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Psychometric Properties of the Starkstein Apathy Scale in Patients With Early Untreated Parkinson Disease
Psychometric Properties of the Starkstein Apathy Scale in Patients With Early Untreated Parkinson Disease Kenn Freddy Pedersen, M.D., Ph.D., Guido Alves, M.D., Ph.D., Jan Petter Larsen, M.D., Ph.D., Ole-Bjørn Tysnes, M.D., Ph.D., Simon Geir Møller, Ph.D., Kolbjørn Brønnick, Ph.D. Background: Although the 14-item Starkstein Apathy Scale (SAS) is recommended to screen for and measure the severity of apathetic symptoms in Parkinson disease (PD), the psychometric attributes of this scale have not yet been fully evaluated. Objective: The authors examined the reliability, factor structure, and discriminant validity of the SAS in 194 nondemented patients with early untreated PD. Design: Cross-sectional multicenter population-based study from Western and Southern Norway. Measurements: Standardized rating scales for parkinsonism and neuropsychiatric symptoms. Results: The SAS showed fair internal consistency (Cronbach’s α = 0.69) and exploratory factor analysis identified two factors: the first factor (24.2% of the variance) represented cognitive-behavioral aspects of apathy (items 1, 2, and 4–8; Cronbach’s α = 0.74) and the second factor (15.0% of the variance) a general apathy dimension (items 3 and 9–14; Cronbach’s α = 0.52). The correlation between these two factors was low (Spearman’s r = 0.19, N = 194, p = 0.008), indicating clinically distinct dimensions, but both factor scores were strongly related to the total SAS score (Spearman’s r > 0.6, N = 194, p < 0.0005). Item 3 (insight or self-reflection) showed a negative item-total correlation, and removing this item raised the Cronbach’s α of the second factor to 0.70, but did not substantially alter the other results. Both the total score and factor scores of SAS showed fair discriminant validity. Conclusions: Although the SAS showed fairly good psychometric properties and the exploratory factor analysis suggested a two-factor solution, the results with this PD sample indicate that item 3 is ambiguous and should be considered removed from the scale. (Am J Geriatr Psychiatry 2012; 20:142–148) Key Words: Discriminant validity, factor analysis, Parkinson disease, reliability, Starkstein Apathy Scale
Received October 8, 2010; revised May 23, 2011; accepted June 6, 2011. From the Norwegian Centre for Movement Disorders, Stavanger University Hospital, Stavanger, Norway (KFP, GA, JPL, SGM, KB); Department of Neurology, Stavanger University Hospital, Stavanger, Norway (KFP, GA, JPL); Department of Neurology, Haukeland University Hospital, Bergen, Norway (O-BT); and Centre of Organelle Research, Faculty of Science and Technology, University of Stavanger, Stavanger, Norway (SGM). Send correspondence and reprint requests to Dr. Kenn Freddy Pedersen, The Norwegian Centre for Movement Disorders, Stavanger University Hospital, PO Box 8100, N-4068 Stavanger, Norway. e-mail: [email protected] C 2012 American Association for Geriatric Psychiatry DOI: 10.1097/JGP.0b013e31823038f2
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Pedersen et al.
A
pathy is a common behavioral problem in Parkinson disease (PD) and other neurodegenerative disorders across ethnically and culturally different populations.1–4 In a recent review of the psychometric properties of apathy rating scales,5 a Movement Disorder Society task force concluded that the Starkstein Apathy Scale (SAS) is the most appropriate psychometric tool for assessing apathy in PD patients. The SAS consists of 14 items (total score range 0–42; higher scores indicate more severe apathy) phrased as questions that are to be answered on a four-point Likert scale (intensity scores: not at all, slightly, some, a lot). In the first eight questions, the “not at all” answer corresponds to severe apathy; for question 9–14, the intensity scores are reversed, such that the “a lot” answer corresponds to more severe apathy. Using the original patient-based version, Starkstein and colleagues6 reported good face validity and internal consistency (Cronbach’s α = 0.76) in 50 PD patients, acceptable criterion validity (comparison to clinical impression as a gold standard yielded a sensitivity of 66% and a specificity of 100% when using a cut-off score of 13/14) in 12 PD patients, as well as good interrater (r = 0.81) and test-retest (r = 0.90) reliability in 11 PD patients.6 Clinimetric testing of the SAS has not been performed in larger PD cohorts, nor by others than the original developers, who did not assess the factor structure or itemtotal correlations. As apathy is one of the main psychiatric manifestations in untreated PD,7 and because dopaminergic drugs have the potential to influence the occurrence and severity of apathy in early PD,8 a large cohort of newly diagnosed patients with untreated PD from the Norwegian ParkWest study9 was recruited to examine the psychometric attributes of SAS. Although apathy is now considered as one single syndrome, recent consensus diagnostic criteria10 define apathy as a disorder of motivation characterized by symptoms in three different domains: behavioral, cognitive, and emotional. Therefore, we hypothesized that these three domains should be revealed as different factors in an exploratory factor analysis of the SAS. Reliability was assessed using Cronbach’s α and item-total correlations, whereas correlational analyses were conducted to investigate the discriminant validity of the SAS.
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SUBJECTS AND METHODS Study Design, Case Ascertainment, and Diagnostic Procedures The study is part of the Norwegian ParkWest project, a multicenter population-based prospective longitudinal cohort study of the incidence, neurobiology, and prognosis of PD in Western and Southern Norway. Findings obtained from the baseline evaluation of patients who were assessed between November 1, 2004, and August 31, 2006, were used for the present analysis. The study was approved by the Regional Committee for Medical Research Ethics at the University of Bergen and signed written informed consent was obtained from all subjects. A detailed description of the multiple case finding strategies and the diagnostic procedures is provided elsewhere.9 Briefly, we established a representative incident cohort of 212 unmedicated patients who fulfilled accepted diagnostic research criteria of idiopathic PD.11 To optimize diagnostic accuracy at this early stage, only patients whose diagnosis remained unchanged during follow-up, on average 28 months after inclusion, were included in the project. General exclusion criteria were cases with possible or probable dementia with Lewy bodies, Alzheimer disease, vascular parkinsonism, or atypical parkinsonian disorders including multiple system atrophy, corticobasal degeneration, and progressive supranuclear palsy.9 In the present study, we also excluded patients who met diagnostic criteria of PD-related dementia, on the basis of clinical history and examination, and comprehensive neuropsychological assessment, as previously described.12 Subjects Of the 212 subjects who agreed to take part in a longitudinal study follow-up and participated in standardized baseline examinations, 201 had never been exposed to antiparkinson drugs. In addition, seven patients fulfilled operationalized criteria for dementia,13 all with typical PD without a history of cognitive impairment during the first year after motor onset, leaving 194 patients eligible for inclusion in this study.
