Background Although the short-term benefits of bilateral stimulationof the subthalamic nucleus in patients with advanced Parkinson'sdisease have been well documented, the long-term outcomes ofthe procedure are unknown.
Methods We conducted a five-year prospective study of the first49 consecutive patients whom we treated with bilateral stimulationof the subthalamic nucleus. Patients were assessed at one, three,and five years with levodopa (on medication) and without levodopa(off medication), with use of the Unified Parkinson's DiseaseRating Scale. Seven patients did not complete the study: threedied, and four were lost to follow-up.
Results As compared with base line, the patients' scores atfive years for motor function while off medication improvedby 54 percent (P<0.001) and those for activities of dailyliving improved by 49 percent (P<0.001). Speech was the onlymotor function for which off-medication scores did not improve.The scores for motor function on medication did not improveone year after surgery, except for the dyskinesia scores. On-medicationakinesia, speech, postural stability, and freezing of gait worsenedbetween year 1 and year 5 (P<0.001 for all comparisons).At five years, the dose of dopaminergic treatment and the durationand severity of levodopa-induced dyskinesia were reduced, ascompared with base line (P<0.001 for each comparison). Theaverage scores for cognitive performance remained unchanged,but dementia developed in three patients after three years.Mean depression scores remained unchanged. Severe adverse eventsincluded a large intracerebral hemorrhage in one patient. Onepatient committed suicide.
Conclusions Patients with advanced Parkinson's disease who weretreated with bilateral stimulation of the subthalamic nucleushad marked improvements over five years in motor function whileoff medication and in dyskinesia while on medication. Therewas no control group, but worsening of akinesia, speech, posturalstability, freezing of gait, and cognitive function betweenthe first and the fifth year is consistent with the naturalhistory of Parkinson's disease.
Levodopa is the standard treatment for Parkinson's disease butcauses long-term motor complications despite other pharmacologicinterventions.1 In 1998, we reported that the first series ofpatients with Parkinson's disease who were treated with bilateralstimulation of the subthalamic nucleus2 had improvement in motorfunction while off medication one year after surgery. We alsoreported an associated improvement in on-medication dyskinesiaand off-medication dystonia.3,4 These findings have been confirmedby other groups,5,6 but little information about the long-termoutcome of this therapy has been published. We report here theresults of a five-year prospective cohort study of the first49 patients with advanced Parkinson's disease whom we treatedin our center with bilateral stimulation of the subthalamicnucleus.
Methods
Patients
We studied the first 49 consecutive patients who received implantsat our institution from 1993 through 1997 for bilateral stimulationof the subthalamic nucleus. The selection criteria were clinicallydiagnosed Parkinson's disease, severe levodopa-related motorcomplications despite optimal adjustment of antiparkinsonianmedication, an age under 70 years, no surgical contraindications,and no dementia or major ongoing psychiatric illness. The ethicscommittee of Grenoble University, in France, approved the study,and all the patients gave written informed consent.
Surgery
We located the subthalamic nucleus by contrast ventriculography,magnetic resonance imaging (MRI), and electrophysiological recordingsand stimulation. The quadripolar electrodes (DBS 3387 and 3389,Medtronic) were implanted bilaterally in a single operationin all but the first three patients, in whom the second electrodewas implanted from 1 to 12 months after the first. All patientsunderwent MRI postoperatively for the assessment of surgicalcomplications. A few days after implantation of the electrodes,a programmable pulse generator (Itrel II, Medtronic) was implantedsubcutaneously on each side of the brain while the patientswere under general anesthesia. Stimulation settings and medicationwere progressively adjusted.
Assessments
Patients were evaluated preoperatively and postoperatively atone, three, and five years with use of the Unified Parkinson'sDisease Rating Scale.7 Unblinded assessments were performedwhen patients had taken no medication for 8 to 12 hours (offmedication)8 and during periods of maximal clinical benefitafter the administration of a dose of liquid levodopa that was50 percent higher than the usual morning dose of dopaminergictreatment (on medication).9 Postoperatively, patients were assessedduring stimulation.
