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Subjective Cognitive Complaints in Parkinson Disease Without Dementia: A Preliminary Study a
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Daniel P. Koster , Christopher I. Higginson , Elizabeth E. MacDougall , Vicki L. Wheelock & Karen A. Sigvardt a
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Department of Psychology, Loyola University Maryland, Baltimore, Maryland
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Department of Neurology, University of California-Davis Medical Center, Sacramento, California c
Center for Neuroscience, University of California, Davis, California Published online: 12 Dec 2014.
To cite this article: Daniel P. Koster, Christopher I. Higginson, Elizabeth E. MacDougall, Vicki L. Wheelock & Karen A. Sigvardt (2014): Subjective Cognitive Complaints in Parkinson Disease Without Dementia: A Preliminary Study, Applied Neuropsychology: Adult, DOI: 10.1080/23279095.2014.925902 To link to this article: http://dx.doi.org/10.1080/23279095.2014.925902
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APPLIED NEUROPSYCHOLOGY: ADULT, 0: 1–6, 2015 Copyright # Taylor & Francis Group, LLC ISSN: 2327-9095 print/2327-9109 online DOI: 10.1080/23279095.2014.925902
Subjective Cognitive Complaints in Parkinson Disease Without Dementia: A Preliminary Study Daniel P. Koster, Christopher I. Higginson, and Elizabeth E. MacDougall Department of Psychology, Loyola University Maryland, Baltimore, Maryland
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Vicki L. Wheelock Department of Neurology, University of California-Davis Medical Center, Sacramento, California
Karen A. Sigvardt Center for Neuroscience, University of California, Davis, California and Department of Neurology, University of California-Davis Medical Center, Sacramento, California
Little is known about the subjective cognitive complaints of individuals with Parkinson disease (PD). Such complaints have become a topic of interest recently as they play a role in the diagnosis of neurocognitive disorders. The aim of this preliminary study was to determine whether a sample of nondemented individuals with PD reported significantly more difficulties with multiple elements of cognition than a control sample and to assess the relation between their ratings and demographics, motor symptom severity, neuropsychological test performance, and measures of depression and anxiety. Forty nondemented individuals with PD and 27 healthy individuals completed a questionnaire assessing everyday cognitive difficulties. Independent t tests indicated that individuals with PD reported significantly more cognitive complaints in general and in specific tasks involving complex attention, executive function, processing speed, and verbal fluency but not memory. Questionnaire ratings significantly correlated with measures assessing anxiety, verbal memory, processing speed, and verbal fluency. Results suggest that it is important to ask individuals with PD about cognitive complaints across several cognitive domains and also inquire about symptoms of anxiety, which may be related to their self-reported cognitive difficulties.
Key words:
everyday functioning, mild cognitive impairment, Parkinson disease
Individuals with Parkinson disease (PD) perform worse than healthy controls on neuropsychological measures assessing complex attention, executive functions, memory, verbal fluency, and processing speed (Stennis Watson & Leverenz, 2010; Verbaan et al., 2007), but great variability in cognitive function exists among individuals with PD (Kehagia, Barker, & Robbins, 2010). The syndrome of mild cognitive Address correspondence to Christopher I. Higginson, Department of Psychology, Loyola University Maryland, 4501 North Charles Street, Baltimore, MD 21210-2699. E-mail: [email protected]
impairment (MCI) has been applied to PD in an attempt to more accurately characterize the large proportion of individuals with PD who do not experience the global cognitive decline and significant functional impairment indicative of dementia (Tröster, 2011). The presence of subjective cognitive complaints is an element of early conceptualizations of MCI (Petersen et al., 2001), proposed research criteria for MCI in PD (Tröster, 2011), and Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (American Psychiatric Association, 2013) neurocognitive disorders. However, it is not clear which particular cognitive complaints nondemented
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individuals with PD report more than healthy individuals or how these cognitive complaints relate to motor symptom severity, neuropsychological test performance, and the depression and anxiety commonly seen in individuals with PD (Aarsland, Påhlhagen, Ballard, Ehrt, & Svenningsson, 2012; Richard, Schiffer, & Kurlan, 1996). While some studies have considered the relation between cognitive ratings and depression in PD (Hirsch & Rohrle, 2011; Lanni et al., 2014; Poliakoff & Smith-Spark, 2008; Sitek, Sotan, Wieczorek, Robowski, & Sawek, 2011), this is the first study to consider the relation between cognitive ratings and anxiety in PD. The purpose of the current study was to investigate these issues. A better understanding of individuals’ cognitive complaints will assist clinicians in making appropriate referrals for neuropsychological assessment and assist neuropsychologists in accurately diagnosing cognitive deficits in PD. That is, knowing what cognitive difficulties to ask about should reduce the possibility that such difficulties will go undetected and may lead to earlier identification of cognitive impairment. METHODS Participants The sample consisted of 40 (12 female) individuals with idiopathic PD undergoing evaluation for functional neurosurgery and 27 (16 female) healthy adults (NC). Exclusion criteria for the NC group included chronic health problems, history of psychiatric diagnosis or treatment, grade repetition or special education services, and dementia diagnosis following neuropsychological assessment. Average age and education for the PD group were 60.68 years (SD ¼ 12.35) and 14.80 years (SD ¼ 2.90) respectively. Average age and education for the NC group were 59.88 years (SD ¼ 11.96) and 14.38 years (SD ¼ 2.45), respectively. The groups did not significantly differ in terms of age, t(65) ¼ 0.27, p ¼ .79, or education, t(65) ¼ 0.70, p ¼ .49; however, they were significantly different in terms of gender proportion, x2(1) ¼ 5.67, p ¼ .017. Individuals with PD were excluded if they met Diagnostic and Statistical Manual of Mental Disorders-Fourth Edition, Text Revision (American Psychiatric Association, 2000) criteria for dementia based on clinical judgment following neuropsychological evaluation. Average disease duration was 11.53 years (SD ¼ 7.02). The average Unified Parkinson Disease Rating Scale (UPDRS; Fahn, Elton, & UPDRS Development Committee, 1987) Motor score was 24.08 (SD ¼ 8.37) in the off state and 11.04 (SD ¼ 6.48) in the on state, while their medication was effectively treating their hypokinetic symptoms. Individuals with PD completed all measures in the on state. Materials and Procedure Following the provision of informed written consent, all participants completed a questionnaire assessing everyday
cognitive difficulties (see the Appendix) as well as the following measures: Minnesota Multiphasic Personality Inventory-Second Edition (MMPI-2; Butcher et al., 2001); the Symbol Search, Letter-Number Sequencing, and Matrix Reasoning subtests from the Wechsler Adult Intelligence Scale-Third Edition (WAIS-III; Wechsler, 1997a); Spatial Span from the Wechsler Memory Scale-Third Edition (Wechsler, 1997b); Stroop Neuropsychological Screening Test (Trenerry, Crosson, DeBoe, & Leber, 1989); California Verbal Learning Test-Second Edition (CVLT-II; Delis, Kramer, Kaplan, & Ober, 2000), letter fluency (FAS), and animal fluency. The questionnaire was developed to include daily tasks involving multiple areas of cognition that are commonly impacted by PD. Items were created with the goal of high face validity and were organized into groups based on clinical intuition after consideration of the neuropsychological profile associated with PD. We chose to develop our own cognitive questionnaire for this preliminary study because we were not able to identify a measure that was relatively short and also assessed multiple cognitive domains. The measure is composed of 27 items rated on a 4-point Likert scale ranging from 0 (no difficulty) to 3 (severe difficulty); therefore, scores can range from 0 to 81, with higher scores representing greater impairment. Multiple items assess executive functions (Items 6–8, 12, 15–18), complex attention (Items 1–5, 9, 10, 13, 14), and memory (Items 20– 27); individual items address processing speed (Item 11) and verbal fluency (Item 19). Total score and subscales had good internal consistency as indicated by the following values for Cronbach’s alpha: total score ¼ .96, executive functions ¼ .89, complex attention ¼ .90, and memory ¼ .90. To assess the validity of the responses from individuals with PD, the questionnaire was also completed by a significant other familiar with the daily functioning of the individuals with PD. Ratings by individuals with PD significantly correlated with ratings by significant others, r ¼ .75, p ¼ .01. To determine whether the PD group reported significantly more cognitive complaints than the NC group on the three subscales (i.e., Executive Functions, Complex Attention, and Memory) and two individual items (i.e., processing speed and verbal fluency), independent t tests were performed.
