Effects of stereotactic neurosurgery on postural instability and gait in Parkinson's disease

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Effects of Stereotactic Neurosurgeryon Postural Instability and Gait in

Parkinson’s Disease

Maaike Bakker, MSc,1 Rianne A.J. Esselink, MD,1,2

Marten Munneke, MSc,1

Patricia Limousin-Dowsey, MD, PhD,3

Hans D. Speelman, MD, PhD,2 andBastiaan R. Bloem, MD, PhD1*

1Department of Neurology, University Medical Centre StRadboud, Nijmegen, The Netherlands; 2Department ofNeurology, Academic Medical Centre, Amsterdam, The

Netherlands; 3Sobell Department for Motor Neurosciencesand Movement Disorders, Queen Square, London,

United Kingdom

Abstract: Postural instability and gait disability (PIGD) aredisabling signs of Parkinson’s disease. Stereotactic surgeryaimed at the internal globus pallidus (GPi) or subthalamicnucleus (STN) might improve PIGD, but the precise effectsremain unclear. We performed a systematic review of studiesthat examined the effects of GPi or STN surgery on PIGD.Most studies examined the effects of bilateral GPi stimulation,bilateral STN stimulation, and unilateral pallidotomy; we,therefore, only performed a meta-analysis on these studies.Bilateral GPi stimulation, bilateral STN stimulation, and to alesser extent, unilateral pallidotomy significantly improvedPIGD, and more so during the ON phase than during the OFFphase. © 2004 Movement Disorder Society

Key words: Parkinson’s disease; surgery; posture; gait; glo-bus pallidus; subthalamic nucleus

Postural instability and gait disability (PIGD) in Par-kinson’s disease result in loss of independence and fre-

quent falls, often with debilitating injuries.1,2 Stereotacticsurgery might improve PIGD, but depending on thetargeted nucleus and the technique used, the effects onPIGD seem to differ.

Stereotactic surgery for Parkinson’s disease has beenaimed at different nuclei, including the thalamus, internalglobus pallidus (GPi), and subthalamic nucleus (STN),and has been performed with different techniques andapproaches, including unilateral lesioning, bilateral le-sioning, unilateral stimulation, and bilateral stimulation.There is overall agreement that thalamic stereotacticsurgery is not effective in improving PIGD.3 Stereotacticsurgery aimed at GPi or STN might be more effective.4–7

We performed a systematic review of studies that exam-ined the effects of GPi or STN surgery on PIGD.

MATERIALS AND METHODS

Literature Search

We searched the MEDLINE and EMBASE electronicdatabases for articles published before April 2003, usingtwo search strategies. One strategy searched for articleswith one or more of the following key words: “pal-lidotomy,” “pallidal stimulation,” “subthalamic nucleusstimulation” or “subthalamotomy.” The other strategyused the keywords “subthalamic nucleus” or “globuspallidus,” “Parkinson’s disease”, and “surgery or neuro-surgery or deep brain surgery.” We also examined thereference lists of relevant publications.

Selection Criteria

Studies had to meet the following selection criteria:(1) English language; (2) stereotactic surgery of GPi orSTN for Parkinson’s disease; (3) effects on PIGD mea-sured with the Unified Parkinson’s Disease Rating Scale(UPDRS)8 (items 13, 14, 15, 27, 28, 29, or 30), withtimed tests (timed walking or stand–walk–sit test)9, withposturography or with quantified gait analysis; (4) fol-low-up at 3, 6, and/or 12 months postoperatively; and (5)original data (no reviews, editorials). For studies withoverlapping data sets, we chose the study with the largestpopulation.

Exclusion criteria were the following: (1) case reports;(2) effects pooled across different types of surgery; (3)inclusion of patients who previously had undergone adifferent type of surgery for Parkinson’s disease; (4)results presented in figures from which no quantitativeimprovements could be estimated; and (5) results pre-sented as the percentage or number of patients that im-proved or worsened (this strategy precluded quantitativecomparisons with studies presenting mean improve-ments).

