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March 31, 2015; 84 (13) Article

Neuropsychological outcome after deep brain stimulation for Parkinson disease

Vincent J.J. Odekerken, Judith A. Boel, Gert J. Geurtsen, Ben A. Schmand, I.P. Dekker, Rob J. de Haan, P. Richard Schuurman, Rob M.A. de Bie, The NSTAPS Study Group
First published February 27, 2015, DOI: https://doi.org/10.1212/WNL.0000000000001419
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Abstract

Objective: To assess the neuropsychological outcome 12 months after bilateral deep brain stimulation (DBS) of the globus pallidus pars interna (GPi) or subthalamic nucleus (STN) for advanced Parkinson disease.

Methods: We randomly assigned patients to receive either GPi DBS or STN DBS. Standardized neuropsychological tests were performed at baseline and after 12 months. Patients and study assessors were masked to treatment allocation.

Results: Univariate analysis of change scores indicated group differences on Stroop word reading and Stroop color naming (confidence interval [CI] 1.9–10.0 and 2.1–8.8), on Trail Making Test B (CI 0.5–10.3), and on Wechsler Adult Intelligence Scale similarities (CI −0.01 to 1.5), with STN DBS showing greater negative change than GPi DBS. No differences were found between GPi DBS and STN DBS on the other neuropsychological tests. Older age and better semantic fluency at baseline predicted cognitive decline after DBS.

Conclusions: We found no clinically significant differences in neuropsychological outcome between GPi DBS and STN DBS. No satisfactory explanation is available for the predictive value of baseline semantic fluency for cognitive decline.

Classification of evidence: This study provides Class I evidence that there is no large difference in neuropsychological outcome between GPi DBS and STN DBS after 12 months. The study lacks the precision to exclude a moderate difference in outcomes.

GLOSSARY

CI=
confidence interval;
DBS=
deep brain stimulation;
GPi=
globus pallidus pars interna;
LED=
levodopa equivalent dose;
MDRS=
Mattis Dementia Rating Scale;
NSTAPS=
Netherlands Subthalamic and Pallidal Stimulation;
OR=
odds ratio;
PD=
Parkinson disease;
PDQL=
Parkinson's Disease Quality of Life Questionnaire;
QOL=
quality of life;
RAVLT=
Rey Auditory Verbal Learning Test;
RBMT=
Rivermead Behavioral Memory Test;
RCI=
reliable change index;
STN=
subthalamic nucleus;
TMTA=
Trail Making Test part A;
TMTB=
Trail Making Test part B;
UPDRS=
Unified Parkinson's Disease Rating Scale;
WAIS-III=
Wechsler Adult Intelligence Scale III

Patients with advanced Parkinson disease (PD) often respond unsatisfactorily to adjustments of pharmacologic treatment.1 In this advanced stage, motor symptoms and dyskinesias are effectively treated by deep brain stimulation (DBS). Both bilateral DBS of the globus pallidus pars interna (GPi) and bilateral DBS of the subthalamic nucleus (STN) are effective procedures in PD.2,–,4 Two randomized controlled trials comparing bilateral DBS of the GPi and bilateral DBS of the STN reported equal efficacy on PD motor symptoms and dyskinesias.2,3 The Netherlands Subthalamic and Pallidal Stimulation (NSTAPS) trial, the third randomized controlled multicenter study comparing bilateral GPi DBS and bilateral STN DBS, indicated greater functional improvement during the medication off-drug phase in STN DBS.4 This study also showed no difference between the groups on a composite score for cognition, mood, and behavior. Conversely, previous studies have reported more cognitive problems in the STN group compared to GPi DBS2,5 and controls with PD.6 A decline in cognition as well as negative changes in mood and other behavioral features have a negative effect on quality of life.7 Thus, the impact of GPi DBS and STN DBS on cognition, mood, and behavior are important aspects of the outcome after surgery. Establishing baseline parameters that can predict cognitive deterioration might help in patient selection for DBS. Only one previous randomized controlled trial comparing neuropsychological outcome after GPi DBS and STN DBS is available. This trial found less motor improvement in the off-drug phase after STN DBS than the NSTAPS trial. In this article, we examine the neuropsychological outcomes after GPi DBS and STN DBS of the NSTAPS trial and investigate the predictive value of baseline parameters on cognitive decline after DBS.