TABLE 1 Questionnaire Scores Control Mean
SD
Mean
SD
Cohen’s d
1.8 2.9 4.4 0.3 0.2 9.6
2.0 2.8 3.2 0.6 0.5 7.6
4.9 5.3 5.8 0.8 1.0 17.6
4.5 4.4 4.0 0.7 0.8 13.2
0.89 0.65 0.39 0.77 1.20 0.74
Executive Functions Complex Attention Memory Processing Speed Verbal Fluency Total Score
p < .05.
p < .01.
PD
p < .001.
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COGNITIVE COMPLAINTS IN PARKINSON DISEASE TABLE 2 Intercorrelation Matrix
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1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.
Questionnaire Total Age Education UPDRS Motor Score MMPI-2 Depression MMPI-2 Psychesthenia Symbol Search Letter-Number Sequencing Spatial Span Stroop Color-Word Matrix Reasoning CVLT-II Trials 1–5 CVLT-II LDFR Letter Fluency Animal Fluency
1
2
3
4
5
6
7
8
9
10
11
12
13
14
.06 .13 .20 .15 .71 .41 .03 .01 .06 .27 .46 .39 .33 .30
.09 .11 .35 .02 .47 .47 .33 .11 .40 .47 .36 .35 .36
.39 .44 .20 .03 .04 .18 .09 .12 .12 .24 .23 .12
.43 .13 .24 .22 0.14 .36 .21 .07 .05 .25 .12
.33 .20 .40 .24 .19 .29 .55 .41 .16 .02
.29 .07 .08 .38 .37 .10 .03 .27 .30
.64 .63 .25 .67 .70 .57 .76 .59
.62 .30 .60 .50 .52 .62 .43
.25 .59 .35 .43 .57 .54
.27 .09 .16 .23 .24
.46 .47 .52 .50
.85 .43 .46
.44 .44
.48
UPDRS ¼ Unified Parkinson Disease Rating Scale; MMPI-2 ¼ Minnesota Multiphasic Personality Inventory-2; CVLT-2 ¼ California Verbal Learning Test-Second Edition; LDFR ¼ Long-Delay Free Recall. p < .05. p < .01.
Pearson correlation coefficients were calculated to assess the degree of linear relationship between questionnaire ratings and demographic, motor, psychological, and neuropsychological variables. To reduce the number of analyses (and limit the potential for Type I error), select variables were chosen from tests that produce multiple scores. Scale 2 (Depression) and Scale 7 (Psychesthenia) were chosen from the MMPI-2, the color-word score was chosen from the Stroop Neuropsychological Screening Test, and total learning trials (1–5) and long-delay free recall were chosen from the CVLT-II. Alpha was set to .05 for all analyses. This study was approved by the applicable institutional review boards and was conducted in compliance with relevant laws and institutional guidelines.
RESULTS Table 1 lists the results of independent t tests comparing the PD and NC groups on the various questionnaire values. The PD group reported significantly higher scores (i.e., greater cognitive complaints) for executive functions, complex attention, processing speed, verbal fluency, and total score, but not for memory. Although the PD and NC groups were significantly different in terms of gender proportion, ratings were not significantly different in men versus women in either the PD or NC group, indicating that gender ratio could not account for any differences found between the PD and NC groups on the questionnaire. Table 2 provides an intercorrelation matrix. Questionnaire ratings were significantly correlated with the Psychesthenia scale from the MMPI-2, r ¼ .71, p < .001, performance on the CVLT-II learning trials (1–5), r ¼ .46, p ¼ .003, long-delay free recall, r ¼ .39, p ¼ .013, letter fluency (FAS), r ¼ .33, p ¼ .048, and WAIS-III Symbol Search, r ¼ .41, p ¼ .016.
The correlation between questionnaire ratings and animal fluency, r ¼ .30, p ¼ .07, was moderately large and approached significance.