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Psychometric Properties of the Starkstein Apathy Scale Assessments Neurologists from the ParkWest study group performed standardized assessments, including a semistructured interview on demographic variables, medical history, and medication, in addition to general neurological and medical examinations. Severity of motor symptoms and disability was rated using the Unified Parkinson’s Disease Rating Scale, parts II and III.14 Global cognitive status was assessed with the Mini Mental State Exam15 and severity of depressive symptoms was determined using the Montgomery-Aasberg Depression Rating Scale.16 Fatigue severity was examined using the Fatigue Severity Scale.17 Apathy was measured using the selfreport version of SAS, which has previously been translated from the original English version6 into Norwegian by Aarsland.18 The SAS is an abridged and modified version of Marin’s Apathy Evaluation Scale19 and includes items concerning diminished motivation (items 7 and 12) as well as behavioral (items 4, 5, 8, and 9), cognitive (items 1, 2, 6, and 11), emotional (items 10 and 13), and insight (items 3 and 14) aspects of apathy.20 In the present study, back-translation was made by one of the authors (SGM) who is bilingual but did not know the original English text. A critical assessment of the backtranslation was made by four of the authors (KFP, GA, JPL, and KB) to ensure that the original and translated versions of SAS were acceptable equivalent. Clinical examination was performed blind to the SAS scores.
to retain was determined by a subsequent evaluation of the Kaiser’s criterion (eigenvalues >1), inspection of the screeplot (number of factors above the elbow, or break in the plot), and the clinical meaningfulness of the factor solutions. Reliability of the SAS was evaluated using Cronbach’s α coefficient (internal consistency) and corrected Pearson’s item-total correlations. Correlational analyses (Spearman’s r [rs ] for nonparametric data) were performed to investigate the relationship between individual items and the total score of SAS, the relationship between SAS total score and factor scores, and the discriminant validity of the SAS. Effect sizes for the correlation coefficients were defined by the following criteria: rs < 0.3, weak; rs = 0.3– 0.5, moderate; rs >0.5, strong.22 Mann-Whitney tests were used for comparisons of medians for continuous variables when appropriate. Statistics were performed using SPSS version 15.0 (SPSS, Inc., Chicago, IL). All tests were two-tailed, with p values <0.05 considered statistically significant.
RESULTS Demographic and clinical data for the PD patients are shown in Table 1, whereas the mean value (SD) of the items comprising the SAS and the Spearman’s correlation coefficients of each item with the total SAS score are presented in Table 2. Of notice, all items except item 3 (concerned about health problems) were significantly correlated with the total score (all rs ≥0.28, N = 194, p < 0.0005). The total SAS scores were
Statistical Analysis Before exploring the underlying structure of SAS using exploratory factor analysis, the data were assessed for its suitability for factor analysis. Inspection of the correlation matrix showed several coefficients > 0.3, the Bartlett’s test of sphericity was highly significant (p < 0.0005), and the Kaiser-Meyer-Olkin measure of sampling adequacy value was 0.76; all assessments supporting the factorability of the dataset.21 Principal component analysis was used to extract the factors followed by Varimax (orthogonal) rotation. We chose to use an orthogonal rotation because of the explorative design of this study and because the SAS items were hypothesized to be indicators of three different factors, which implies the factors to be uncorrelated. The number of factors
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TABLE 1. Demographic and Clinical Characteristics of Patients With Early Untreated PD (N = 194) Variable
Value
Age, years Education, years Male, n (%) Disease duration, years UPDRS ADL score UPDRS motor score MMSE score MADRS score Antidepressants, n (%)a Sedatives, n (%)a
67.9 (9.0) 11.0 (3.3) 115 (59.3) 2.3 (1.8) 8.8 (5.0) 23.2 (11.4) 27.8 (2.3) 4.5 (5.0) 27 (13.9) 22 (11.3)
Notes: Data are mean (SD) or number (% of assessed patients). ADL: activity of daily living; MMSE: Mini Mental State Exam; MADRS: Montgomery-Aasberg Depression Rating Scale; UPDRS: Unified Parkinson’s Disease Rating Scale. a Missing data for two patients (N = 192).
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Pedersen et al. strictly unimodal distributed with a mean score of 15.5 (SD 4.6), median 15.0, and range 4–29. Reliability The Cronbach’s α value for the 14-item SAS was 0.69. Analysis of the SAS items (corrected Pearson’s item-total correlations) indicated good and acceptable item characteristics (correlations >0.30, N = 194)23 for most of the items, see last column of Table 2. For items 8 (energy for daily activities), 9 (dependency on prompts to structure everyday activity), and 13 (neither happy nor sad), discriminatory power was small (correlations ≤ 0.20, N = 194). Noteworthy, item 3 showed a negative value of − 0.12, which indicates that subjects with low scores on this question get high scores on the total SAS score. After removing item 3 from the scale, the Cronbach’s α for the modified 13-item SAS was 0.74. Exploratory Factor Analysis Principal component analysis revealed four eigenvalues exceeding 1, accounting for 57.7% of the variance. From inspection of the screeplot, a two-factor model provided the best fit. The two-factor solution also gave the most clinically meaningful model, with the major factor accounting for 24.2% and the minor for 15.0% of the variance. Varimax rotation was then performed, and inspection of the rotated com-
TABLE 2.
ponent matrix (Table 3) showed a clear two factor solution, with both components showing a number of strong loadings. The correlation between the two factor scores was weak (rs = 0.19, N = 194, p = 0.008). Factor 1 included items representing cognitivebehavioral aspects of apathy (Cronbach’s α = 0.74, corrected item-total correlation range 0.23–0.66), whereas factor 2 represented a general apathy dimension including aspects of insight (Cronbach’s α = 0.52, corrected item-total correlation range − 0.18–0.48). As with the entire 14-item SAS, item 3 showed a negative corrected item-total correlation ( − 0.18) with factor 2. The correlation between the total score of SAS and the sum score of each factor was strong (rs = 0.82, N = 194, p < 0.0005 for factor 1; and rs = 0.67, N = 194, p < 0.0005 for factor 2). Because item 3 showed poor item-total correlation, we explored the structure of the SAS after removal of this item. Principal component analysis with Varimax rotation was repeated for the remaining 13 items, which confirmed the two-factor solution previously found for the original scale (except for item 3 removed), accounting for 41.7% of the variance. The Cronbach’s α value for factor 1 remained unchanged (0.74), but increased to 0.70 for the new factor 2 (corrected item-total correlations range 0.37–0.52). The correlation between the modified 13-item SAS total score and the sum score of each factor remained almost unaltered (rs = 0.83, N = 194, p < 0.0005 for factor 1; and rs = 0.63, N = 194, p < 0.0005 for factor 2), as
SAS Item Characteristics (N = 194)
Item
Mean (SD)
Correlation With Total SAS Scorea
Item—Total Correlationb
1. Are you interested in learning new things? 2. Does anything interest you? 3. Are you concerned about your condition? 4. Do you put much effort into things? 5. Are you always looking for something to do? 6. Do you have plans and goals for the future? 7. Do you have motivation? 8. Do you have the energy for daily activities? 9. Does someone have to tell you what to do each day? 10. Are you indifferent to things? 11. Are you unconcerned with many things? 12. Do you need a push to get started on things? 13. Are you neither happy nor sad, just in between? 14. Would you consider yourself apathetic?
