(Suppl 2): II42–5. [25] Simuni T, Jaggi JL, Mulholland H, Hurtig H, Colcher A, Siderowf AD, et al. Bilateral stimulation of the subthalamic nucleus in patients with Parkinson’s disease: a study of efficacy and safety. J Neurosurg 2002;96:666–72.
107
[26] Goto S, Yamada K, Ushio Y. Subthalamic nucleus stimulation in a parkinsonian patient with previous bilateral thalamotomy. J Neurol Neurosurg Psychiat 2004;75:163–71. [27] Yamada K, Goto S. Bilateral subthalamic nucleus stimulation results in reversal of alopecia in Parkinson’s disease. Parkinsonism Relat Disord 2004;10:353–5. [28] Benazzouz A, Breit S, Koudsie A, Pollak P, Krack P, Benabid AL. Intraoperative microrecordings of the subthalamic nucleus in Parkinson’s disease. Movement Disord 2002;17(Suppl 3):S145–9. [29] Romito LM, Scerrati M, Contarino MF, Bentivoglio AR, Tonali P, Albanese A. Long-term follow up of subthalamic nucleus stimulation in Parkinson’s disease. Neurology 2002;58:1546–50.