DISCUSSION This sample of nondemented individuals with PD reported significantly more cognitive difficulties than a similar sample of healthy adults. The difficulties appear to involve tasks with executive, complex attention, processing speed, and verbal fluency components, many of the elements of cognition that have been implicated in PD. According to Cohen’s guidelines (1988), the size of the statistical effects were large for executive functions and verbal fluency and medium for complex attention and processing speed, indicating that the differences between the groups were substantial. Although it may not be surprising that individuals with a neurological disorder perceive cognitive difficulties in their daily life, it is surprising that individuals with PD did not report significantly more complaints with memory than healthy individuals because memory deficits are well known in PD (Stennis Watson & Leverenz, 2010; Verbaan et al., 2007) and memory problems are a common clinical complaint. The group means for the memory items indicate that the failure to find a significant difference between the groups is at least partially due to the endorsement of some memory difficulties in the control group, supporting the overall high prevalence of memory complaints. However, other explanations are possible. One is that the questionnaire did not adequately sample memory (i.e., a content validity issue). Perhaps the questions, which assessed the episodic element of long-term explicit=declarative memory as well as prospective memory, did not capture some of the
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memory types or processes that are associated with PD, such as implicit memory and memory retrieval (Stennis Watson & Leverenz, 2010). If we had included memory items on the questionnaire that involved visual stimuli, the PD sample might have reported greater memory complaints because neuropsychological measures of visual memory have shown significant correlations with performance of instrumental activities of daily living in PD (Uc et al., 2005). However, contrary to this explanation, the questionnaire significantly correlated with performance on neuropsychological measures of memory. A second explanation is a statistical one: The current study lacked the power to detect the small effect observed for the memory items. In any case, the finding, in conjunction with the large difference between the groups in terms of executive complaints, is consistent with other results suggesting a paramount role for executive dysfunction in PD (Bondi, Kaszniak, Bayles, & Vance, 1993; Higginson, Wheelock, Levine, Pappas, & Sigvardt, 2011; Taylor, Saint-Cyr, & Lang, 1990). It may simply be the case that memory complaints are not as common as complaints in other areas of cognition. We are not aware of any other studies that have reported this finding, and if accurate, it highlights the importance of inquiring about other elements of cognition in PD. The current results are fairly consistent with the few other studies of subjective cognitive complaints in PD. Individuals with PD have reported significantly more difficulties with memory and attention tasks (Hirsch & Rohrle, 2011; Poliakoff & Smith-Spark, 2008) and executive functions (Lanni et al., 2014). Individuals with PD also report experiencing more difficulty with self-cued prospective memory tasks than did the NC group (Foster, McDaniel, Repovs, & Hershey, 2009). Although we did not observe greater complaints with memory, only two of the memory items from the questionnaire involve prospective memory (Items 21 and 27). Therefore, this study contributes to the literature by simultaneously assessing a greater range of cognition than previous studies and by assessing complaints about areas of cognition that have not been previously addressed in PD—namely, processing speed and verbal fluency. Although the questionnaire used has not undergone extensive psychometric analysis, our preliminary results provide evidence of its reliability, by way of internal consistency estimates, and validity, by way of correlations with neuropsychological test performance. The total score on the questionnaire significantly correlated with performance on measures of processing speed, episodic memory, and verbal fluency, thereby providing evidence of convergent validity and supporting a role for these elements of cognition in the everyday cognitive activities of individuals with PD. On the other hand, the total score on the questionnaire did not correlate with performance on measures of working memory, visual attention, inhibition, and abstract reasoning, thereby providing evidence of discriminant validity, as a review of the items suggests that these elements of cognition do
not appear to be involved in the everyday tasks assessed by the questionnaire. Others have also reported a number of moderate correlations between cognitive ratings and neuropsychological tests in PD (Lanni et al., 2014; Poliakoff & Smith-Spark, 2008; Sitek et al., 2011). Although Poliakoff and Smith-Spark (2008) and Sitek et al. (2011) did not include measures of processing speed, Lanni et al. (2014) reported that such a measure contributed to the prediction of reported difficulties with executive function. This is consistent with the moderate correlation between Symbol Search performance and cognitive complaints found here. While some studies have reported a significant relation between cognitive ratings and symptoms of depression in PD (Hirsch & Rohrle, 2011; Lanni et al., 2014; Sitek et al., 2011), others have not (Poliakoff & Smith-Spark, 2008). The correlation between level of depression and cognitive ratings in the current study was small in size (r ¼ .15) and not statistically significant. In this regard, it is important to note that the indicator of depression used here, Scale 2 from the MMPI-2, is not commonly used as a measure of depression in empirical studies and may capture different variance in cognitive ratings. Nonetheless, Scale 2 has been shown to differentiate individuals with depressive spectrum illnesses as well as a more prototypical depression questionnaire (Lane, 2001) and has been used by others as an indicator of depression in a neurological patient sample (e.g., Gass, 1996). In contrast, the correlation between anxiety, as measured with Scale 7 from the MMPI-2, and cognitive ratings was large and statistically significant. In fact, this indicator of anxiety independently predicted 50% of the variance in cognitive ratings. Much like the concern regarding Scale 2 noted earlier, Scale 7 is not commonly used as an indicator of anxiety in empirical studies; however, it also has been used as such by others (e.g., Gass, 1996; Temple, Horner, & Taylor, 2004). Anxiety has received less attention than depression in the PD literature; nonetheless, a number of studies have shown increased anxiety in PD (Dissanayaka et al., 2010; Menza & Mark, 1994). Although Scale 7 did not significantly correlate with any of the neuropsychological measures, a number of the correlations were medium-sized effects that approached significance. Indeed, others have reported a relation between anxiety and cognition in PD (Hanna, 2006). To our knowledge, this is the first study to consider the relation between anxiety and cognitive ratings in PD, and our results suggest that this is an area worthy of additional attention. Although intriguing, the current results are subject to a number of limitations. First, as noted earlier, knowledge about the psychometric characteristics of the cognitive questionnaire is limited and based on a relatively small sample. Second, the results may not generalize beyond individuals with PD who are potential candidates for functional neurosurgery. This nature of the sample may explain why individuals did not report more cognitive difficulties after 11 years of illness; those who had obvious cognitive deficits may not have
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COGNITIVE COMPLAINTS IN PARKINSON DISEASE