1.46 (0.74) 0.92 (0.76) 1.62 (0.91) 1.45 (0.77) 1.64 (0.83) 1.67 (0.86) 1.43 (0.79) 1.35 (0.66) 0.19 (0.41) 0.53 (0.65) 0.98 (0.75) 0.85 (0.72) 1.21 (0.77) 0.21 (0.46)
0.57 0.49 0.08 0.44 0.43 0.66 0.72 0.27 0.28 0.49 0.42 0.52 0.34 0.42
0.44 0.36 − 0.12 0.28 0.31 0.57 0.63 0.16 0.19 0.37 0.29 0.41 0.20 0.35
SAS: Starkstein Apathy Scale. a Uncorrected Spearman correlation coefficient (nonparametric); all items p <0.0005, except item 3, which was not significant (N = 194, p = 0.271). b Corrected Pearson correlation coefficient.
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Psychometric Properties of the Starkstein Apathy Scale
TABLE 3.
Factor Analysis of the 14-Item SAS (Two-Factor Solution)
Item 6. Do you have plans and goals for the future? 7. Do you have motivation? 1. Are you interested in learning new things? 2. Does anything interest you? 4. Do you put much effort into things? 5. Are you always looking for something to do? 8. Do you have the energy for daily activities? 14. Would you consider yourself apathetic? 10. Are you indifferent to things? 13. Are you neither happy nor sad, just in between? 11. Are you unconcerned with many things? 9. Does someone have to tell you what to do each day? 12. Do you need a push to get started on things? 3. Are you concerned about your condition? Eigenvalue Variance explained by each factor (%) Internal consistency (Cronbach’s α)
Factor 1: CognitiveBehavioral Apathy
Factor 2: General Apathy
0.82
0.04
0.76
0.30
0.70
0.07
0.66
− 0.01
0.52
− 0.14
0.47
0.05
0.32
0.13
0.15
0.71
0.14
0.68
0.05
0.60
0.03
0.60
− 0.07
0.58
0.23
0.58
0.04
− 0.35
3.4 24.2
2.1 15.0
0.74
0.52a
SAS: Starkstein Apathy Scale. Notes: N = 194. Major loadings > 0.3 for each item are in bold. a Cronbach’s α after removal of item 3 from factor 2 was 0.70.
did the intercorrelation between the two factor scores (rs = 0.18, N = 194, p = 0.01). Discriminant Validity Table 4 presents the results of the correlational analyses examining the discriminant validity of the SAS. Both the total score and the two-factor model of the 14-item SAS showed weak to moderate correlations with the Montgomery-Aasberg Depression Rating Scale, Mini Mental State Exam, Unified Parkinson’s Disease Rating Scale motor, and Fatigue
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Severity Scale scores (rs ≤ 0.31, N = 194), which indicate fair discriminant validity of the self-report version of SAS. To explore whether the use of antidepressants or sedatives (11.3%–13.9% of the patients) could have influenced the results, bivariate analyses with type of medication as the dependent variable and total score and factor scores of the SAS as independent variables were performed. Patients using either antidepressants (n = 27) or sedatives (n = 22) scored significantly higher on the 14-item total score (range 0–42) (mean 17.0 [SD 4.8] versus 15.3 [4.5], Mann-Whitney z = − 1.97, N = 192, p = 0.049 for antidepressant therapy or not; mean 18.0 [SD 5.2] versus 15.2 [4.4], MannWhitney z = − 2.39, N = 192, p = 0.017 for use of sedatives or not) and factor 1 score (range 0–21) (mean 11.0 [SD 3.6] versus 9.7 [3.3], Mann-Whitney z = − 2.13, N = 192, p = 0.033 for antidepressant therapy or not; mean 12.4 [SD 3.8] versus 9.6 [3.2], Mann-Whitney z = − 3.38, N = 192, p = 0.001 for use of sedatives or not) than those without such medication. In contrast, no difference in factor 2 scores was found among patients using antidepressants or sedatives compared with unmedicated patients.
DISCUSSION The main purpose of this study was to explore the factor structure of the self-report version of SAS in a large cohort of newly diagnosed patients with drugna¨ıve PD. On the basis of recent consensus diagnostic criteria for apathy,10 we hypothesized that the behavioral, cognitive, and emotional domains of apathy should be revealed as different factors in the exploratory factor analysis of the SAS. This hypothesis was not supported by the data. Instead, we found that the 14 items of the SAS fell into two clinically distinct and relevant apathy factors. The low correlation between the factors and the strong correlation of each factor with the total score of SAS suggests that these factors not only capture unique aspects of PD-related apathy but also measure a single apathy construct. There was a fair level of internal consistency for the entire scale and the cognitive-behavioral apathy factor, whereas the internal consistency for the general apathy factor was inadequate. The Cronbach’s α for the SAS in our study was approximately similar to that reported by Starkstein and colleagues6 in their
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Pedersen et al.
TABLE 4.
Discriminant Validity of the 14-Item SAS and the Two-Factor Model
Variable MADRS score MMSE score UPDRS motor score FSS mean score
Total SAS Score
Cognitive-Behavioral Apathy Factor
General Apathy Factor
General Apathy Factor (Without Item 3)
0.25a − 0.17b 0.21a 0.14
0.24a − 0.24a 0.31c 0.17b
0.14b − 0.02 − 0.03 0.001
0.28c 0.01 − 0.01 0.13
Notes: SAS: Starkstein Apathy Scale; FSS: Fatigue Severity Scale; MADRS: Montgomery-Aasberg Depression Rating Scale; MMSE: Mini Mental State Exam; UPDRS: Unified Parkinson’s Disease Rating Scale; N = 194. a p < 0.005. b p < 0.05. c p < 0.0005.