METHODS

Primary outcomes of the initial study were functional health and the number of patients with a negative composite score of cognitive, mood, and behavioral effects. These primary outcomes were published previously. This article describes the results of the neuropsychological tests used for the cognitive evaluation.

This study provides Class I evidence on neuropsychological outcome 12 months after GPi DBS and STN. The study lacks the precision to exclude a moderate difference in outcomes.

Patients.

Between January 2007 and March 2011, 5 participating centers in the Netherlands enrolled a total of 128 patients. Enrollment criteria, study design, and study procedures have been elaborately reported previously.4 Patients were included in the study if they were aged 18 years or older, had idiopathic PD, and, despite optimal pharmacologic treatment, experienced at least one of the following symptoms: severe response fluctuations, dyskinesias, painful dystonias, or bradykinesia. Exclusion criteria consisted of previous stereotactic surgery, Hoehn & Yahr stage 5 at the best moment of the day,8 a Mattis Dementia Rating Scale (MDRS) score of 120 or lower (out of 144),9 active psychosis, or contraindications for the neurosurgical procedure.

Standard protocol approvals, registrations, and patient consents.

The medical ethics committee of each of the participating centers approved the study protocol and patients provided written informed consent. This trial is registered with www.controlled-trials.com (ISRCTN85542074).

Procedures.

Based on a computer-generated sequence, patients were randomly assigned to receive either GPi DBS or STN DBS in a one-to-one ratio, applying a minimization procedure according to drug use (levodopa equivalent dose <1,000 mg vs ≥1,000 mg) and treatment center. Patients as well as clinical, neuropsychological, and psychiatric assessors were blinded for treatment allocation. Patients regularly visited a nonblinded neurologist at the outpatient clinic to adjust DBS settings together with adjustment of PD medication. Adjustments were allowed in both groups. The DBS surgery was performed according to each center's standard protocol, and the final position of the electrode was determined on the basis of MRI, macroelectrode stimulation effects, and, in 3 of 5 centers, semi-microelectrode recordings. Baseline and 12-month motor assessments were done during standardized off-drug and on-drug phases (off phase, withholding antiparkinsonian drugs for 12 hours overnight; on phase, 1 hour after a suprathreshold levodopa dose). Patients performed the neuropsychological tests and questionnaires during the on-drug phase at baseline and 12 months, with the stimulators turned on at 12 months.

Neuropsychological tests.

Neuropsychologists assessed an extensive battery of standardized neuropsychological tests. Premorbid intelligence was assessed using the Dutch Adult Reading Test,10 which is the Dutch version of the National Adult Reading Test. Attention and working memory was assessed using the Stroop color-word test,11 Trail Making Test parts A and B (TMTA/TMTB),12 the subtest Letter and Number Sequencing of the Wechsler Adult Intelligence Scale III (WAIS-III),13 the subtest Digit Span of the WAIS-III, and the Vienna Test System simple and choice reaction speed tests (S1 and S3).14 Executive functions were assessed using the Wisconsin Card Sorting Test15; the Controlled Oral Word Association Test, referred to as phonemic fluency16; and category fluency, referred to as semantic fluency.16 Language was assessed using the Boston Naming Test17 and the subtest Similarities of the WAIS-III.13 Memory was assessed by the Dutch version of the Rey Auditory Verbal Learning Test (RAVLT),18 and logical memory by the Rivermead Behavioral Memory Test (RBMT).19 Spatial reasoning was assessed by the subtest Matrix Reasoning of the WAIS-III.13 Where possible, parallel test versions were used at 12-month assessments to avoid retest effects (see appendix e-1 on the Neurology® Web site at Neurology.org for additional explanation on the neuropsychological tests).