been referred for presurgical evaluation. The exclusion of individuals with dementia would also contribute to the relatively few cognitive complaints reported. Also, individuals being considered for surgery will likely experience elevated symptoms of anxiety related to worry about being rejected for the procedure or undergoing the procedure itself. Such worry could also lead patients to underreport cognitive difficulties for fear that they would be rejected for surgery. In summary, this group of nondemented presurgical individuals with PD reported significantly more cognitive complaints than a group of healthy individuals. The complaints appear to involve executive functions, complex attention, processing speed, and verbal fluency, and they moderately correlate with performance on neuropsychological measures of processing speed, memory, and fluency. Most impressive was the novel and large correlation between cognitive ratings and level of anxiety. Regarding the clinical diagnosis of cognitive deficits in PD, these preliminary results highlight the importance of inquiring about multiple cognitive domains when evaluating cognitive complaints. The results also suggest that inquiry into symptoms of anxiety that may be related to complaints would be wise. FUNDING This work was supported by the National Institutes of Health (NS39121). REFERENCES Aarsland, D., Påhlhagen, S., Ballard, C. G., Ehrt, U., & Svenningsson, P. (2012). Depression in Parkinson disease—epidemiology, mechanisms and management. Nature Reviews: Neurology, 8, 35–47. doi: 10.1038= nrneurol.2011.189 American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington, DC: Author. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing. Bondi, M. W., Kaszniak, A. W., Bayles, K. A., & Vance, K. T. (1993). Contributions of frontal system dysfunction to memory and perceptual abilities in Parkinson’s disease. Neuropsychology, 7, 89–102. Butcher, J. N., Graham, J. R., Ben-Porath, Y. S., Tellegen, A., Dahlstrom, W. G., & Kraemmer, B. (2001). MMPI-2: Manual for administration, scoring, and interpretation (Rev. ed.). Minneapolis: University of Minnesota Press. Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum. Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). California Verbal Learning Test-Second Edition (CVLT-II). San Antonio, TX: Psychological Corporation. Dissanayaka, N. N., Sellbach, A., Matheson, S., O’Sullivan, J. D., Silburn, P. A., Byrne, G. J., & Mellick, G. D. (2010). Anxiety disorders in Parkinson’s disease: Prevalence and risk factors. Movement Disorders, 25, 838–845. doi: 10.1002=mds.22833 Fahn, S., Elton, R. L., & Unified Parkinson’s Disease Rating Scale Development Committee. (1987). Unified Parkinson’s Disease Rating Scale. In
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S. Fahn C. D. Marsden M. Goldstein & D. B. Calne (Eds.), Recent developments in Parkinson’s disease (Vol. 2, pp. 153–164). Florham Park, NJ: Macmillan Health Care Information. Foster, E. R., McDaniel, M. A., Repovs, G., & Hershey, T. (2009). Prospective memory in Parkinson disease across laboratory and self-reported everyday performance. Neuropsychology, 23, 347–358. doi: 10.1037=a0014692 Gass, C. S. (1996). MMPI-2 variables in attention and memory test performance. Psychological Assessment, 8, 135–138. Hanna, K. K. (2006). Anxiety, cognition and quality of life in Parkinson’s disease (Doctoral dissertation). Available from ProQuest Dissertations and Theses database. Retrieved from http://search.proquest.com/ docview/305364493?accountid=12164 (UMI No. 3214942) Higginson, C. I., Wheelock, V. L., Levine, D., Pappas, C. T. E., & Sigvardt, K. A. (2011). Predictors of HVOT performance in Parkinson’s disease. Applied Neuropsychology, 18, 210–215. doi: 10.1080= 09084282.2011.595447 Hirsch, O., & Rohrle, B. (2011). Association between self-assessed attention and objective neuropsychological tests in Parkinson disease. Cognitive and Behavioral Neurology, 24, 68–73. doi: 10.1097=WNN. 0b013e3182274e7a Kehagia, A. A., Barker, R. A., & Robbins, T. W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurology, 9, 1200–1213. doi: 10.1016=S1474-4422(10)70212-X Lane, D. W. (2001). An analysis of the MMPI-2 and SCL-90-R in the diagnosis of depressive illness (Doctoral dissertation). Available from ProQuest Dissertations and Theses database. (UMI No. 3013491) Lanni, K., Ross, J., Higginson, C. I., Dressler, E., Sigvardt, K. A., Zhang, L., . . . Disbrow, E. A. (2014). Perceived and performance-based executive dysfunction in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 36, 342–355. doi: 10.1080/13803395. 2014.892059 Menza, M. A., & Mark, M. H. (1994). Parkinson’s disease and depression: The relationship to disability and personality. Journal of Neuropsychiatry and Clinical Neurosciences, 6, 165–169. Petersen, R. C., Doody, R., Kurz, A., Mohs, R. C., Morris, J. C., Rabins, P. V., & Ritchie, K. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992. Poliakoff, E., & Smith-Spark, J. H. (2008). Everyday cognitive failures and memory problems in Parkinson’s patients without dementia. Brain and Cognition, 67, 340–350. doi: 10.1016=j.bandc.2008.02.004 Richard, I. H., Schiffer, R. B., & Kurlan, R. (1996). Anxiety and Parkinson’s disease. Journal of Neuropsychiatry and Clinical Neurosciences, 8, 383–392. Sitek, E. J., Sotan, W., Wieczorek, D., Robowski, P., & Sawek, J. (2011). Self-awareness of memory function in Parkinson’s disease in relation to mood and symptom severity. Aging & Mental Health, 15, 150–156. Stennis Watson, G., & Leverenz, J. B. (2010). Profile of cognitive impairment in Parkinson’s disease. Brain Pathology, 20, 640–645. doi: 10.1111=j.1750-3639.2010.00373.x Taylor, A. E., Saint-Cyr, J. A., & Lang, A. E. (1990). Memory and learning in early Parkinson’s disease: Evidence for a `frontal lobe syndrome.' Brain and Cognition, 13, 211–232. Temple, R. O., Horner, M. D., & Taylor, R. M. (2004). Relationship of MMPI-2 anxiety and defensiveness to neuropsychological test performance and psychotropic medication use. Cognition and Emotion, 18, 989–998. doi: 10.1080=02699930341000012 Trenerry, M. R., Crosson, B., DeBoe, J., & Leber, W. R. (1989). The Stroop Neuropsychological Screening Test. Lutz, FL: Psychological Assessment Resources. Tröster, A. I. (2011). A précis of recent advances in the neuropsychology of mild cognitive impairment(s) in Parkinson’s disease and a proposal of preliminary research criteria. Journal of the International Neuropsychological Society, 17, 393–406. doi: 10.1017=S1355 617711000257
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APPENDIX This questionnaire asks about problems that people sometimes have with their thinking. For each item, please circle the number that best describes you during the past 2 weeks. Try your best to answer questions without help from others. Use the following scale:
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0 ¼ no difficulty
1 ¼ mild difficulty
Do you have difficulty: 1) understanding conversations? 2) taking telephone messages? 3) following the plot in a TV show? 4) paying attention while reading or listening? 5) with losing your train of thought? 6) saving money? 7) organizing tax and insurance papers? 8) with changes in your daily routine? 9) finishing tasks? 10) switching from one task to another? 11) thinking quickly? 12) deciding what to do? 13) following verbal directions? 14) following written directions? 15) planning what order to do things in? 16) choosing the right clothes to wear? 17) making important decisions? 18) planning a big event (e.g., vacation)? 19) speaking quickly? Do you have difficulty remembering: 20) things that happened during the past few weeks? 21) appointments? 22) the names of people who you met during the past few months? 23) where you have placed things? 24) things that people have told you within the last few weeks? 25) things that you have told others within the last few weeks? 26) birthdays or anniversaries? 27) to take your medication?