original psychometric study of this scale, which included fewer patients with more advanced disease. Further reliability analysis revealed that the majority of SAS items showed good discriminant power, whereas three items (8, 9, and 13) had less adequate item characteristics. In addition, item 3 had a negative item-total correlation, indicating that patients who get low scores on this question (i.e., more concerned about their condition) get high scores on the total SAS score. Thus, this item proved to be highly ambiguous and therefore less suitable as a screening question for apathy in our PD sample. Indeed, removal of this item increased the internal consistency of the entire scale (modified 13-item SAS) and factor 2 subscale in particular. If replicated by others, a modified version of SAS with item 3 excluded might therefore be more appropriate to assess apathy in PD patients. The correlations between the total score and factor scores of SAS and standardized measurements of depression, cognitive impairment, parkinsonism, and fatigue were only weak to moderate (Table 4), indicating at least fair discriminant validity of the self-report version of SAS. In addition, the relationship between use of antidepressants or sedatives and the total score and factor scores of the SAS was explored. We found that these drugs were associated with higher total scores and cognitivebehavioral factor scores of the 14-item SAS. This finding was not unexpected, given the overlapping symptoms between apathy and depression,24 and the fact that apathy and anxiety are frequent residual symptoms among individuals treated for depressive disorder.25 We did not examine the criterion or convergent validity of SAS, which is a shortcoming of this study.
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Such data would have been valuable since high reliability of a rating scale not necessarily implies that it actually assess the construct of interest. At present, we are not aware of any studies reporting the convergent validity of SAS. However, Starkstein and colleagues6 reported acceptable criterion validity of the 14-item SAS using clinical impression as a gold standard for a diagnosis of apathy in patients with PD. Nevertheless, future studies should include structured interviews with patients and informants, using recently proposed consensus criteria for apathy as a guide,10 to investigate the validity of SAS in patients with PD. Although acceptable reliability and factor structure are important pieces of evidence for the internal structure of a clinical rating scale,26 this is to our knowledge the first study ever to examine the item-total correlation and factor structure of the SAS. Because the SAS is gaining popularity as a brief screening instrument for measurement of apathy in a variety of clinical populations,5 further studies exploring its factor structure in different populations are needed before one could make inferences based on the resultant scores. The findings here should be considered in the context of an exploratory factor analysis, which requires follow-up studies confirming whether the factor structure may be generalizable to patients with early PD using antiparkinsonian drug therapy, or to more advanced cases of PD. In summary, the results of this study support the use of the self-report version of SAS as a reliable and valid assessment instrument for measuring the severity of apathy symptoms, as well as distinct dimensions of apathy, in early untreated PD. However, because of the apparent ambiguity of item
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Psychometric Properties of the Starkstein Apathy Scale 3, this question may be considered removed from the scale to increase its internal consistency, especially when examining the different apathy dimensions of SAS revealed in this study. The two-factor model of SAS needs to be confirmed and future studies should attempt to clarify whether longitudinal changes in specific SAS domains rather than total scores would better predict the impact of apathy in patients with PD.
The authors are grateful to all patients for their willingness to participate in this study. We also thank all personnel who contributed to planning and conducting this study. The Norwegian ParkWest study was funded by the Western Norway Regional Health Authority (grant # 911218) and the Research Council of Norway (grant # 177966). The authors have no disclosures to report.
References 1. van Reekum R, Stuss DT, Ostrander L: Apathy: why care? J Neuropsychiatry Clin Neurosci 2005; 17:7–19 2. Aarsland D, Marsh L, Schrag A: Neuropsychiatric symptoms in Parkinson’s disease. Mov Disord 2009; 24:2175–2186 3. Tatsch MF, Bottino CM, Azevedo D, et al: Neuropsychiatric symptoms in Alzheimer disease and cognitively impaired, nondemented elderly from a community-based sample in Brazil: prevalence and relationship with dementia severity. Am J Geriatr Psychiatry 2006; 14:438–445 4. Chan WC, Lam LC, Tam CW, et al: Prevalence of neuropsychiatric symptoms in Chinese older persons with mild cognitive impairment-a population-based study. Am J Geriatr Psychiatry 18:948–954 5. Leentjens AF, Dujardin K, Marsh L, et al: Apathy and anhedonia rating scales in Parkinson’s disease: critique and recommendations. Mov Disord 2008; 23:2004–2014 6. Starkstein SE, Mayberg HS, Preziosi TJ, et al: Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 1992; 4:134–139 7. Aarsland D, Bronnick K, Alves G, et al: The spectrum of neuropsychiatric symptoms in patients with early untreated Parkinson’s disease. J Neurol Neurosurg Psychiatry 2009; 80:928–930 8. Bodi N, Keri S, Nagy H, et al: Reward-learning and the noveltyseeking personality: a between- and within-subjects study of the effects of dopamine agonists on young Parkinson’s patients. Brain 2009; 132:2385–2395 9. Alves G, Muller B, Herlofson K, et al: Incidence of Parkinson’s disease in Norway: the Norwegian ParkWest study. J Neurol Neurosurg Psychiatry 2009; 80:851–857 10. Robert P, Onyike CU, Leentjens AF, et al: Proposed diagnostic criteria for apathy in Alzheimer’s disease and other neuropsychiatric disorders. Eur Psychiatry 2009; 24:98–104 11. Gelb DJ, Oliver E, Gilman S: Diagnostic criteria for Parkinson disease. Arch Neurol 1999; 56:33–39 12. Aarsland D, Bronnick K, Larsen JP, et al: Cognitive impairment in incident, untreated Parkinson disease: the Norwegian ParkWest study. Neurology 2009; 72:1121–1126 13. Emre M, Aarsland D, Brown R, et al: Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 2007; 22:1689–1707
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14. Fahn S, Elton RL: Unified Parkinson’s Disease Rating Scale, in Recent Developments in Parkinson’s Disease. In: Fahn S, Marsden CD, Calne DB, Goldstein M. eds. Florham Park, New Jersey: Macmillan Healthcare Information, 1987; 153– 163 15. Folstein MF, Folstein SE, McHugh PR: “Mini-mental state.” A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189–198 16. Montgomery SA, Asberg M: A new depression scale designed to be sensitive to change. Br J Psychiatry 1979; 134:382–389 17. Schwartz JE, Jandorf L, Krupp LB: The measurement of fatigue: a new instrument. J Psychosom Res 1993; 37:753–762 18. Pedersen KF, Larsen JP, Aarsland D: Validation of the Unified Parkinson’s Disease Rating Scale (UPDRS) section I as a screening and diagnostic instrument for apathy in patients with Parkinson’s disease. Parkinsonism Relat Disord 2008; 14:183–186 19. Marin RS, Biedrzycki RC, Firinciogullari S: Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 1991; 38:143–162 20. Robinson RG: Apathy, in The Clinical Neuropsychiatry of Stroke: Cognitive, Behavioral and Emotional Disorders following Vascular Brain Injury. 2nd ed. Edited by Robinson RG. Cambridge: Cambridge University Press, 2006; 392–402 21. Tabachnick BG, Fidell LS: Principal Components and Factor Analysis, in Using Multivariate Statistics. 5th ed. Edited by Tabachnick BG, Fidell LS. Boston: Pearson Education, Inc./Allyn and Bacon, 2007, pp 607–675 22. Cohen JW: Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale, New Jersey: Lawrence Erlbaum Associates, 1988 23. Streiner DL, Norman GR: Health Measurement Scales: A Practical Guide To Their Development And Use. 3rd ed. Oxford: Oxford University Press, 2003 24. Marin RS, Firinciogullari S, Biedrzycki RC: The sources of convergence between measures of apathy and depression. J Affect Disord 1993; 28:117–124 25. Fava M: Pharmacological approaches to the treatment of residual symptoms. J Psychopharmacol 2006; 20:29–34 26. Cook DA, Beckman TJ: Current concepts in validity and reliability for psychometric instruments: theory and application. Am J Med 2006; 119:166: e167–e116