Neuropsychological tests included the Mattis Dementia RatingScale10 for global cognitive assessment and an assessment offrontal-lobe dysfunction.11 Mood was assessed with the BeckDepression Inventory.12 In addition, patients were interviewedannually by the same neuropsychologist, a method that permitteddetailed assessment of behavioral abnormalities. Apathy wasdiagnosed according to the definition of Marin,13 and dementiaaccording to criteria in the Diagnostic and Statistical Manualof Mental Disorders, fourth edition (DSM-IV).14
Statistical Analysis
The primary outcome measures were the scores on part II (activitiesof daily living) and part III (motor examination) of the UnifiedParkinson's Disease Rating Scale at base line and at the clinicalend points of one year, three years, and five years. The secondaryoutcome measures were the subscores on part III (limb tremor,limb rigidity, limb akinesia, speech, postural stability, andgait) and part IV (the dyskinesia items) of the Unified Parkinson'sDisease Rating Scale, the scores on the Schwab and England scaleof global activities of daily living,15 the results of neuropsychologicaltests, and the dose of dopaminergic treatment and stimulationsettings at one year, three years, and five years.
Data are presented as means ±SD. Repeated-measures analysisof variance was used to predict motor scores on the basis oftwo independent variables: medication status (on or off medication),and time (length of follow-up). So as to avoid a type I errorwhen conducting multiple analyses over time, a P value of 0.005was considered to indicate statistical significance with useof the Bonferroni correction method. For post hoc comparisonsof base-line data with data at year 1 and at year 5, we usedthe Student's t-test or the Wilcoxon signed-rank test.
Results
Table 1 shows the characteristics of the patients at base line.Of the 49 patients who underwent bilateral stimulation of thesubthalamic nucleus, 7 could not be evaluated at five years:3 patients died and 4 were lost to follow-up (2 lived overseasand 2 were unable to return for the five-year follow-up forpersonal reasons).
Table 1. Base-Line Characteristics of the 49 Patients.
Off-Medication Evaluation
With stimulation in the off-medication state, the total scoreon part III of the Unified Parkinson's Disease Rating Scale,a standardized evaluation of all the motor signs of the disease,improved from the base-line value (55.7±11.9) by 66 percentat one year, 59 percent at three years, and 54 percent at fiveyears. (Scores on the scale range from 0 to 108, and a reductionin scores indicates an improvement in function.) As comparedwith base line, at five years the scores for tremor improvedby 75 percent, those for rigidity by 71 percent, and those forakinesia by 49 percent (Table 2). Postural stability and gaitalso improved. The score for speech improved only during thefirst year and then progressively worsened, returning to thebase-line score at five years.
Table 2. Effect of Bilateral Stimulation of the Subthalamic Nucleus on Off-Medication UPDRS Subscores.
In comparison with the base-line score (30.4±6.6), thetotal score with stimulation on part II of the Unified Parkinson'sDisease Rating Scale (which assesses activities of daily living;range of scores, 0 to 52) improved by 66 percent at one year,51 percent at three years, and 49 percent at five years; theworsening between one year and five years was significant (P<0.001)(Table 2). All changes from base line to one year indicatedan improvement in parkinsonism, and all changes from one tofive years a worsening. The scores on the Schwab and Englandscale, which measures activities of daily living, range from0 to 100 percent (with 100 percent indicating normal function).The scores dramatically improved postoperatively in the off-medicationcondition (Figure 1). Five years after surgery, most patientswere independent in their activities of daily living in theoff-medication condition (mean score on the Schwab and Englandscale, 73 percent), whereas before surgery most had been fullydependent on a caregiver (mean score on the Schwab and Englandscale, 33 percent). Before surgery, 35 of the 49 patients (71percent) had painful dystonia while off medication; 8 of 43patients (19 percent) had dystonia at one year, and 14 of 42patients (33 percent) had dystonia at five years.
Figure 1. Off-Medication and On-Medication Scores on the Schwab and England Scale for Activities of Daily Living (ADL) at Base Line and One, Three, and Five Years after Surgery.
Data are means ±SD. After surgery, evaluation was performed with bilateral stimulation activated. Scores range from 0 to 100 percent (with a score of 100 percent indicating normal function). A score above 70 percent indicates complete independence in activities of daily living. A score of 70 percent or lower indicates that patients need the help of a caregiver. Off-medication scores were improved at one, three, and five years (P<0.001 for all three comparisons).
On-Medication Evaluation
A levodopa test could not be performed in two patients at threeyears and in three patients at five years who had stopped dopaminergictreatment. These patients could not tolerate a levodopa challenge.For the remaining patients, motor function and activities ofdaily living in the on-medication state did not improve afterstimulation of the subthalamic nucleus. Between the first andthe fifth year, there were no significant changes in individualscores for tremor and rigidity, but scores for akinesia, speech,postural stability, and freezing of gait worsened (P<0.001for each comparison), resulting in a worsening of the totalscore for motor function (P<0.001) and the total score foractivities of daily living (P<0.001), as assessed on theUnified Parkinson's Disease Rating Scale. Activities of dailyliving as assessed by the Schwab and England scale were unchanged.Compared with base line, the severity of the disability relatedto dyskinesia decreased by 58 percent, and the duration of dyskinesiaby 71 percent (Table 3).