2 ¼ moderate difficulty
3 ¼ severe difficulty
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2
3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3
0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1
2 2 2 2 2 2 2 2
3 3 3 3 3 3 3 3
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Subjective Cognitive Complaints in Parkinson Disease Without Dementia: A Preliminary Study a
a
a
b
Daniel P. Koster , Christopher I. Higginson , Elizabeth E. MacDougall , Vicki L. Wheelock & Karen A. Sigvardt a
bc
Department of Psychology, Loyola University Maryland, Baltimore, Maryland
b
Department of Neurology, University of California-Davis Medical Center, Sacramento, California c
Center for Neuroscience, University of California, Davis, California Published online: 12 Dec 2014.
To cite this article: Daniel P. Koster, Christopher I. Higginson, Elizabeth E. MacDougall, Vicki L. Wheelock & Karen A. Sigvardt (2014): Subjective Cognitive Complaints in Parkinson Disease Without Dementia: A Preliminary Study, Applied Neuropsychology: Adult, DOI: 10.1080/23279095.2014.925902 To link to this article: http://dx.doi.org/10.1080/23279095.2014.925902
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APPLIED NEUROPSYCHOLOGY: ADULT, 0: 1–6, 2015 Copyright # Taylor & Francis Group, LLC ISSN: 2327-9095 print/2327-9109 online DOI: 10.1080/23279095.2014.925902
Subjective Cognitive Complaints in Parkinson Disease Without Dementia: A Preliminary Study Daniel P. Koster, Christopher I. Higginson, and Elizabeth E. MacDougall Department of Psychology, Loyola University Maryland, Baltimore, Maryland
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Vicki L. Wheelock Department of Neurology, University of California-Davis Medical Center, Sacramento, California
Karen A. Sigvardt Center for Neuroscience, University of California, Davis, California and Department of Neurology, University of California-Davis Medical Center, Sacramento, California
Little is known about the subjective cognitive complaints of individuals with Parkinson disease (PD). Such complaints have become a topic of interest recently as they play a role in the diagnosis of neurocognitive disorders. The aim of this preliminary study was to determine whether a sample of nondemented individuals with PD reported significantly more difficulties with multiple elements of cognition than a control sample and to assess the relation between their ratings and demographics, motor symptom severity, neuropsychological test performance, and measures of depression and anxiety. Forty nondemented individuals with PD and 27 healthy individuals completed a questionnaire assessing everyday cognitive difficulties. Independent t tests indicated that individuals with PD reported significantly more cognitive complaints in general and in specific tasks involving complex attention, executive function, processing speed, and verbal fluency but not memory. Questionnaire ratings significantly correlated with measures assessing anxiety, verbal memory, processing speed, and verbal fluency. Results suggest that it is important to ask individuals with PD about cognitive complaints across several cognitive domains and also inquire about symptoms of anxiety, which may be related to their self-reported cognitive difficulties.
Key words:
everyday functioning, mild cognitive impairment, Parkinson disease
Individuals with Parkinson disease (PD) perform worse than healthy controls on neuropsychological measures assessing complex attention, executive functions, memory, verbal fluency, and processing speed (Stennis Watson & Leverenz, 2010; Verbaan et al., 2007), but great variability in cognitive function exists among individuals with PD (Kehagia, Barker, & Robbins, 2010). The syndrome of mild cognitive Address correspondence to Christopher I. Higginson, Department of Psychology, Loyola University Maryland, 4501 North Charles Street, Baltimore, MD 21210-2699. E-mail: [email protected]
impairment (MCI) has been applied to PD in an attempt to more accurately characterize the large proportion of individuals with PD who do not experience the global cognitive decline and significant functional impairment indicative of dementia (Tröster, 2011). The presence of subjective cognitive complaints is an element of early conceptualizations of MCI (Petersen et al., 2001), proposed research criteria for MCI in PD (Tröster, 2011), and Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (American Psychiatric Association, 2013) neurocognitive disorders. However, it is not clear which particular cognitive complaints nondemented
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individuals with PD report more than healthy individuals or how these cognitive complaints relate to motor symptom severity, neuropsychological test performance, and the depression and anxiety commonly seen in individuals with PD (Aarsland, Påhlhagen, Ballard, Ehrt, & Svenningsson, 2012; Richard, Schiffer, & Kurlan, 1996). While some studies have considered the relation between cognitive ratings and depression in PD (Hirsch & Rohrle, 2011; Lanni et al., 2014; Poliakoff & Smith-Spark, 2008; Sitek, Sotan, Wieczorek, Robowski, & Sawek, 2011), this is the first study to consider the relation between cognitive ratings and anxiety in PD. The purpose of the current study was to investigate these issues. A better understanding of individuals’ cognitive complaints will assist clinicians in making appropriate referrals for neuropsychological assessment and assist neuropsychologists in accurately diagnosing cognitive deficits in PD. That is, knowing what cognitive difficulties to ask about should reduce the possibility that such difficulties will go undetected and may lead to earlier identification of cognitive impairment. METHODS Participants The sample consisted of 40 (12 female) individuals with idiopathic PD undergoing evaluation for functional neurosurgery and 27 (16 female) healthy adults (NC). Exclusion criteria for the NC group included chronic health problems, history of psychiatric diagnosis or treatment, grade repetition or special education services, and dementia diagnosis following neuropsychological assessment. Average age and education for the PD group were 60.68 years (SD ¼ 12.35) and 14.80 years (SD ¼ 2.90) respectively. Average age and education for the NC group were 59.88 years (SD ¼ 11.96) and 14.38 years (SD ¼ 2.45), respectively. The groups did not significantly differ in terms of age, t(65) ¼ 0.27, p ¼ .79, or education, t(65) ¼ 0.70, p ¼ .49; however, they were significantly different in terms of gender proportion, x2(1) ¼ 5.67, p ¼ .017. Individuals with PD were excluded if they met Diagnostic and Statistical Manual of Mental Disorders-Fourth Edition, Text Revision (American Psychiatric Association, 2000) criteria for dementia based on clinical judgment following neuropsychological evaluation. Average disease duration was 11.53 years (SD ¼ 7.02). The average Unified Parkinson Disease Rating Scale (UPDRS; Fahn, Elton, & UPDRS Development Committee, 1987) Motor score was 24.08 (SD ¼ 8.37) in the off state and 11.04 (SD ¼ 6.48) in the on state, while their medication was effectively treating their hypokinetic symptoms. Individuals with PD completed all measures in the on state. Materials and Procedure Following the provision of informed written consent, all participants completed a questionnaire assessing everyday
cognitive difficulties (see the Appendix) as well as the following measures: Minnesota Multiphasic Personality Inventory-Second Edition (MMPI-2; Butcher et al., 2001); the Symbol Search, Letter-Number Sequencing, and Matrix Reasoning subtests from the Wechsler Adult Intelligence Scale-Third Edition (WAIS-III; Wechsler, 1997a); Spatial Span from the Wechsler Memory Scale-Third Edition (Wechsler, 1997b); Stroop Neuropsychological Screening Test (Trenerry, Crosson, DeBoe, & Leber, 1989); California Verbal Learning Test-Second Edition (CVLT-II; Delis, Kramer, Kaplan, & Ober, 2000), letter fluency (FAS), and animal fluency. The questionnaire was developed to include daily tasks involving multiple areas of cognition that are commonly impacted by PD. Items were created with the goal of high face validity and were organized into groups based on clinical intuition after consideration of the neuropsychological profile associated with PD. We chose to develop our own cognitive questionnaire for this preliminary study because we were not able to identify a measure that was relatively short and also assessed multiple cognitive domains. The measure is composed of 27 items rated on a 4-point Likert scale ranging from 0 (no difficulty) to 3 (severe difficulty); therefore, scores can range from 0 to 81, with higher scores representing greater impairment. Multiple items assess executive functions (Items 6–8, 12, 15–18), complex attention (Items 1–5, 9, 10, 13, 14), and memory (Items 20– 27); individual items address processing speed (Item 11) and verbal fluency (Item 19). Total score and subscales had good internal consistency as indicated by the following values for Cronbach’s alpha: total score ¼ .96, executive functions ¼ .89, complex attention ¼ .90, and memory ¼ .90. To assess the validity of the responses from individuals with PD, the questionnaire was also completed by a significant other familiar with the daily functioning of the individuals with PD. Ratings by individuals with PD significantly correlated with ratings by significant others, r ¼ .75, p ¼ .01. To determine whether the PD group reported significantly more cognitive complaints than the NC group on the three subscales (i.e., Executive Functions, Complex Attention, and Memory) and two individual items (i.e., processing speed and verbal fluency), independent t tests were performed.