Quality of life.

Quality of life (QOL) was assessed using the Parkinson's Disease Quality of Life Questionnaire (PDQL).20 Scores range from 0 points to 185 points, with higher scores indicating better QOL.

Statistical analysis.

Group differences.

Statistical analyses of neuropsychological data were performed on normative scores corrected for age, sex, or education where appropriate. Change scores for neuropsychological tests were calculated by subtracting baseline scores from 12-month scores. Change scores were checked for normality of distribution, and either t tests or Mann-Whitney U tests were used to compare groups. The 95% confidence interval (CI) was reported. The effect sizes of changes were expressed as Cohen d. These were calculated by taking the difference in mean change score of both groups divided by the pooled SDs of the baseline scores. An effect of 0.20–0.49 reflects a small effect, 0.50 to 0.79 a medium effect, and ≥0.80 a large effect.21 We did not correct the level of significance to reduce the probability of type I error due to multiple comparisons because we were mainly interested in detecting adverse effects of the surgical interventions. Under this circumstance, type II error (failing to detect an effect when it actually exists) is more serious than type I error (considering an effect to be real when it actually is not).22

Predictors of cognitive decline.

Apart from between-group differences, a secondary aim was to predict cognitive decline after DBS using baseline parameters. Cognitive decline at 12 months was defined as a significant worsening on 3 or more cognitive tests based on the reliable change index (RCI).23 A decline in 3 scores means a decline on at least 3 out of 12 different neuropsychological tests. In addition, a test that yields multiple scores is combined into 1 score. Example: the Stroop test resulted in 3 scores, which made up the overall Stroop score. If a patient failed 1 Stroop subtest or more, the overall score was scored as fail. The TMT, RAVLT, RBMT, and fluency tests were scored similarly. The other neuropsychological tests yielded only 1 score. The RCI index was calculated according to RCI = (X2 − X1)/Sdiff, where X1 is the patient's baseline score, X2 is the patient's 12-month score, and Sdiff is the standard error of the difference between the test scores. A score of RCI ≤ −1.645 was considered a significant worsening on a test.

Neuropsychological tests were averaged to form composite scores to reduce the amount of variables and, consequently, to increase the power of the analysis. Tests measuring a similar construct were combined. This was based on literature24 and in accordance with a previous study investigating predictors of cognitive decline after DBS.6 The composite score mental speed consisted of Stroop word reading, Stroop color naming, and TMTA; attention consisted of Stroop color-word interference and TMTB; immediate memory consisted of the immediate recall conditions of the RAVLT and RMBT; and delayed memory consisted of the delayed recall conditions of the RAVLT and RBMT.

First, we investigated if there were differences in the groups in cognitive decline after DBS by the use of a χ2 test. Then, we evaluated which available baseline variables that might influence change in cognition (age, sex, education, disease duration, MDRS, Unified Parkinson's Disease Rating Scale (UPDRS)–III off score, levodopa equivalent dose [LED],25 amount of dopamine agonist expressed in LED, levodopa response, the composite baseline neuropsychological scores and remaining standardized neuropsychological test scores) had a significant (p < 0.20) association with cognitive decline. We included all parameters mentioned above as an exploratory analysis since no stable predictors are available from the literature.

These measures were then entered as independent variables into a multivariable logistic regression model using a stepwise forward approach. Effect sizes were expressed in odd ratios (ORs) with their 95% CI. The Hosmer-Lemeshow test was used to determine the goodness of fit of the model. Multicollinearity of the independent variables was assessed using variance inflation factors.

Impact of cognitive decline on QOL.

We compared QOL in patients who cognitively declined (decliners) based on the RCI with that in patients who did not decline (nondecliners). We calculated a change score by subtracting the baseline score from the 12-month score. The change score was checked for normality of distribution, and either a t test or Mann-Whitney U test was used to compare groups.

Missing data.