Table 3. Effect of Bilateral Stimulation of the Subthalamic Nucleus on On-Medication UPDRS Subscores.
Neuropsychological Evaluation
There were no significant changes on the Beck Depression Inventory(maximal score, 63; a higher score indicates more severe depression).The average score on the Mattis Dementia Rating Scale (maximalscore, 144; a higher score indicates better function) was worseat five years, reflecting progressive dementia in three patientsaccording to DSM-IV criteria (Table 4), but the changes werenot significant (131±18 vs. 136±10 at base line,P=0.07). The average score for frontal-lobe function (maximalscore, 50; a higher score indicates better function) tendedto be worse at five years (37.3±11.2 vs. 40.4±9.2at base line, P=0.03).
Postoperatively, the requirement for levodopa (or equivalentmedication) decreased significantly, from a levodopa-equivalentdaily dose of 1409±605 mg at base line to 584±366mg at one year, 526±328 mg at three years, and 518±333mg at five years (P<0.001, by analysis of variance). At fiveyears, 11 of 42 patients were no longer taking levodopa and3 were not taking any dopaminergic drugs. After the first year,there were no significant changes in voltage (one year, 2.8±0.6V; five years, 3.1±0.4 V; P=0.007, by analysis of variance),frequency (one year, 143±19 Hz; five years, 145±19Hz), or pulse width (one year, 61±6 µsec; fiveyears, 64±12 µsec). Monopolar stimulation withthe use of a single contact from the quadripolar electrode wasapplied in 90 percent of patients at one year and five years.With these settings, the stimulators had to be replaced in thefirst five years in only one patient.
Adverse Events
There were three deaths. One patient in whom an intracerebralhemorrhage developed during surgery remained bedridden2 anddied three years after surgery. Another patient died of myocardialinfarction 11 months after surgery. One patient was severelydepressed and had suicidal ideation three months before surgeryand committed suicide six months after surgery.
Surgical complications were frequent but mostly temporary (Table 5).Permanent side effects included dementia in two patients.Transient postoperative delirium, ranging from temporospatialdisorientation to psychosis, occurred in 12 patients (24 percent)during the first few days after surgery. Device-related complicationswere rare. One patient had an infection that required temporaryremoval of the subcutaneous extension lead and pulse generator.
Table 5. Adverse Events Associated with Subthalamic Stimulation.
Treatment-related side effects changed with time during thefollow-up. At three months, 4 patients, and at five years, 2patients indicated that they still had disabling dyskinesia(related to dopaminergic treatment, subthalamic stimulation,or both) as compared with 29 patients at base line. Fifteenof 49 patients (31 percent) had eyelid-opening apraxia in thefirst three months, and this remained a problem in 8 of 42 patients(19 percent) for the duration of follow-up. In the first threemonths, reversible stimulation-induced dyskinesias commonlydeveloped in patients after an increase in voltage. In the longterm, base-line dyskinesias improved.3,4
During the first three months after surgery, 41 patients gainedweight (mean, 3 kg; maximum, 5 kg). Patients on average gainedanother kilogram within the first year; thereafter, weight wasstable. In the immediate postoperative period, transient hypomaniadeveloped in 8 percent of the patients. With longer follow-up,other psychiatric disorders occurred, including transient depressiveepisodes (17 percent) and transient apathy (5 percent), whichwere responsive to antidepressants, an increase in dopaminergicmedication, or both. Permanent apathy occurred in the immediatepostoperative period in one patient, who was dependent on levodopaand in whom the dose of levodopa was drastically decreased aftersurgery. Apathy that did not respond to dopaminergic treatmentoccurred in five patients (12 percent), as did dementia in threepatients (7 percent) between the third year and the fifth yearof follow-up.
Discussion
In patients with advanced Parkinson's disease who were followedprospectively, long-term bilateral stimulation of the subthalamicnucleus led to significant postoperative improvements in allparkinsonian motor signs that were assessed while the patientswere off dopaminergic medication except speech. The improvementsover base line were sustained five years after surgery. Tremorand rigidity improved substantially at one year and remainedstable at five years. Akinesia also improved at one year, butthis improvement was not completely sustained over time. Painfuloff-period dystonia disappeared at five years in most patients.Five years after surgery, most patients were independent intheir activities of daily living when assessed off medication.Before surgery, all patients had depended on a caregiver.