TABLE 1 Questionnaire Scores Control Mean
SD
Mean
SD
Cohen’s d
1.8 2.9 4.4 0.3 0.2 9.6
2.0 2.8 3.2 0.6 0.5 7.6
4.9 5.3 5.8 0.8 1.0 17.6
4.5 4.4 4.0 0.7 0.8 13.2
0.89 0.65 0.39 0.77 1.20 0.74
Executive Functions Complex Attention Memory Processing Speed Verbal Fluency Total Score
p < .05.
p < .01.
PD
p < .001.
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COGNITIVE COMPLAINTS IN PARKINSON DISEASE TABLE 2 Intercorrelation Matrix
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1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.
Questionnaire Total Age Education UPDRS Motor Score MMPI-2 Depression MMPI-2 Psychesthenia Symbol Search Letter-Number Sequencing Spatial Span Stroop Color-Word Matrix Reasoning CVLT-II Trials 1–5 CVLT-II LDFR Letter Fluency Animal Fluency
1
2
3
4
5
6
7
8
9
10
11
12
13
14
.06 .13 .20 .15 .71 .41 .03 .01 .06 .27 .46 .39 .33 .30
.09 .11 .35 .02 .47 .47 .33 .11 .40 .47 .36 .35 .36
.39 .44 .20 .03 .04 .18 .09 .12 .12 .24 .23 .12
.43 .13 .24 .22 0.14 .36 .21 .07 .05 .25 .12
.33 .20 .40 .24 .19 .29 .55 .41 .16 .02
.29 .07 .08 .38 .37 .10 .03 .27 .30
.64 .63 .25 .67 .70 .57 .76 .59
.62 .30 .60 .50 .52 .62 .43
.25 .59 .35 .43 .57 .54
.27 .09 .16 .23 .24
.46 .47 .52 .50
.85 .43 .46
.44 .44
.48
UPDRS ¼ Unified Parkinson Disease Rating Scale; MMPI-2 ¼ Minnesota Multiphasic Personality Inventory-2; CVLT-2 ¼ California Verbal Learning Test-Second Edition; LDFR ¼ Long-Delay Free Recall. p < .05. p < .01.
Pearson correlation coefficients were calculated to assess the degree of linear relationship between questionnaire ratings and demographic, motor, psychological, and neuropsychological variables. To reduce the number of analyses (and limit the potential for Type I error), select variables were chosen from tests that produce multiple scores. Scale 2 (Depression) and Scale 7 (Psychesthenia) were chosen from the MMPI-2, the color-word score was chosen from the Stroop Neuropsychological Screening Test, and total learning trials (1–5) and long-delay free recall were chosen from the CVLT-II. Alpha was set to .05 for all analyses. This study was approved by the applicable institutional review boards and was conducted in compliance with relevant laws and institutional guidelines.
RESULTS Table 1 lists the results of independent t tests comparing the PD and NC groups on the various questionnaire values. The PD group reported significantly higher scores (i.e., greater cognitive complaints) for executive functions, complex attention, processing speed, verbal fluency, and total score, but not for memory. Although the PD and NC groups were significantly different in terms of gender proportion, ratings were not significantly different in men versus women in either the PD or NC group, indicating that gender ratio could not account for any differences found between the PD and NC groups on the questionnaire. Table 2 provides an intercorrelation matrix. Questionnaire ratings were significantly correlated with the Psychesthenia scale from the MMPI-2, r ¼ .71, p < .001, performance on the CVLT-II learning trials (1–5), r ¼ .46, p ¼ .003, long-delay free recall, r ¼ .39, p ¼ .013, letter fluency (FAS), r ¼ .33, p ¼ .048, and WAIS-III Symbol Search, r ¼ .41, p ¼ .016.
The correlation between questionnaire ratings and animal fluency, r ¼ .30, p ¼ .07, was moderately large and approached significance.