If missing values occurred on a test that a patient did not complete due to fatigue or time constraints, the missing score was replaced by the mean score in that specific group. If missing values were due to the inability of the patient to perform the task, the minimum score in that specific group replaced this missing value. Most missing data points were due to fatigue or time constraints; only a small amount of data points were missing due to inability. A total of 7.2% of the neuropsychological data points were missing (4.8% at baseline, 8.8% at 12 months). In the GPi group, 7.0% of the neuropsychological data points were missing: 4.8% at baseline on 18 variables across 16 patients and 9.1% at 12 months on 22 variables across 30 patients. In the STN group, 6.6% of the data points were missing: 4.7% at baseline on 20 variables across 17 patients and 8.5% at 12 months on 16 variables across 25 patients. Analyses with and without missing data yielded comparable results (data available on request). The presented results are based on the imputed dataset.

RESULTS

Characteristics.

A total of 128 patients were randomly assigned to either GPi DBS (65 patients) or STN DBS (63 patients). Fourteen patients, 7 GPi DBS and 7 STN DBS, did not complete neuropsychological assessment at 12 months for the following reasons: some patients refused, some kept canceling appointments, some had no a specified reason. These patients showed no significant differences on baseline measures (age, MDRS, disease duration) and improvement at 12 months on the UPDRS motor section in off-drug phase when compared to the patients with a complete neuropsychological follow-up assessment. Data from 58 GPi DBS patients and 56 STN DBS patients were analyzed. Baseline demographic and clinical characteristics of the 2 groups are shown in table 1.

View this table:
Table 1

Demographic and clinical characteristics at baseline

Between-group comparisons.

Baseline neuropsychological test variables were equally distributed between treatment groups (table 2; raw scores are provided in table e-1). Analyses of change scores showed between-group differences on Stroop word reading (GPi mean [SD] −1.1 [10.4], STN −7.0 [11.3], CI 1.9–10.0) and Stroop color naming (GPi −2.6 [9.6], STN −8.1 [8.1], CI 2.1–8.8), on TMTB (GPi −0.7 [12.0], STN −6.1 [14.2], CI 0.5–10.3), and borderline significance on the WAIS similarities (GPi −0.1 [2.3], STN −0.8 [1.7], CI −0.01 to 1.5) with STN DBS showing greater negative change than GPi DBS. Effect sizes of these differences were small to medium.

View this table:
Table 2

Standardized neuropsychological test scores: Baseline scores and change scores at 12 months in relation to type of intervention

Prediction of cognitive decline.

There was no significant difference between the 2 groups on cognitive decline based on the composite score after DBS. In GPi DBS, 17 patients (29.3%) experienced cognitive decline; in STN DBS, 22 patients (39.3%) experienced cognitive decline (p = 0.26, χ2 test). Six patients had a MDRS below 130 at baseline (1 GPi patient and 5 STN patients). Two STN patients showed significant cognitive decline at 12 months based on the criterion of at least 3 significant RCIs, which is similar to the percentage of patients with cognitive decline in the entire group. The following independent variables were identified as potential predictors for cognitive decline and entered into the logistic regression model based on p < 0.20: age, disease duration, MDRS, agonist LED dose, digit span, semantic fluency (table 3; see table e-2 for the association analyses of all baseline parameters). The stepwise forward regression model showed age at baseline (OR 1.10, 95% CI 1.03–1.18, p = 0.003) and semantic fluency at baseline (OR 1.06, 95% CI 1.01–1.12, p = 0.032) as independent predictors (table 3). The regression model appeared to fit the data (Hosmer-Lemeshow test: p = 0.70). Variance inflation factors indicated that multicollinearity was low (<1.30).

View this table:
Table 3

Impact of baseline parameters on cognitive decline 12 months after DBS

Impact of cognitive decline on QOL.

PDQL results show no significant differences on change scores between decliners and nondecliners (mean improvement of decliners: 9.9 ± 19.6, nondecliners: 15.8 ± 17.9, CI −1.5 to 13.3).