When the patients were assessed while receiving dopaminergicmedication, the duration of dyskinesia and the severity of theassociated disability substantially decreased at one year andremained stable at five years. However, on-medication motorsigns of parkinsonism were not improved after surgery; akinesia,speech, postural stability, and freezing of gait all worsenedbetween years 1 and 5. This decline was reflected in a milddeterioration in the scores for activities of daily living inthe on-medication state, despite the ongoing reduction in theduration and severity of dyskinesia.
The deterioration when the patients were on medication in axialsymptoms, including speech, postural stability, and freezingof gait, is characteristic of the natural history of Parkinson'sdisease16 and has been attributed to the increasing severityof cerebral nondopaminergic lesions.17 The effect of levodopaon akinesia, rigidity, and tremor tends to remain stable overtime,17,18 whereas gait, postural stability, and dysarthriaworsen and become less responsive to levodopa. Since we didnot have a simultaneously treated control group, we speculatethat the deterioration that we observed in our patients is whatone would have expected in the absence of specific treatment.
We reduced the dose of dopaminergic medication during the firstyear and kept it stable thereafter. Stimulation settings werestable after the first year and throughout the study period,indicating that clinically important tolerance to stimulationdoes not develop in patients who undergo such treatment.
The frequency of symptomatic hematomas in this cohort is similarto that reported in patients who undergo microelectrode-guidedstereotactic neurosurgery.19 Although high rates of complicationssuch as electrode fracture, electrode dislocation, and stimulatormalfunction have previously been reported with deep-brain stimulation,20,21no clinically significant problems related to the hardware occurredin our cohort, except for inadvertent and reversible deactivationof the stimulator.
Five patients had cognitive decline: two immediately after thesurgery, and three in whom progressive dementia developed betweenthe third and fifth postoperative years. In the remaining patients,the dementia score remained stable. Because stimulation hasno clinically relevant effects on cognition,11,22 the casesof progressive cognitive deterioration probably reflect thenatural history of long-standing Parkinson's disease.
Psychiatric problems, including depression or mania, have beenreported by several groups in patients treated with stimulationof the subthalamic nucleus.23,24,25,26 These complications maybe related to preexisting psychiatric illness, surgery-relatedstress, changes in medication, alterations in social life thatare associated with improvements in motor function, and themismatch between the final outcome of treatment and the patient'sexpectations.23 Changes in the limbic circuit may also contributeto psychiatric problems.27 Hypomania occurred in five cases,all in the immediate postoperative period, and may be explainedby the synergistic psychotropic effects of stimulation of thesubthalamic nucleus and levodopa.27 In contrast, depressionusually occurred several months postoperatively, coincidingwith the reduction in dopaminergic medication, and was generallyreversible by increasing the dose of the dopaminergic treatment.Although one patient was known to have had severe depressionwith suicidal ideation before surgery, it is possible that thereduction in the dose of dopaminergic medication contributedto his suicide six months after surgery.
Patients who experienced apathy in the initial postoperativemonths responded to dopaminergic treatment, with the exceptionof one patient who was addicted to levodopa and who was notallowed to increase his medication to preoperative levels. Althoughstimulation of the subthalamic nucleus had no overall effecton mood, modifications in the characteristics of the stimulationor in dopaminergic treatment can affect mood substantially inindividual patients, and this possibility needs to be consideredin postoperative management.28
Permanent apathy became apparent in five patients after thethird postoperative year, a development that paralleled a decreasein frontal cognitive function in four of the patients and thusmay relate to the natural progression of the disease. Afterthe immediate postoperative period, only three patients hadhallucinations (those with a parallel cognitive decline), andonly one had transient psychosis, a frequent complication incomparable populations of patients with parkinsonism that aretreated medically.29,30
The Schwab and England scale has been used in other studiesto assess the effects of surgical treatment in patients withParkinson's disease in both on-medication and off-medicationstates.8,15 Although there has been no direct comparison betweenlong-term outcomes of bilateral stimulation of the subthalamicnucleus and those of other surgical therapies in patients withadvanced Parkinson's disease, improvements of the magnitudethat we observed on the Schwab and England scale have not, toour knowledge, been previously reported. Thalamotomy and deep-brainstimulation of the thalamus have resulted in long-term improvementin tremor, but not in akinesia31,32 or in activities of dailyliving.33,34 Unilateral pallidotomy results in sustained improvementin contralateral dyskinesia, but ipsilateral symptoms do notimprove, and initial improvement in gait and akinesia diminishesprogressively with time. Most patients remain dependent on acaregiver when they are in the off-medication state.35,36,37
Data on long-term outcomes of bilateral pallidotomy or pallidalstimulation are sparse, and follow-up is restricted to smallseries of patients and does not exceed three years.38,39,40The reported rates of persistent fatigue, speech disorder, drooling,and dysphagia41 are higher than those with bilateral stimulationof the subthalamic nucleus. Psychiatric problems, includingpostoperative depression and changes in personality, behavior,and executive functions, have also been reported.42
Stimulation of the subthalamic nucleus makes possible a reductionin the dose of dopaminergic treatment, whereas thalamic surgeryand pallidal surgery do not. Although stimulation of the subthalamicnucleus requires very close follow-up of the patient by a clinicianexperienced with this approach,28 once a good balance is achievedbetween the amount of stimulation and dopaminergic treatment,therapeutic adjustments are infrequent, as shown by the stabletreatment settings and the low number of complications beyondthe first postoperative year.