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Received October 8, 2010; revised May 23, 2011; accepted June 6, 2011. From the Norwegian Centre for Movement Disorders, Stavanger University Hospital, Stavanger, Norway (KFP, GA, JPL, SGM, KB); Department of Neurology, Stavanger University Hospital, Stavanger, Norway (KFP, GA, JPL); Department of Neurology, Haukeland University Hospital, Bergen, Norway (O-BT); and Centre of Organelle Research, Faculty of Science and Technology, University of Stavanger, Stavanger, Norway (SGM). Send correspondence and reprint requests to Dr. Kenn Freddy Pedersen, The Norwegian Centre for Movement Disorders, Stavanger University Hospital, PO Box 8100, N-4068 Stavanger, Norway. e-mail: [email protected] C 2012 American Association for Geriatric Psychiatry DOI: 10.1097/JGP.0b013e31823038f2
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A
pathy is a common behavioral problem in Parkinson disease (PD) and other neurodegenerative disorders across ethnically and culturally different populations.1–4 In a recent review of the psychometric properties of apathy rating scales,5 a Movement Disorder Society task force concluded that the Starkstein Apathy Scale (SAS) is the most appropriate psychometric tool for assessing apathy in PD patients. The SAS consists of 14 items (total score range 0–42; higher scores indicate more severe apathy) phrased as questions that are to be answered on a four-point Likert scale (intensity scores: not at all, slightly, some, a lot). In the first eight questions, the “not at all” answer corresponds to severe apathy; for question 9–14, the intensity scores are reversed, such that the “a lot” answer corresponds to more severe apathy. Using the original patient-based version, Starkstein and colleagues6 reported good face validity and internal consistency (Cronbach’s α = 0.76) in 50 PD patients, acceptable criterion validity (comparison to clinical impression as a gold standard yielded a sensitivity of 66% and a specificity of 100% when using a cut-off score of 13/14) in 12 PD patients, as well as good interrater (r = 0.81) and test-retest (r = 0.90) reliability in 11 PD patients.6 Clinimetric testing of the SAS has not been performed in larger PD cohorts, nor by others than the original developers, who did not assess the factor structure or itemtotal correlations. As apathy is one of the main psychiatric manifestations in untreated PD,7 and because dopaminergic drugs have the potential to influence the occurrence and severity of apathy in early PD,8 a large cohort of newly diagnosed patients with untreated PD from the Norwegian ParkWest study9 was recruited to examine the psychometric attributes of SAS. Although apathy is now considered as one single syndrome, recent consensus diagnostic criteria10 define apathy as a disorder of motivation characterized by symptoms in three different domains: behavioral, cognitive, and emotional. Therefore, we hypothesized that these three domains should be revealed as different factors in an exploratory factor analysis of the SAS. Reliability was assessed using Cronbach’s α and item-total correlations, whereas correlational analyses were conducted to investigate the discriminant validity of the SAS.
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SUBJECTS AND METHODS Study Design, Case Ascertainment, and Diagnostic Procedures The study is part of the Norwegian ParkWest project, a multicenter population-based prospective longitudinal cohort study of the incidence, neurobiology, and prognosis of PD in Western and Southern Norway. Findings obtained from the baseline evaluation of patients who were assessed between November 1, 2004, and August 31, 2006, were used for the present analysis. The study was approved by the Regional Committee for Medical Research Ethics at the University of Bergen and signed written informed consent was obtained from all subjects. A detailed description of the multiple case finding strategies and the diagnostic procedures is provided elsewhere.9 Briefly, we established a representative incident cohort of 212 unmedicated patients who fulfilled accepted diagnostic research criteria of idiopathic PD.11 To optimize diagnostic accuracy at this early stage, only patients whose diagnosis remained unchanged during follow-up, on average 28 months after inclusion, were included in the project. General exclusion criteria were cases with possible or probable dementia with Lewy bodies, Alzheimer disease, vascular parkinsonism, or atypical parkinsonian disorders including multiple system atrophy, corticobasal degeneration, and progressive supranuclear palsy.9 In the present study, we also excluded patients who met diagnostic criteria of PD-related dementia, on the basis of clinical history and examination, and comprehensive neuropsychological assessment, as previously described.12 Subjects Of the 212 subjects who agreed to take part in a longitudinal study follow-up and participated in standardized baseline examinations, 201 had never been exposed to antiparkinson drugs. In addition, seven patients fulfilled operationalized criteria for dementia,13 all with typical PD without a history of cognitive impairment during the first year after motor onset, leaving 194 patients eligible for inclusion in this study.
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Psychometric Properties of the Starkstein Apathy Scale Assessments Neurologists from the ParkWest study group performed standardized assessments, including a semistructured interview on demographic variables, medical history, and medication, in addition to general neurological and medical examinations. Severity of motor symptoms and disability was rated using the Unified Parkinson’s Disease Rating Scale, parts II and III.14 Global cognitive status was assessed with the Mini Mental State Exam15 and severity of depressive symptoms was determined using the Montgomery-Aasberg Depression Rating Scale.16 Fatigue severity was examined using the Fatigue Severity Scale.17 Apathy was measured using the selfreport version of SAS, which has previously been translated from the original English version6 into Norwegian by Aarsland.18 The SAS is an abridged and modified version of Marin’s Apathy Evaluation Scale19 and includes items concerning diminished motivation (items 7 and 12) as well as behavioral (items 4, 5, 8, and 9), cognitive (items 1, 2, 6, and 11), emotional (items 10 and 13), and insight (items 3 and 14) aspects of apathy.20 In the present study, back-translation was made by one of the authors (SGM) who is bilingual but did not know the original English text. A critical assessment of the backtranslation was made by four of the authors (KFP, GA, JPL, and KB) to ensure that the original and translated versions of SAS were acceptable equivalent. Clinical examination was performed blind to the SAS scores.
