Journal of Geriatric Psychiatry and Neurology http://jgp.sagepub.com/

Do Subjective Memory Complaints Herald the Onset of Mild Cognitive Impairment in Parkinson Disease? Roberto Erro, Gabriella Santangelo, Paolo Barone, Marina Picillo, Marianna Amboni, Katia Longo, Flavio Giordano, Marcello Moccia, Roberto Allocca, Maria Teresa Pellecchia and Carmine Vitale J Geriatr Psychiatry Neurol published online 30 April 2014 DOI: 10.1177/0891988714532015 The online version of this article can be found at: http://jgp.sagepub.com/content/early/2014/04/29/0891988714532015

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Research Investigation

Do Subjective Memory Complaints Herald the Onset of Mild Cognitive Impairment in Parkinson Disease?

Journal of Geriatric Psychiatry and Neurology 1-6 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0891988714532015 jgpn.sagepub.com

Roberto Erro, MD1, Gabriella Santangelo, PhD2,3, Paolo Barone, PhD4, Marina Picillo, MD5, Marianna Amboni, PhD3, Katia Longo, PhD3, Flavio Giordano, MD4, Marcello Moccia, MD5, Roberto Allocca, MD5, Maria Teresa Pellecchia, PhD4, and Carmine Vitale, PhD3,6

Abstract Background: Longitudinal studies on healthy participants have shown that subjective memory impairment (defined as subjective cognitive complaints with normal cognitive objective performance) might be a strong predictor of mild cognitive impairment (MCI). Parkinson disease (PD) also manifests cognitive disturbances, but whether subjective memory complaints may predict the development of MCI in PD has not yet been explored. Methods: We prospectively screened newly diagnosed, untreated patients with PD in order to evaluate whether subjective memory complaints may predict development of MCI over a 2-year follow-up evaluation. Results: We enrolled 76 de novo untreated patients with PD. Of the 76 patients, 23 (30.3%) complained memory issues. Among the patients cognitively unimpaired at baseline, those with subjective complaints were more likely to develop MCI at follow-up. The regression model confirmed that presence of subjective memory complaints at baseline was an independent predictor of development of MCI at follow-up. Discussion: This is the first prospective study to explore the relationship between subjective and objective cognitive deficits in newly diagnosed, untreated patients. Our results provide preliminary evidence that subjective memory complaints might predict future development of MCI. Keywords Parkinson disease, cognitive impairment, cognitive testing

Introduction It is well known that patients with Parkinson disease (PD) may exhibit prominent nonmotor symptoms including mood and cognitive disturbances, even at the earliest stage.1,2 The Sidney multicenter study has shown that, over a 15-year follow-up period, up to 80% of patients with PD would develop dementia,3 which in turn negatively affects their quality of life and significantly contributes to institutionalization.4,5 The evidence that in PD there is a spectrum of cognitive dysfunction, ranging from a mild impairment to a frank dementia, has led to borrow the construct of mild cognitive impairment (MCI) from research on Alzheimer disease (AD). Mild cognitive impairment is characterized by a subjective complaint of cognitive decline reported by either the patient or the informant, along with cognitive deficits on formal neuropsychological testing, which results in minimal or no effect on day-to-day functioning.6 Although MCI has been suggested to predict the development of dementia in PD over the long term,7 it is also clear that there is a wide variability among patients with PD with regard to cognitive functions.8

Longitudinal studies on healthy participants have shown that subjective memory impairment (SMI) might be a predictor of dementia, with 10% of persons with SMI converting to a diagnosis of MCI over 3 years.9 These data are corroborated

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Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London (UCL), London, United Kingdom 2 Department of Psychology, Neuropsychology Laboratory, Second University of Naples, Caserta, Italy 3 IDC Hermitage—Capodimonte, Naples, Italy 4 Center for Neurodegenerative Diseases—CEMAND, University of Salerno, Salerno, Italy 5 Department of Neurological Science, University of Naples ‘‘Federico II’’, Naples, Italy 6 Department of Motor Sciences, University of Naples ‘‘Parthenope’’, Naples, Italy Corresponding Author: Paolo Barone, University of Salerno, Center for Neurodegenerative Disease— CEMAND, Via S. Allende, 84081 Baronissi, Salerno, Italy. Email: [email protected]