*Correspondence to: Dr. Bastiaan R. Bloem, Department of Neurology,326, University Medical Centre St Radboud, PO Box 9101, 6500 HBNijmegen, The Netherlands. E-mail: [email protected]

Received 15 July 2003; Revised 18 December 2003; Accepted 2February 2004

Published online 8 April 2004 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/mds.20116

1092 M. BAKKER ET AL.

Movement Disorders, Vol. 19, No. 9, 2004

Systematic Review

We calculated the effect of stereotactic surgery onPIGD for measurements performed in the medication onand off state. For studies of deep brain stimulation, weonly used the postoperative assessments made with thestimulators switched on.

Because our analysis showed that the effect of stereo-tactic surgery did not change considerably within the firstyear after surgery, we report only one postoperativeassessment for each individual study. Because most stud-ies assessed PIGD at 6 months, we report this assessmentif available. If a study examined the effects at both 3 and12 months, we report the 12-month assessment. If astudy examined the effects only at 3 months, we reportthis assessment.

Because the majority of studies used the UPDRS toassess PIGD, we only performed a quantitative meta-analysis for these studies. We systematically review theresults of studies that used timed tests, dynamic postu-rography, or quantified gait analysis to assess PIGD.

UPDRS: Meta-Analysis.

For each study that used the UPDRS to assess PIGD,we expressed the effect of stereotactic surgery as thedifference scores between pre- and postoperative values.We also calculated the confidence intervals (CIs) forthese difference scores. Subsequently, we calculated theoverall effect using the fixed effects model. Not allstudies examined the same items of the UPDRS. Somestudies reported a summed composite score of severalitems, whereas others reported the scores of each indi-vidual item. For those studies that reported a summedcomposite score, we normalised each difference scoreand standard error to a minimal value of �4 (indicatingmaximal improvement) and a maximal value of 4 (indi-cating maximal worsening). If a study examined morethan one item, we first calculated the difference score andstandard error (SE) for each individual item and thancalculated the mean difference and pooled SE.

The majority of studies did not report the SE of thechange score. We, therefore, calculated the SE on thebasis of several other values. If reported, we used thestandard deviation (SD) of the difference score to calcu-late the SE. If only the P value and mean pre- andpostoperative scores were provided, we used the P valueto calculate the SE. If neither of these values was re-ported, we used the SD of the pre- and postoperativevalues to calculate the SE of the difference score. If thestudy did not report sufficient data to calculate the SE,we only presented the mean change score. This wasdone, for example, for all studies presenting medianscores instead of mean scores.

For all studies included in the meta-analysis, we re-corded the following clinical characteristics: (1) meanbaseline off-state PIGD score; (2) mean baseline on-statePIGD score; (3) mean age at disease onset; (4) meandisease duration; (5) mean age at surgery; (6) meanbaseline of PIGD levodopa response; and (7) mean post-operative percentage change in medication. All meanswere weighted for sample size.

Timed Tests: Review.

We only analysed the most frequently used timedtests: the stand–walk–sit test and the timed walking test.The stand–walk–sit test measures the time required for apatient to stand up from a chair, walk a certain distance,make a turn, walk back, and sit down. The timed walkingtest measures the time required to walk a certain distancefrom a standing start, turn around, and return to thestarting point. If a study examined both tests, we onlyanalysed the stand–walk–sit test as this was most com-monly used.

Dynamic Posturography and Quantified GaitAnalysis: Review.

Several studies used more elaborate techniques toquantify PIGD, using treadmills or posturography. Wewill only briefly mention the effects of surgery on PIGDreported by these studies.

Adverse Effects on PIGD

For each study, we scored the number of reportedpatients with adverse effects on PIGD, the nature of theseadverse effects, and whether these were transient orpersistent.

RESULTS

Due to the selection criteria, we had to exclude severalpotentially interesting studies examining the effects ofDBS on PIGD. We will give some examples of studiesthat were excluded. Common reasons for exclusion werepooling of the effects of different types of surgery,10–12

inclusion of patients who had already previously under-gone surgery for PD,12–16 follow-up before 3 months orafter 12 months postoperatively,17,18 PIGD items of theUPDRS pooled with other items of the UPDRS that donot examine balance and gait,18–22 or studies with over-lapping data sets.23,24

Unilateral Pallidotomy, Bilateral GPi Stimulation,and Bilateral STN Stimulation

UPDRS.