DISCUSSION This sample of nondemented individuals with PD reported significantly more cognitive difficulties than a similar sample of healthy adults. The difficulties appear to involve tasks with executive, complex attention, processing speed, and verbal fluency components, many of the elements of cognition that have been implicated in PD. According to Cohen’s guidelines (1988), the size of the statistical effects were large for executive functions and verbal fluency and medium for complex attention and processing speed, indicating that the differences between the groups were substantial. Although it may not be surprising that individuals with a neurological disorder perceive cognitive difficulties in their daily life, it is surprising that individuals with PD did not report significantly more complaints with memory than healthy individuals because memory deficits are well known in PD (Stennis Watson & Leverenz, 2010; Verbaan et al., 2007) and memory problems are a common clinical complaint. The group means for the memory items indicate that the failure to find a significant difference between the groups is at least partially due to the endorsement of some memory difficulties in the control group, supporting the overall high prevalence of memory complaints. However, other explanations are possible. One is that the questionnaire did not adequately sample memory (i.e., a content validity issue). Perhaps the questions, which assessed the episodic element of long-term explicit=declarative memory as well as prospective memory, did not capture some of the
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memory types or processes that are associated with PD, such as implicit memory and memory retrieval (Stennis Watson & Leverenz, 2010). If we had included memory items on the questionnaire that involved visual stimuli, the PD sample might have reported greater memory complaints because neuropsychological measures of visual memory have shown significant correlations with performance of instrumental activities of daily living in PD (Uc et al., 2005). However, contrary to this explanation, the questionnaire significantly correlated with performance on neuropsychological measures of memory. A second explanation is a statistical one: The current study lacked the power to detect the small effect observed for the memory items. In any case, the finding, in conjunction with the large difference between the groups in terms of executive complaints, is consistent with other results suggesting a paramount role for executive dysfunction in PD (Bondi, Kaszniak, Bayles, & Vance, 1993; Higginson, Wheelock, Levine, Pappas, & Sigvardt, 2011; Taylor, Saint-Cyr, & Lang, 1990). It may simply be the case that memory complaints are not as common as complaints in other areas of cognition. We are not aware of any other studies that have reported this finding, and if accurate, it highlights the importance of inquiring about other elements of cognition in PD. The current results are fairly consistent with the few other studies of subjective cognitive complaints in PD. Individuals with PD have reported significantly more difficulties with memory and attention tasks (Hirsch & Rohrle, 2011; Poliakoff & Smith-Spark, 2008) and executive functions (Lanni et al., 2014). Individuals with PD also report experiencing more difficulty with self-cued prospective memory tasks than did the NC group (Foster, McDaniel, Repovs, & Hershey, 2009). Although we did not observe greater complaints with memory, only two of the memory items from the questionnaire involve prospective memory (Items 21 and 27). Therefore, this study contributes to the literature by simultaneously assessing a greater range of cognition than previous studies and by assessing complaints about areas of cognition that have not been previously addressed in PD—namely, processing speed and verbal fluency. Although the questionnaire used has not undergone extensive psychometric analysis, our preliminary results provide evidence of its reliability, by way of internal consistency estimates, and validity, by way of correlations with neuropsychological test performance. The total score on the questionnaire significantly correlated with performance on measures of processing speed, episodic memory, and verbal fluency, thereby providing evidence of convergent validity and supporting a role for these elements of cognition in the everyday cognitive activities of individuals with PD. On the other hand, the total score on the questionnaire did not correlate with performance on measures of working memory, visual attention, inhibition, and abstract reasoning, thereby providing evidence of discriminant validity, as a review of the items suggests that these elements of cognition do
not appear to be involved in the everyday tasks assessed by the questionnaire. Others have also reported a number of moderate correlations between cognitive ratings and neuropsychological tests in PD (Lanni et al., 2014; Poliakoff & Smith-Spark, 2008; Sitek et al., 2011). Although Poliakoff and Smith-Spark (2008) and Sitek et al. (2011) did not include measures of processing speed, Lanni et al. (2014) reported that such a measure contributed to the prediction of reported difficulties with executive function. This is consistent with the moderate correlation between Symbol Search performance and cognitive complaints found here. While some studies have reported a significant relation between cognitive ratings and symptoms of depression in PD (Hirsch & Rohrle, 2011; Lanni et al., 2014; Sitek et al., 2011), others have not (Poliakoff & Smith-Spark, 2008). The correlation between level of depression and cognitive ratings in the current study was small in size (r ¼ .15) and not statistically significant. In this regard, it is important to note that the indicator of depression used here, Scale 2 from the MMPI-2, is not commonly used as a measure of depression in empirical studies and may capture different variance in cognitive ratings. Nonetheless, Scale 2 has been shown to differentiate individuals with depressive spectrum illnesses as well as a more prototypical depression questionnaire (Lane, 2001) and has been used by others as an indicator of depression in a neurological patient sample (e.g., Gass, 1996). In contrast, the correlation between anxiety, as measured with Scale 7 from the MMPI-2, and cognitive ratings was large and statistically significant. In fact, this indicator of anxiety independently predicted 50% of the variance in cognitive ratings. Much like the concern regarding Scale 2 noted earlier, Scale 7 is not commonly used as an indicator of anxiety in empirical studies; however, it also has been used as such by others (e.g., Gass, 1996; Temple, Horner, & Taylor, 2004). Anxiety has received less attention than depression in the PD literature; nonetheless, a number of studies have shown increased anxiety in PD (Dissanayaka et al., 2010; Menza & Mark, 1994). Although Scale 7 did not significantly correlate with any of the neuropsychological measures, a number of the correlations were medium-sized effects that approached significance. Indeed, others have reported a relation between anxiety and cognition in PD (Hanna, 2006). To our knowledge, this is the first study to consider the relation between anxiety and cognitive ratings in PD, and our results suggest that this is an area worthy of additional attention. Although intriguing, the current results are subject to a number of limitations. First, as noted earlier, knowledge about the psychometric characteristics of the cognitive questionnaire is limited and based on a relatively small sample. Second, the results may not generalize beyond individuals with PD who are potential candidates for functional neurosurgery. This nature of the sample may explain why individuals did not report more cognitive difficulties after 11 years of illness; those who had obvious cognitive deficits may not have
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COGNITIVE COMPLAINTS IN PARKINSON DISEASE