DISCUSSION

This in-depth analysis of the neuropsychological data of the NSTAPS trial shows only small differences between GPi DBS and STN DBS at 12 months after DBS. We found significant differences on Stroop word reading, Stroop color naming, TMTB, and WAIS similarities, with STN DBS showing greater negative change than GPi DBS. These results suggest a larger decline in mental speed (Stroop word reading and Stroop color naming), attention (TMTB), and possibly language (WAIS similarities) after STN DBS. However, this effect was not reproduced on the TMTA and Stroop color-word interference, respectively. These differences in cognitive change are similar to previous randomized controlled trials comparing GPi DBS and STN DBS. Follet et al.3 only found a significant difference between the groups on a task measuring processing speed and working memory (WAIS-III digit symbol test), with the decline being greater for STN DBS after 24 months. Although different cognitive tasks were used, the differences between GPi DBS and STN DBS seem to occur mainly on tasks measuring components of speed.3,4 One must interpret the statistically significant findings with care since we did not correct for multiple comparisons.

The rate of cognitive decline in our study appears high compared to a recent publication by Rothlind et al.26 The amount of patients showing cognitive decline based on the RCIs was about 3 times as high (NSTAPS: GPi 29.3%, STN DBS 39.3% compared to Rothlind: 10.9% for DBS in general) in our study. However, the Rothlind et al. study uses a different strategy for calculating a composite RCI for overall decline, which makes comparison of how many patients show cognitive decline between the 2 studies difficult. Results are similar when comparing percent decline on individual neuropsychological tests (mean decline on all matching tests of the 2 studies: 9.0% in the Rothlind study and 6.5% in our study on matching tests).

In contrast to the Rothlind et al. study, we found an improvement in QOL in both the decliners and nondecliners. The difference in improvement between these groups was not statistically significant. This could be a power issue.

In the smaller study by Anderson et al.,2 cognitive complications were only observed in the STN group. A recently published review concluded that there might be a possible advantage of unilateral and bilateral GPi DBS over STN DBS when comparing cognitive outcomes.27 However, the clinical relevance of this difference is unknown, since functional outcome scores and quality of life scores do not differ between these groups.2,4 Additionally, no difference was found in our study between GPi DBS and STN DBS when using a composite score for neuropsychological examination.

STN DBS might even be superior to GPi DBS when evaluating functional improvement during the medication off-drug phase.4

The predictive model from the multivariate logistic regression indicated higher age and better semantic fluency at baseline as independent predictors for cognitive decline at 12 months. Age is a plausible predictor for cognitive outcome. Better baseline semantic fluency, on the other hand, was not expected to predict cognitive decline. We have no satisfactory explanation for this finding.

To our knowledge, only 2 other studies have reported on predictive modeling of cognitive decline after DBS. Smeding et al.6 reported age, attention, and levodopa response at baseline to be predictors for cognitive decline at 12 months in STN DBS. The statistical evaluation and method of assessment of cognitive decline was different in our study. Cognitive decline in our study is based on RCI derived from the test manuals, whereas in the study by Smeding et al. it was based on multivariate normative comparison with the PD control group.

The other study indicated that baseline list learning and IQ were the best predictors for post DBS immediate story recall, the variable that was most affected after STN DBS in their sample.28 This study did not asses predictors of decline of cognition on a composite score.

The results from our regression analysis, as well as the variation in predictors between different studies thus far, suggest that these models for predicting cognitive outcome are unstable. Small sample sizes and differences in study protocols might contribute to this variation. A stable predictive model would be useful for clinicians in daily practice. Since new randomized controlled trials between GPi DBS and STN DBS are less likely to be performed, a meta-analysis using individual patient data of previous studies might be the preferred strategy to obtain a more reliable prediction model for cognitive outcome after DBS.

No large differences in neuropsychological outcome between GPi DBS and STN DBS have been found in randomized clinical trials. The choice for either GPi DBS or STN DBS cannot be reliably based on baseline patient characteristics with the models that are currently available.