to retain was determined by a subsequent evaluation of the Kaiser’s criterion (eigenvalues >1), inspection of the screeplot (number of factors above the elbow, or break in the plot), and the clinical meaningfulness of the factor solutions. Reliability of the SAS was evaluated using Cronbach’s α coefficient (internal consistency) and corrected Pearson’s item-total correlations. Correlational analyses (Spearman’s r [rs ] for nonparametric data) were performed to investigate the relationship between individual items and the total score of SAS, the relationship between SAS total score and factor scores, and the discriminant validity of the SAS. Effect sizes for the correlation coefficients were defined by the following criteria: rs < 0.3, weak; rs = 0.3– 0.5, moderate; rs >0.5, strong.22 Mann-Whitney tests were used for comparisons of medians for continuous variables when appropriate. Statistics were performed using SPSS version 15.0 (SPSS, Inc., Chicago, IL). All tests were two-tailed, with p values <0.05 considered statistically significant.
RESULTS Demographic and clinical data for the PD patients are shown in Table 1, whereas the mean value (SD) of the items comprising the SAS and the Spearman’s correlation coefficients of each item with the total SAS score are presented in Table 2. Of notice, all items except item 3 (concerned about health problems) were significantly correlated with the total score (all rs ≥0.28, N = 194, p < 0.0005). The total SAS scores were
Statistical Analysis Before exploring the underlying structure of SAS using exploratory factor analysis, the data were assessed for its suitability for factor analysis. Inspection of the correlation matrix showed several coefficients > 0.3, the Bartlett’s test of sphericity was highly significant (p < 0.0005), and the Kaiser-Meyer-Olkin measure of sampling adequacy value was 0.76; all assessments supporting the factorability of the dataset.21 Principal component analysis was used to extract the factors followed by Varimax (orthogonal) rotation. We chose to use an orthogonal rotation because of the explorative design of this study and because the SAS items were hypothesized to be indicators of three different factors, which implies the factors to be uncorrelated. The number of factors
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TABLE 1. Demographic and Clinical Characteristics of Patients With Early Untreated PD (N = 194) Variable
Value
Age, years Education, years Male, n (%) Disease duration, years UPDRS ADL score UPDRS motor score MMSE score MADRS score Antidepressants, n (%)a Sedatives, n (%)a
67.9 (9.0) 11.0 (3.3) 115 (59.3) 2.3 (1.8) 8.8 (5.0) 23.2 (11.4) 27.8 (2.3) 4.5 (5.0) 27 (13.9) 22 (11.3)
Notes: Data are mean (SD) or number (% of assessed patients). ADL: activity of daily living; MMSE: Mini Mental State Exam; MADRS: Montgomery-Aasberg Depression Rating Scale; UPDRS: Unified Parkinson’s Disease Rating Scale. a Missing data for two patients (N = 192).
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Pedersen et al. strictly unimodal distributed with a mean score of 15.5 (SD 4.6), median 15.0, and range 4–29. Reliability The Cronbach’s α value for the 14-item SAS was 0.69. Analysis of the SAS items (corrected Pearson’s item-total correlations) indicated good and acceptable item characteristics (correlations >0.30, N = 194)23 for most of the items, see last column of Table 2. For items 8 (energy for daily activities), 9 (dependency on prompts to structure everyday activity), and 13 (neither happy nor sad), discriminatory power was small (correlations ≤ 0.20, N = 194). Noteworthy, item 3 showed a negative value of − 0.12, which indicates that subjects with low scores on this question get high scores on the total SAS score. After removing item 3 from the scale, the Cronbach’s α for the modified 13-item SAS was 0.74. Exploratory Factor Analysis Principal component analysis revealed four eigenvalues exceeding 1, accounting for 57.7% of the variance. From inspection of the screeplot, a two-factor model provided the best fit. The two-factor solution also gave the most clinically meaningful model, with the major factor accounting for 24.2% and the minor for 15.0% of the variance. Varimax rotation was then performed, and inspection of the rotated com-
TABLE 2.
ponent matrix (Table 3) showed a clear two factor solution, with both components showing a number of strong loadings. The correlation between the two factor scores was weak (rs = 0.19, N = 194, p = 0.008). Factor 1 included items representing cognitivebehavioral aspects of apathy (Cronbach’s α = 0.74, corrected item-total correlation range 0.23–0.66), whereas factor 2 represented a general apathy dimension including aspects of insight (Cronbach’s α = 0.52, corrected item-total correlation range − 0.18–0.48). As with the entire 14-item SAS, item 3 showed a negative corrected item-total correlation ( − 0.18) with factor 2. The correlation between the total score of SAS and the sum score of each factor was strong (rs = 0.82, N = 194, p < 0.0005 for factor 1; and rs = 0.67, N = 194, p < 0.0005 for factor 2). Because item 3 showed poor item-total correlation, we explored the structure of the SAS after removal of this item. Principal component analysis with Varimax rotation was repeated for the remaining 13 items, which confirmed the two-factor solution previously found for the original scale (except for item 3 removed), accounting for 41.7% of the variance. The Cronbach’s α value for factor 1 remained unchanged (0.74), but increased to 0.70 for the new factor 2 (corrected item-total correlations range 0.37–0.52). The correlation between the modified 13-item SAS total score and the sum score of each factor remained almost unaltered (rs = 0.83, N = 194, p < 0.0005 for factor 1; and rs = 0.63, N = 194, p < 0.0005 for factor 2), as
SAS Item Characteristics (N = 194)
Item
Mean (SD)
Correlation With Total SAS Scorea
Item—Total Correlationb
1. Are you interested in learning new things? 2. Does anything interest you? 3. Are you concerned about your condition? 4. Do you put much effort into things? 5. Are you always looking for something to do? 6. Do you have plans and goals for the future? 7. Do you have motivation? 8. Do you have the energy for daily activities? 9. Does someone have to tell you what to do each day? 10. Are you indifferent to things? 11. Are you unconcerned with many things? 12. Do you need a push to get started on things? 13. Are you neither happy nor sad, just in between? 14. Would you consider yourself apathetic?