Our study has limitations. Patients and evaluators were notblinded, and there was no placebo group. Placebo effects inParkinson's disease, however, are rarely sustained in repeatedtesting.43,44 Furthermore, no placebo effect was observed intwo double-blind, controlled studies of neurosurgical interventionsfor Parkinson's disease.6,45 Because in our study the evaluationperiod was nine years, assessments were done by different investigators.However, the reliability is good among the various neurologistsusing the Unified Parkinson's Disease Rating Scale,46 especiallyconsidering the magnitude of the changes observed in motor scoresover time.
Our findings show that the efficacy of stimulation of the subthalamicnucleus in reducing off-medication motor symptoms and levodopa-induceddyskinesia in relatively young patients with severe Parkinson'sdisease is largely maintained five years after surgery. However,over time there is deterioration in akinesia, axial symptoms,and cognitive problems that is consistent with the progressionof the underlying disease. Stimulation of the subthalamic nucleusseems most useful for relatively young patients who have motorcomplications from levodopa treatment and who are independentin activities of daily living in their best on-medication state.Those patients who already have disabling motor signs that areresistant to levodopa, or who have cognitive deterioration,are not good candidates for this treatment.
Supported by grants from INSERM, France; the French Ministryof Health; the Rhône-Alpes government; Agence Universitairede la Francophonie, France (to Dr. Batir); Medtronic (to Dr.Benabid); and the University of Kiel, Germany (to Dr. Krack).
We are indebted to the following neurologists who participatedin the evaluation of the patients: Elena Caputo (Milan, Italy),David Charles (Nashville), Rianne Esselink (Amsterdam), EmilianaFincati (Verona, Italy), Pedro Garcia-Ruiz (Madrid), EmmelineLagrange (Grenoble, France), Michela Manfredi (Brescia, Italy),Alexandre Mendes (Porto, Portugal), Elena Moro (Rome), IsabellePayen (Grenoble, France), Mario Rizzone (Turin, Italy), FilippoTamma (Milan, Italy), Stéphane Thobois (Lyons, France),Laurent Vercueil (Grenoble, France), and Jing Xie (Grenoble,France). We are also indebted to Brigitte Piallat (Grenoble,France) for assistance in intraoperative neurophysiology, LauraCastana (Milan, Italy) and Dominique Hoffmann (Grenoble, France)for surgical assistance, Sylvie Grand (Grenoble, France) formagnetic resonance imaging, Hélène Klinger (Grenoble,France) and Aurélie Funkiewiez (Grenoble, France) forneuropsychological evaluation, Jean-Luc Bosson (Grenoble, France)for help with biostatistics, and Glenna Case (Minneapolis) foreditorial assistance.
Source Information
From the Departments of Clinical and Biological Neurosciences (P.K., A. Batir, N.V.B., S.C., V.F., C.A., A.K., P.D.L., A. Benazzouz, A.-L.B., P.P.) and Magnetic Resonance Imaging (J.F.L.), Joseph Fourier University, Grenoble, France.
Address reprint requests to Dr. Krack at the Department of Clinical and Biological Neurosciences, Département de Neurologie, Centre Hospitalier Universitaire de Grenoble, BP 217, 38043 Grenoble CEDEX 9, France, or at paul.krack{at}ujf-grenoble.fr.
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[Abstract]
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