AUTHOR CONTRIBUTIONS

Dr. Odekerken: conceptualization of the study, analysis and interpretation of the data, drafting and revision of the manuscript. Ms. Boel: analysis and interpretation of the data, drafting and revision of the manuscript. Dr. Geurtsen: interpretation of the data, revision of the manuscript. Dr. Schmand: conceptualization of the study, interpretation of the data, revision of the manuscript. Dr. de Haan: interpretation of the data, revision of the manuscript. Dr. Schuurman: interpretation of the data, revision of the manuscript. Dr. de Bie: design and conceptualization of the study, interpretation of the data, revision of the manuscript. The NSTAPS study group: revision of the manuscript.

STUDY FUNDING

The NSTAPS study group is supported by a grant from Stichting Parkinson Fonds (Hoofddorp, the Netherlands), Prinses Beatrix Fonds (The Hague, the Netherlands), and Parkinson Vereniging (Bunnik, the Netherlands). The Movement Disorders department of the Academic Medical Center receives an unrestricted fellowship grant from Medtronic.

DISCLOSURE

V. Odekerken has received a traveling grant from Medtronic. J. Boel reports no disclosures relevant to the manuscript. G. Geurtsen received grants from the Michael J. Fox Foundation and Parkinson Fonds. B. Schmand is a consultant for the Pearson Assessment at Boom Test Publishers. I. Dekker and R. de Haan report no disclosures relevant to the manuscript. P. Schuurman has received lecture payments from Medtronic. R. de Bie received financial support for travel and hotel for scientific conferences from Medtronic and received research grants from ZonMw, Stichting Parkinson Fonds, Prinses Beatrix Fonds, Parkinson Vereniging, Kinetics Foundation, and GEHealth. Go to Neurology.org for full disclosures.

Footnotes

  • ↵* These authors contributed equally to this work.

  • Coinvestigators are listed on the Neurology® Web site at Neurology.org.

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Supplemental data at Neurology.org

  • Received August 4, 2014.
  • Accepted in final form December 15, 2014.