1.46 (0.74) 0.92 (0.76) 1.62 (0.91) 1.45 (0.77) 1.64 (0.83) 1.67 (0.86) 1.43 (0.79) 1.35 (0.66) 0.19 (0.41) 0.53 (0.65) 0.98 (0.75) 0.85 (0.72) 1.21 (0.77) 0.21 (0.46)
0.57 0.49 0.08 0.44 0.43 0.66 0.72 0.27 0.28 0.49 0.42 0.52 0.34 0.42
0.44 0.36 − 0.12 0.28 0.31 0.57 0.63 0.16 0.19 0.37 0.29 0.41 0.20 0.35
SAS: Starkstein Apathy Scale. a Uncorrected Spearman correlation coefficient (nonparametric); all items p <0.0005, except item 3, which was not significant (N = 194, p = 0.271). b Corrected Pearson correlation coefficient.
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Psychometric Properties of the Starkstein Apathy Scale
TABLE 3.
Factor Analysis of the 14-Item SAS (Two-Factor Solution)
Item 6. Do you have plans and goals for the future? 7. Do you have motivation? 1. Are you interested in learning new things? 2. Does anything interest you? 4. Do you put much effort into things? 5. Are you always looking for something to do? 8. Do you have the energy for daily activities? 14. Would you consider yourself apathetic? 10. Are you indifferent to things? 13. Are you neither happy nor sad, just in between? 11. Are you unconcerned with many things? 9. Does someone have to tell you what to do each day? 12. Do you need a push to get started on things? 3. Are you concerned about your condition? Eigenvalue Variance explained by each factor (%) Internal consistency (Cronbach’s α)
Factor 1: CognitiveBehavioral Apathy
Factor 2: General Apathy
0.82
0.04
0.76
0.30
0.70
0.07
0.66
− 0.01
0.52
− 0.14
0.47
0.05
0.32
0.13
0.15
0.71
0.14
0.68
0.05
0.60
0.03
0.60
− 0.07
0.58
0.23
0.58
0.04
− 0.35
3.4 24.2
2.1 15.0
0.74
0.52a
SAS: Starkstein Apathy Scale. Notes: N = 194. Major loadings > 0.3 for each item are in bold. a Cronbach’s α after removal of item 3 from factor 2 was 0.70.
did the intercorrelation between the two factor scores (rs = 0.18, N = 194, p = 0.01). Discriminant Validity Table 4 presents the results of the correlational analyses examining the discriminant validity of the SAS. Both the total score and the two-factor model of the 14-item SAS showed weak to moderate correlations with the Montgomery-Aasberg Depression Rating Scale, Mini Mental State Exam, Unified Parkinson’s Disease Rating Scale motor, and Fatigue
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Severity Scale scores (rs ≤ 0.31, N = 194), which indicate fair discriminant validity of the self-report version of SAS. To explore whether the use of antidepressants or sedatives (11.3%–13.9% of the patients) could have influenced the results, bivariate analyses with type of medication as the dependent variable and total score and factor scores of the SAS as independent variables were performed. Patients using either antidepressants (n = 27) or sedatives (n = 22) scored significantly higher on the 14-item total score (range 0–42) (mean 17.0 [SD 4.8] versus 15.3 [4.5], Mann-Whitney z = − 1.97, N = 192, p = 0.049 for antidepressant therapy or not; mean 18.0 [SD 5.2] versus 15.2 [4.4], MannWhitney z = − 2.39, N = 192, p = 0.017 for use of sedatives or not) and factor 1 score (range 0–21) (mean 11.0 [SD 3.6] versus 9.7 [3.3], Mann-Whitney z = − 2.13, N = 192, p = 0.033 for antidepressant therapy or not; mean 12.4 [SD 3.8] versus 9.6 [3.2], Mann-Whitney z = − 3.38, N = 192, p = 0.001 for use of sedatives or not) than those without such medication. In contrast, no difference in factor 2 scores was found among patients using antidepressants or sedatives compared with unmedicated patients.
DISCUSSION The main purpose of this study was to explore the factor structure of the self-report version of SAS in a large cohort of newly diagnosed patients with drugna¨ıve PD. On the basis of recent consensus diagnostic criteria for apathy,10 we hypothesized that the behavioral, cognitive, and emotional domains of apathy should be revealed as different factors in the exploratory factor analysis of the SAS. This hypothesis was not supported by the data. Instead, we found that the 14 items of the SAS fell into two clinically distinct and relevant apathy factors. The low correlation between the factors and the strong correlation of each factor with the total score of SAS suggests that these factors not only capture unique aspects of PD-related apathy but also measure a single apathy construct. There was a fair level of internal consistency for the entire scale and the cognitive-behavioral apathy factor, whereas the internal consistency for the general apathy factor was inadequate. The Cronbach’s α for the SAS in our study was approximately similar to that reported by Starkstein and colleagues6 in their
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Pedersen et al.
TABLE 4.
Discriminant Validity of the 14-Item SAS and the Two-Factor Model
Variable MADRS score MMSE score UPDRS motor score FSS mean score
Total SAS Score
Cognitive-Behavioral Apathy Factor
General Apathy Factor
General Apathy Factor (Without Item 3)
0.25a − 0.17b 0.21a 0.14
0.24a − 0.24a 0.31c 0.17b
0.14b − 0.02 − 0.03 0.001
0.28c 0.01 − 0.01 0.13
Notes: SAS: Starkstein Apathy Scale; FSS: Fatigue Severity Scale; MADRS: Montgomery-Aasberg Depression Rating Scale; MMSE: Mini Mental State Exam; UPDRS: Unified Parkinson’s Disease Rating Scale; N = 194. a p < 0.005. b p < 0.05. c p < 0.0005.
original psychometric study of this scale, which included fewer patients with more advanced disease. Further reliability analysis revealed that the majority of SAS items showed good discriminant power, whereas three items (8, 9, and 13) had less adequate item characteristics. In addition, item 3 had a negative item-total correlation, indicating that patients who get low scores on this question (i.e., more concerned about their condition) get high scores on the total SAS score. Thus, this item proved to be highly ambiguous and therefore less suitable as a screening question for apathy in our PD sample. Indeed, removal of this item increased the internal consistency of the entire scale (modified 13-item SAS) and factor 2 subscale in particular. If replicated by others, a modified version of SAS with item 3 excluded might therefore be more appropriate to assess apathy in PD patients. The correlations between the total score and factor scores of SAS and standardized measurements of depression, cognitive impairment, parkinsonism, and fatigue were only weak to moderate (Table 4), indicating at least fair discriminant validity of the self-report version of SAS. In addition, the relationship between use of antidepressants or sedatives and the total score and factor scores of the SAS was explored. We found that these drugs were associated with higher total scores and cognitivebehavioral factor scores of the 14-item SAS. This finding was not unexpected, given the overlapping symptoms between apathy and depression,24 and the fact that apathy and anxiety are frequent residual symptoms among individuals treated for depressive disorder.25 We did not examine the criterion or convergent validity of SAS, which is a shortcoming of this study.