The number of included studies differed considerablyacross the eight different types of stereotactic surgery. As

SURGERY IN PD: A META-ANALYSIS 1093


most studies examined the effects of unilateral pal-lidotomy, bilateral GPi stimulation, or bilateral STNstimulation, we only performed a meta-analysis for theseinterventions. We will review qualitatively the results ofstudies examining the remaining types of surgery.

A total of 36 studies were included in the meta-analysis. Of these studies, 17 examined the effects ofunilateral pallidotomy,5,6,25–39 9 the effects of bilateralGPi stimulation,4,40–47 and 10 the effects of bilateralSTN stimulation.4,7,23,41,43,47–51 There were no major dif-ferences in the baseline clinical characteristics of patientsrecruited for different types of surgery (Table 1). How-ever, there was a difference between surgeries in thereduction of medication postoperatively. Medication wasreduced after bilateral STN stimulation, whereas it re-mained approximately unchanged after bilateral GPistimulation and unilateral pallidotomy.

In the off state, bilateral STN stimulation (pooledeffect, �1.4; CI, �1.2 to �1.7), bilateral Gpi stimulation(�1.0; �0.8 to �1.3), and unilateral pallidotomy (�0.4;�0.3 to �0.5 ) were all significantly effective in improv-ing PIGD (Fig. 1). Bilateral STN stimulation and bilat-eral Gpi stimulation were significantly more effectivethan unilateral pallidotomy, with a trend for bilateralSTN stimulation to be more effective than bilateral GPistimulation. Several studies that directly compared theeffects of bilateral GPi stimulation and bilateral STNstimulation also showed this trend.32,46–48

Unilateral pallidotomy, bilateral GPi stimulation, andbilateral STN stimulation were also effective in improv-ing PIGD in the on state (Fig. 2), but the effects were lesspronounced compared to the off state. The pooled effectwas �0.2 (CI, �0.1 to �0.4) for bilateral STN stimula-tion, �0.5 (CI, �0.3 to �0.7) for bilateral Gpi stimula-tion, and �0.2 (CI, �0.1 to �0.3) for unilateral pal-lidotomy.

Comparison of the baseline PIGD levodopa response(Table 1) with the effects of surgery in the off state showsthat the effect of bilateral Gpi and bilateral STN stimu-

lation approximately equalled that of medication preop-eratively, whereas there was a trend that the effect ofunilateral pallidotomy was smaller than that of medica-tion.

Timed Tests.

All studies examining the effects of unilateral pal-lidotomy,5,19,26,52–55 bilateral GPi stimulation,56 and bi-lateral STN stimulation7,50,51 on PIGD with timed tests,showed an off state PIGD improvement. In the on state,all except two studies51,57 showed that unilateral pal-lidotomy,5,19,26,52,54 bilateral GPi stimulation,56,57 and bi-lateral STN stimulation50,51 improve timed tests ofPIGD. However, the improvements in the on state weresmaller compared to those observed in the off state.

Quantified Gait Analysis and Posturography.

Several studies using quantified gait analysis demon-strated that unilateral pallidotomy,32 bilateral GPi stim-ulation,23,40,44,46 and bilateral STN stimulation23,58–63canimprove gait. Several studies using posturography dem-onstrated that unilateral pallidotomy,18,32,34,64 bilateralGPi stimulation,40 and bilateral STN stimulation65 canalso improve balance reactions.

Bilateral Pallidotomy, Unilateral GPi or STNStimulation, and Subthalamotomy

Six studies described the effects of bilateral pal-lidotomy on PIGD. Five of these studies used the UP-DRS to assess PIGD32,39,66–68 and one used quantifiedgait analysis.69 Two of the studies using the UPDRSreported worsening of PIGD,66,68 whereas three othersreported improvement.32,39,67 The study that used quan-tified gait analysis reported PIGD improvement.69

Four studies examined the effects of unilateral GPistimulation on PIGD, two using the UPDRS 36,45 and twousing timed tests.56,57 All studies reported PIGD im-provement.