been referred for presurgical evaluation. The exclusion of individuals with dementia would also contribute to the relatively few cognitive complaints reported. Also, individuals being considered for surgery will likely experience elevated symptoms of anxiety related to worry about being rejected for the procedure or undergoing the procedure itself. Such worry could also lead patients to underreport cognitive difficulties for fear that they would be rejected for surgery. In summary, this group of nondemented presurgical individuals with PD reported significantly more cognitive complaints than a group of healthy individuals. The complaints appear to involve executive functions, complex attention, processing speed, and verbal fluency, and they moderately correlate with performance on neuropsychological measures of processing speed, memory, and fluency. Most impressive was the novel and large correlation between cognitive ratings and level of anxiety. Regarding the clinical diagnosis of cognitive deficits in PD, these preliminary results highlight the importance of inquiring about multiple cognitive domains when evaluating cognitive complaints. The results also suggest that inquiry into symptoms of anxiety that may be related to complaints would be wise. FUNDING This work was supported by the National Institutes of Health (NS39121). REFERENCES Aarsland, D., Påhlhagen, S., Ballard, C. G., Ehrt, U., & Svenningsson, P. (2012). Depression in Parkinson disease—epidemiology, mechanisms and management. Nature Reviews: Neurology, 8, 35–47. doi: 10.1038= nrneurol.2011.189 American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington, DC: Author. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing. Bondi, M. W., Kaszniak, A. W., Bayles, K. A., & Vance, K. T. (1993). Contributions of frontal system dysfunction to memory and perceptual abilities in Parkinson’s disease. Neuropsychology, 7, 89–102. Butcher, J. N., Graham, J. R., Ben-Porath, Y. S., Tellegen, A., Dahlstrom, W. G., & Kraemmer, B. (2001). MMPI-2: Manual for administration, scoring, and interpretation (Rev. ed.). Minneapolis: University of Minnesota Press. Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum. Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). California Verbal Learning Test-Second Edition (CVLT-II). San Antonio, TX: Psychological Corporation. Dissanayaka, N. N., Sellbach, A., Matheson, S., O’Sullivan, J. D., Silburn, P. A., Byrne, G. J., & Mellick, G. D. (2010). Anxiety disorders in Parkinson’s disease: Prevalence and risk factors. Movement Disorders, 25, 838–845. doi: 10.1002=mds.22833 Fahn, S., Elton, R. L., & Unified Parkinson’s Disease Rating Scale Development Committee. (1987). Unified Parkinson’s Disease Rating Scale. In
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S. Fahn C. D. Marsden M. Goldstein & D. B. Calne (Eds.), Recent developments in Parkinson’s disease (Vol. 2, pp. 153–164). Florham Park, NJ: Macmillan Health Care Information. Foster, E. R., McDaniel, M. A., Repovs, G., & Hershey, T. (2009). Prospective memory in Parkinson disease across laboratory and self-reported everyday performance. Neuropsychology, 23, 347–358. doi: 10.1037=a0014692 Gass, C. S. (1996). MMPI-2 variables in attention and memory test performance. Psychological Assessment, 8, 135–138. Hanna, K. K. (2006). Anxiety, cognition and quality of life in Parkinson’s disease (Doctoral dissertation). Available from ProQuest Dissertations and Theses database. Retrieved from http://search.proquest.com/ docview/305364493?accountid=12164 (UMI No. 3214942) Higginson, C. I., Wheelock, V. L., Levine, D., Pappas, C. T. E., & Sigvardt, K. A. (2011). Predictors of HVOT performance in Parkinson’s disease. Applied Neuropsychology, 18, 210–215. doi: 10.1080= 09084282.2011.595447 Hirsch, O., & Rohrle, B. (2011). Association between self-assessed attention and objective neuropsychological tests in Parkinson disease. Cognitive and Behavioral Neurology, 24, 68–73. doi: 10.1097=WNN. 0b013e3182274e7a Kehagia, A. A., Barker, R. A., & Robbins, T. W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurology, 9, 1200–1213. doi: 10.1016=S1474-4422(10)70212-X Lane, D. W. (2001). An analysis of the MMPI-2 and SCL-90-R in the diagnosis of depressive illness (Doctoral dissertation). Available from ProQuest Dissertations and Theses database. (UMI No. 3013491) Lanni, K., Ross, J., Higginson, C. I., Dressler, E., Sigvardt, K. A., Zhang, L., . . . Disbrow, E. A. (2014). Perceived and performance-based executive dysfunction in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 36, 342–355. doi: 10.1080/13803395. 2014.892059 Menza, M. A., & Mark, M. H. (1994). Parkinson’s disease and depression: The relationship to disability and personality. Journal of Neuropsychiatry and Clinical Neurosciences, 6, 165–169. Petersen, R. C., Doody, R., Kurz, A., Mohs, R. C., Morris, J. C., Rabins, P. V., & Ritchie, K. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992. Poliakoff, E., & Smith-Spark, J. H. (2008). Everyday cognitive failures and memory problems in Parkinson’s patients without dementia. Brain and Cognition, 67, 340–350. doi: 10.1016=j.bandc.2008.02.004 Richard, I. H., Schiffer, R. B., & Kurlan, R. (1996). Anxiety and Parkinson’s disease. Journal of Neuropsychiatry and Clinical Neurosciences, 8, 383–392. Sitek, E. J., Sotan, W., Wieczorek, D., Robowski, P., & Sawek, J. (2011). Self-awareness of memory function in Parkinson’s disease in relation to mood and symptom severity. Aging & Mental Health, 15, 150–156. Stennis Watson, G., & Leverenz, J. B. (2010). Profile of cognitive impairment in Parkinson’s disease. Brain Pathology, 20, 640–645. doi: 10.1111=j.1750-3639.2010.00373.x Taylor, A. E., Saint-Cyr, J. A., & Lang, A. E. (1990). Memory and learning in early Parkinson’s disease: Evidence for a `frontal lobe syndrome.' Brain and Cognition, 13, 211–232. Temple, R. O., Horner, M. D., & Taylor, R. M. (2004). Relationship of MMPI-2 anxiety and defensiveness to neuropsychological test performance and psychotropic medication use. Cognition and Emotion, 18, 989–998. doi: 10.1080=02699930341000012 Trenerry, M. R., Crosson, B., DeBoe, J., & Leber, W. R. (1989). The Stroop Neuropsychological Screening Test. Lutz, FL: Psychological Assessment Resources. Tröster, A. I. (2011). A précis of recent advances in the neuropsychology of mild cognitive impairment(s) in Parkinson’s disease and a proposal of preliminary research criteria. Journal of the International Neuropsychological Society, 17, 393–406. doi: 10.1017=S1355 617711000257
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APPENDIX This questionnaire asks about problems that people sometimes have with their thinking. For each item, please circle the number that best describes you during the past 2 weeks. Try your best to answer questions without help from others. Use the following scale:
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0 ¼ no difficulty
1 ¼ mild difficulty
Do you have difficulty: 1) understanding conversations? 2) taking telephone messages? 3) following the plot in a TV show? 4) paying attention while reading or listening? 5) with losing your train of thought? 6) saving money? 7) organizing tax and insurance papers? 8) with changes in your daily routine? 9) finishing tasks? 10) switching from one task to another? 11) thinking quickly? 12) deciding what to do? 13) following verbal directions? 14) following written directions? 15) planning what order to do things in? 16) choosing the right clothes to wear? 17) making important decisions? 18) planning a big event (e.g., vacation)? 19) speaking quickly? Do you have difficulty remembering: 20) things that happened during the past few weeks? 21) appointments? 22) the names of people who you met during the past few months? 23) where you have placed things? 24) things that people have told you within the last few weeks? 25) things that you have told others within the last few weeks? 26) birthdays or anniversaries? 27) to take your medication?
2 ¼ moderate difficulty
3 ¼ severe difficulty
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2
3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3
0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1
2 2 2 2 2 2 2 2
3 3 3 3 3 3 3 3