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Such data would have been valuable since high reliability of a rating scale not necessarily implies that it actually assess the construct of interest. At present, we are not aware of any studies reporting the convergent validity of SAS. However, Starkstein and colleagues6 reported acceptable criterion validity of the 14-item SAS using clinical impression as a gold standard for a diagnosis of apathy in patients with PD. Nevertheless, future studies should include structured interviews with patients and informants, using recently proposed consensus criteria for apathy as a guide,10 to investigate the validity of SAS in patients with PD. Although acceptable reliability and factor structure are important pieces of evidence for the internal structure of a clinical rating scale,26 this is to our knowledge the first study ever to examine the item-total correlation and factor structure of the SAS. Because the SAS is gaining popularity as a brief screening instrument for measurement of apathy in a variety of clinical populations,5 further studies exploring its factor structure in different populations are needed before one could make inferences based on the resultant scores. The findings here should be considered in the context of an exploratory factor analysis, which requires follow-up studies confirming whether the factor structure may be generalizable to patients with early PD using antiparkinsonian drug therapy, or to more advanced cases of PD. In summary, the results of this study support the use of the self-report version of SAS as a reliable and valid assessment instrument for measuring the severity of apathy symptoms, as well as distinct dimensions of apathy, in early untreated PD. However, because of the apparent ambiguity of item
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Psychometric Properties of the Starkstein Apathy Scale 3, this question may be considered removed from the scale to increase its internal consistency, especially when examining the different apathy dimensions of SAS revealed in this study. The two-factor model of SAS needs to be confirmed and future studies should attempt to clarify whether longitudinal changes in specific SAS domains rather than total scores would better predict the impact of apathy in patients with PD.
The authors are grateful to all patients for their willingness to participate in this study. We also thank all personnel who contributed to planning and conducting this study. The Norwegian ParkWest study was funded by the Western Norway Regional Health Authority (grant # 911218) and the Research Council of Norway (grant # 177966). The authors have no disclosures to report.
References 1. van Reekum R, Stuss DT, Ostrander L: Apathy: why care? J Neuropsychiatry Clin Neurosci 2005; 17:7–19 2. Aarsland D, Marsh L, Schrag A: Neuropsychiatric symptoms in Parkinson’s disease. Mov Disord 2009; 24:2175–2186 3. Tatsch MF, Bottino CM, Azevedo D, et al: Neuropsychiatric symptoms in Alzheimer disease and cognitively impaired, nondemented elderly from a community-based sample in Brazil: prevalence and relationship with dementia severity. Am J Geriatr Psychiatry 2006; 14:438–445 4. Chan WC, Lam LC, Tam CW, et al: Prevalence of neuropsychiatric symptoms in Chinese older persons with mild cognitive impairment-a population-based study. Am J Geriatr Psychiatry 18:948–954 5. Leentjens AF, Dujardin K, Marsh L, et al: Apathy and anhedonia rating scales in Parkinson’s disease: critique and recommendations. Mov Disord 2008; 23:2004–2014 6. Starkstein SE, Mayberg HS, Preziosi TJ, et al: Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 1992; 4:134–139 7. Aarsland D, Bronnick K, Alves G, et al: The spectrum of neuropsychiatric symptoms in patients with early untreated Parkinson’s disease. J Neurol Neurosurg Psychiatry 2009; 80:928–930 8. Bodi N, Keri S, Nagy H, et al: Reward-learning and the noveltyseeking personality: a between- and within-subjects study of the effects of dopamine agonists on young Parkinson’s patients. Brain 2009; 132:2385–2395 9. Alves G, Muller B, Herlofson K, et al: Incidence of Parkinson’s disease in Norway: the Norwegian ParkWest study. J Neurol Neurosurg Psychiatry 2009; 80:851–857 10. Robert P, Onyike CU, Leentjens AF, et al: Proposed diagnostic criteria for apathy in Alzheimer’s disease and other neuropsychiatric disorders. Eur Psychiatry 2009; 24:98–104 11. Gelb DJ, Oliver E, Gilman S: Diagnostic criteria for Parkinson disease. Arch Neurol 1999; 56:33–39 12. Aarsland D, Bronnick K, Larsen JP, et al: Cognitive impairment in incident, untreated Parkinson disease: the Norwegian ParkWest study. Neurology 2009; 72:1121–1126 13. Emre M, Aarsland D, Brown R, et al: Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 2007; 22:1689–1707
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14. Fahn S, Elton RL: Unified Parkinson’s Disease Rating Scale, in Recent Developments in Parkinson’s Disease. In: Fahn S, Marsden CD, Calne DB, Goldstein M. eds. Florham Park, New Jersey: Macmillan Healthcare Information, 1987; 153– 163 15. Folstein MF, Folstein SE, McHugh PR: “Mini-mental state.” A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189–198 16. Montgomery SA, Asberg M: A new depression scale designed to be sensitive to change. Br J Psychiatry 1979; 134:382–389 17. Schwartz JE, Jandorf L, Krupp LB: The measurement of fatigue: a new instrument. J Psychosom Res 1993; 37:753–762 18. Pedersen KF, Larsen JP, Aarsland D: Validation of the Unified Parkinson’s Disease Rating Scale (UPDRS) section I as a screening and diagnostic instrument for apathy in patients with Parkinson’s disease. Parkinsonism Relat Disord 2008; 14:183–186 19. Marin RS, Biedrzycki RC, Firinciogullari S: Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 1991; 38:143–162 20. Robinson RG: Apathy, in The Clinical Neuropsychiatry of Stroke: Cognitive, Behavioral and Emotional Disorders following Vascular Brain Injury. 2nd ed. Edited by Robinson RG. Cambridge: Cambridge University Press, 2006; 392–402 21. Tabachnick BG, Fidell LS: Principal Components and Factor Analysis, in Using Multivariate Statistics. 5th ed. Edited by Tabachnick BG, Fidell LS. Boston: Pearson Education, Inc./Allyn and Bacon, 2007, pp 607–675 22. Cohen JW: Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale, New Jersey: Lawrence Erlbaum Associates, 1988 23. Streiner DL, Norman GR: Health Measurement Scales: A Practical Guide To Their Development And Use. 3rd ed. Oxford: Oxford University Press, 2003 24. Marin RS, Firinciogullari S, Biedrzycki RC: The sources of convergence between measures of apathy and depression. J Affect Disord 1993; 28:117–124 25. Fava M: Pharmacological approaches to the treatment of residual symptoms. J Psychopharmacol 2006; 20:29–34 26. Cook DA, Beckman TJ: Current concepts in validity and reliability for psychometric instruments: theory and application. Am J Med 2006; 119:166: e167–e116
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