TABLE 1. Baseline clinical characteristics of patients included in the studies examined in this meta-analysis

Clinical characteristics Unil. pallidotomy Bil. GPi stimulation Bil. STN stimulation

Baseline off-state PIGD (UPDRS) 2.2 (1.5 to 2.7) 2.5 (1.9 to 3.4) 2.6 (2.0 to 2.9)Baseline on-state PIGD (UPDRS) 1.1 (0.4 to 1.8) 1.4 (0.8 to 2.3) 1.2 (0.5 to 1.5)Age at onset (yr) 43 (40 to 55) 42 (35 to 46) 44 (35 to 53)Disease duration (yr) 14 (1 to 16) 14 (11 to 20) 14 (11 to 16)Age at surgery (yr) 61 (56 to 66) 56 (46 to 65) 59 (51 to 67)Baseline PIGD levodopa response (UPDRS) �1.1 (�1.6 to �0.9) �1.2 (�2.7 to �0.6) �1.6 (�2.8 to �1.2)Medication reduction postoperatively 0% (�20 to 11%) �1% (�16 to 28%) �46% (�72 to �37%)

Values are means (range). United Parkinson’s Disease Rating Scale (UPDRS) values were normalized to a maximal valueof 4. Medication reduction was calculated from levodopa equivalent units.

PIGD, postural instability and gait disability; GPi, internal globus pallidus; STN, subthalamic nucleus; unil, unilateral; bil,bilateral.



No study examined the effects of bilateral subthalamot-omy on PIGD, whereas one study reported that unilateralsubthalamotomy improved PIGD.70 Finally, one study re-ported that unilateral STN stimulation improved PIGD.71

Adverse Effects on PIGD

Adverse effects were relatively most common andpersistent after bilateral pallidotomy (Table 2). No ad-verse effects on PIGD were reported after unilateral GPistimulation or unilateral STN stimulation.

DISCUSSION

We only performed a meta-analysis for unilateralpallidotomy, bilateral Gpi stimulation, and bilateralSTN stimulation because the number of studies exam-ining the remaining types of surgery was small. Notethat the studies included in this meta-analysis re-cruited relatively young patients with L-dopa–responsive PIGD preoperatively (Table 1). Hence, anyconclusions drawn from our study will only be appli-cable to this type of patients. The meta-analysis dem-

FIG. 1. Effect and 95% confidence interval with regard to Unified Parkinson’s Disease Rating Scale scores of postural instability and gait disability(PIGD) for three different types of stereotactic surgery in the off state. The effect is expressed as the difference score compared to the preoperativestate. A negative effect indicates an improvement in PIGD. Bil., bilateral; GPi, internal globus pallidus; STN, subthalamic nucleus; Unil., unilateral.The studies that are underlined directly compared the effects of two different types of surgery. The values between parentheses represent the monthsafter surgery at which the assessment was performed. No overlap of the confidence interval with zero indicates a significant effect of surgery. Filledtriangles, unilateral pallidotomy; open triangles, bilateral GPi stimulation; filled squares, bilateral STN stimulation; filled circle, overall effect.



onstrates that unilateral pallidotomy, bilateral Gpistimulation, and bilateral STN stimulation are all ef-fective in improving PIGD in the off state. BilateralSTN stimulation and bilateral GPi stimulation weremore effective in improving PIGD than unilateralpallidotomy. For bilateral GPi stimulation and bilat-eral STN stimulation, the effects approximatelyequalled the effects of medication preoperatively,whereas for unilateral pallidotomy, there was a trendfor these effects to be smaller than the effects of

medication preoperatively. Unilateral pallidotomy, bi-lateral GPi stimulation, and bilateral STN stimulationalso improved PIGD in the on state, but these im-provements were markedly smaller than those ob-served in the off state. Medication was only reducedafter bilateral STN stimulation and remained approx-imately unchanged after bilateral GPi stimulation orunilateral pallidotomy. Adverse effects on PIGD weremost common and persistent after bilateral pal-lidotomy.