REFERENCES

  1. 1.↵
    1. Vidailhet M
    . Movement disorders in 2010: Parkinson disease: symptoms and treatments. Nat Rev Neurol 2011;7:70–72.
    OpenUrlPubMed
  2. 2.↵
    1. Anderson VC,
    2. Burchiel KJ,
    3. Hogarth P,
    4. Favre J,
    5. Hammerstad JP
    . Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease. Arch Neurol 2005;62:554–560.
    OpenUrlCrossRefPubMed
  3. 3.↵
    1. Follett KA,
    2. Weaver FM,
    3. Stern M,
    4. et al
    . Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. N Engl J Med 2010;362:2077–2091.
    OpenUrlCrossRefPubMed
  4. 4.↵
    1. Odekerken VJ,
    2. van Laar T,
    3. Staal MJ,
    4. et al
    . Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson's disease (NSTAPS study): a randomised controlled trial. Lancet Neurol 2013;12:37–44.
    OpenUrlCrossRefPubMed
  5. 5.↵
    1. Okun MS,
    2. Foote KD
    . Subthalamic nucleus vs globus pallidus interna deep brain stimulation, the rematch: will pallidal deep brain stimulation make a triumphant return? Arch Neurol 2005;62:533–536.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Smeding HM,
    2. Speelman JD,
    3. Huizenga HM,
    4. Schuurman PR,
    5. Schmand B
    . Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson's disease. J Neurol Neurosurg Psychiatry 2011;82:754–760.
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    1. Schrag A,
    2. Jahanshahi M,
    3. Quinn N
    . What contributes to quality of life in patients with Parkinson's disease? J Neurol Neurosurg Psychiatry 2000;69:308–312.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    1. Hoehn MM,
    2. Yahr MD
    . Parkinsonism: onset, progression and mortality. Neurology 1967;17:427–442.
    OpenUrlFREE Full Text
  9. 9.↵
    1. Mattis S
    . Dementia Rating Scale Professional Manual. Odessa, FL: Psychological Assessment Resources; 1973.
  10. 10.↵
    1. Schmand B,
    2. Lindeboom J,
    3. van Harskamp F
    . Nederlandse Leestest Voor Volwassenen (Dutch Adult Reading Test). Lisse, the Netherlands: Swets and Zeitlinger; 1992.
  11. 11.↵
    1. Stroop JR
    . Studies of interference in serial verbal reactions. J Exp Psychol 1935;1935:643–662.
    OpenUrl
  12. 12.↵
    1. Reitan RM
    . Trail Making Test Manual for Administration and Scoring. Tucson, AZ: Reitan Neuropsychological Laboratory; 1992.
  13. 13.↵
    1. Wechsler D
    . WAIS-III Administration and Scoring Manual. San Antonio: The Psychological Corporation; 1997.
  14. 14.↵
    Schuhfried GmbH. Vienna Test System, RT Reaction Test. Moedling, Austria: 2004.
  15. 15.↵
    1. Alpherts WCJ,
    2. Aldenkamp AP
    . Fepsy. Heemstede: Instituut voor epilepsiebestrijding; 1994.
  16. 16.↵
    1. Rosen WG
    . Verbal fluency in aging and dementia. J Clin Neuropsychol 1980;2:135–146.
    OpenUrlCrossRef
  17. 17.↵
    1. Kaplan EG,
    2. Goodglass H,
    3. Weintraub S
    . Boston Naming Test. Philadelphia: Lea and Febiger; 2005.
  18. 18.↵
    1. Rey A
    . l'Éxamen Clinique en Psychologie. Paris: Presses Universitaires de France; 1964.
  19. 19.↵
    1. Wilson B,
    2. Cockburn J,
    3. Baddeley AD
    . The Rivermead Behavioral Memory Test. Reading, UK: Thames Valley Test Company; 1985.
  20. 20.↵
    1. de Boer AG,
    2. Wijker W,
    3. Speelman JD,
    4. de Haes JC
    . Quality of life in patients with Parkinson's disease: development of a questionnaire. J Neurol Neurosurg Psychiatry 1996;61:70–74.
    OpenUrlAbstract/FREE Full Text
  21. 21.↵
    1. Cohen JD
    . Statistical Power Analysis for the Behavioral Science. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988.
  22. 22.↵
    1. Rothman KJ
    . No adjustments are needed for multiple comparisons. Epidemiology 1990;1:43–46.
    OpenUrlCrossRefPubMed
  23. 23.↵
    1. Jacobson NS,
    2. Truax P
    . Clinical significance: a statistical approach to defining meaningful change in psychotherapy research. J Consult Clin Psychol 1991;59:12–19.
    OpenUrlCrossRefPubMed
  24. 24.↵
    1. Lezak MD,
    2. Howieson DB,
    3. Bigler ED,
    4. Tranel D
    . Neuropsychological Assessment. New York: Oxford University Press; 2012.
  25. 25.↵
    1. Esselink RA,
    2. de Bie RM,
    3. de Haan RJ,
    4. et al
    . Unilateral pallidotomy versus bilateral subthalamic nucleus stimulation in PD: a randomized trial. Neurology 2004;62:201–207.
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    1. Rothlind JC,
    2. York MK,
    3. Carlson K,
    4. et al
    . Neuropsychological changes following deep brain stimulation surgery for Parkinson's disease: comparisons of treatment at pallidal and subthalamic targets versus best medical therapy. J Neurol Neurosurg Psychiatry Epub 2014 Sep 2.
  27. 27.↵
    1. Williams NR,
    2. Foote KD,
    3. Okun MS
    . STN vs. GPi deep brain stimulation: translating the rematch into clinical practice. Mov Disord Clin Pract 2014;1:24–35.
    OpenUrl
  28. 28.↵
    1. Yaguez L,
    2. Costello A,
    3. Moriarty J,
    4. et al
    . Cognitive predictors of cognitive change following bilateral subthalamic nucleus deep brain stimulation in Parkinson's disease. J Clin Neurosci 2014;21:445–450.
    OpenUrlPubMed

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