FIG. 2. Effect and 95% confidence interval with regard to Unified Parkinson’s Disease Rating Scale scores of postural instability and gait disability(PIGD) for three different types of stereotactic surgery in the on state. The effect is expressed as the difference score compared to the preoperativestate. A negative effect indicates an improvement in PIGD. Bil., bilateral; GPi, internal globus pallidus; STN, subthalamic nucleus; Unilat., unilateral.The studies that are underlined directly compared the effects of two different types of surgery. The values between parentheses represent the monthsafter surgery at which the assessment was performed. No overlap of the confidence interval with zero indicates a significant effect of surgery. Filledtriangles, unilateral pallidotomy; open triangles, bilateral GPi stimulation; filled squares, bilateral STN stimulation; filled circle, overall effect.



This study has several shortcomings. First, the major-ity of studies lacked a control group. Therefore, wecannot exclude that the observed improvements withsurgery were at least in part placebo effects.

Second, patients were not randomly assigned to thedifferent types of surgery, and there may have beendifferences in design across studies that make our com-parisons less reliable. For example, there may have beendifferences in the dose of medication used to obtain anon state.23 Also, selection criteria used to recruit patientsfor surgery may have differed between studies examin-ing different surgeries. However, it was reassuring thatthere were no major differences in the clinical charac-teristics of patients that were recruited for the differenttypes of surgery and that the few face-to-face compari-sons across different interventions4,41,43,47 reached con-clusions largely similar to those of our meta-analysis.

Third, we only examined effects on PIGD within thefirst year after surgery. During this period, the effects ofsurgery appeared to be stable. It still remains to beestablished whether the positive effects of surgery arestable for more than 1 year after surgery.

Fourth, the clinical outcome measures used for scoringPIGD—derived from the UPDRS part III—are limited by

their subjective nature and by disagreement about the exactscoring system.72,73 However, analysis of the more objec-tive timed tests led to similar conclusions as the clinicaloutcome measures. Furthermore, studies that used quanti-fied gait analysis or dynamic posturography also confirmedour findings that unilateral pallidotomy, bilateral GPi stim-ulation, and bilateral STN can improve PIGD.

Finally, we probably underestimated the incidenceof adverse effects on PIGD, for two reasons. First, thenumber of adverse effects reported in a study dependsgreatly on how the authors monitored adverse effects.Many authors probably did not systematically examineadverse effects on PIGD. Second, we only examined asubgroup of the total number of studies examining theeffects of STN or GPi surgery. Therefore, we mayhave missed additional adverse effects reported in theremaining published studies. However, our reviewdoes show that, apart from the beneficial effects forthe entire group, PIGD may worsen in individualpatients. Such adverse effects on PIGD, as well asother adverse effects of stereotactic surgery (e.g.,dysarthria, psychiatric complications) must be takeninto account when considering patients for stereotacticsurgery.

TABLE 2. Adverse effects on PIGD

Stereotacticsurgery Reference Worsening of Patients (n) Duration

Unilateralpallidotomy

3 Balance 2 Persistent26 Balance 2 Transient19 Balance 1 Not reported28 Balance 1 Persistent32 Balance & falling 2 Not reported

Bilateralpallidotomy

66 Initiation of gait 2 Not reported68 Freezing gait 3 Persistent39 Freezing gait 6 Not reported

Bilateral GPistimulation

46 Freezing 1 Transient43 Freezing 3 Transient42 Gait akinesia 3 Persistent41 Balance — Transient47 Falling 1 Transient

Unilateralsubthalamotomy

70 Gait stability 1 Persistent

Bilateral STNstimulation

7 Postural instability 1 Persistent41 Balance — Transient47 Falling 2 Transient

Dashes indicate that the number of patients involved was not reported; it was only reported thattransient balance impairment was common after the surgery. For unilateral GPi stimulation,bilateral subthalamotomy, and unilateral STN stimulation, no adverse effects on PIGD werereported.

GPi, internal globus pallidus; STN, subthalamic nucleus; PIGD, postural instability and gaitdisability.



Acknowledgments: B.R.B. and M.B. were supported byresearch grants of the Prinses Beatrix Fonds and the Interna-tional Parkinson Foundation.

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Effects of stereotactic neurosurgery on postural instability and gait in Parkinson's disease

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