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by a growing literature showing that patients with SMI have alterations consistent with incipient AD on structural magnetic resonance imaging,10 fluorodeoxyglucose positron emission tomography (PET),11 amyloid PET,12 and cerebrospinal fluid,13 compared to healthy controls without memory complaints. Subjective memory impairment, defined as a subjective cognitive complaint along with normal performance on formal neuropsychological testing, would indeed represent a new construct that should fill the gap in between patients with normal cognition and no subjective reports of memory worsening and patients with MCI. There have been a few studies exploring the relationship between subjective and objective cognitive performances in PD with conflicting results.14-16 Koerts and colleagues found little agreement between subjective complaints and objective measurements of executive functions in PD.14,15 At the opposite, Dujardin et al suggested that objective cognitive decline and dementia might be more frequent among patients with PD having subjective complaints than in patients without.16 However, in the study by Dujardin et al, more severe cognitive complaints were not mirrored by more severe objective deficits.16 Several factors may contribute to such discrepancies, including sample size, methodological issues related to the definition of subjective complaints, and the cross-sectional design of these studies. Furthermore, it is has been reported that (1) cognitive functions in patients with PD can be affected by presence of mood disturbances17; (2) patients with PD having subthreshold depression tend to overestimate their cognitive deficits18; and (3) dopaminergic drugs can affect both cognitive performances and mood.19-21 To address this topic avoiding such potential biases, we prospectively screened newly diagnosed, untreated patients with PD to evaluate whether subjective memory complaints could identify patients with MCI at baseline or predict new development of MCI during a 2year follow-up.

Patients and Methods Patients Enrollment All the patients included in this study were prospectively enrolled in an ongoing research project conducted at the movement disorder center, University Federico II of Naples, Italy. The study was approved by the local ethics committee, and all patients provided written informed consent. Inclusion and exclusion criteria have been extensively described elsewhere.22-25 In brief, we enrolled newly diagnosed, untreated patients with PD (de novo), with symptoms onset less than 2 years. Two years after enrollment, all patients underwent a clinical follow-up to confirm the diagnosis of PD according to both positive response to dopaminergic therapy and exclusion of atypical symptoms/signs. Detailed clinical information was obtained from the patient’s history and neurological examination. Parkinsonism was diagnosed by movement disorder specialists experienced in parkinsonian disorders and staged

according to Hoehn and Yahr (HY stage).26 The Unified Parkinson’s Disease Rating Scale part III—motor subscale (UPDRS-III) was used to evaluate motor disability.27

Neuropsychological Evaluation At baseline, all patients underwent a neuropsychological battery in order to test: (1) memory functions (immediate and delayed recall of the Rey auditory verbal learning test and delayed recall of the Rey-Osterrieth complex figure test)28; (2) visuospatial abilities (Benton judgment of line orientation test, constructional apraxia test—a cognitive task in which a patient has to copy simple and complex figures, thus exploring spatial organization and visuoconstructional skills—and clock drawing test)29-31; and (3) attention/executive functions (frontal assessment battery, phonological and semantic fluency task, copy task of Rey-Osterrieth complex figure test, Corsi block test, verbal span test, Trail making test: part B minus Part A, and interference task of Stroop color-word test).28,29,32-35 In the present study, we did not use Auditory Verbal Learning Test and Rey-Osterrieth complex figure test alternate forms at follow-up since practice effect has been found to be very small in patients with early PD.36-38 Such neuropsychological battery was also administered after a 2-year follow-up. An altered performance in a cognitive test was defined according to methods recently reported.39 Briefly, for each cognitive test, averaged Z scores were calculated and adjusted according to age, education, and sex on the basis of a multiple regression analysis performed in a control group. Tests were considered altered when the difference between the actual Z score and the expected Z score was below 1.5. For the purpose of this study, MCI was diagnosed according to the Movement Disorder Society (MDS) criteria for MCI in PD (level I)6 but regardless of the presence of subjective cognitive complaints. In detail, MDS criteria for MCI require a cognitive decline reported by either the patient or the informant, or observed by the clinician, which does not interfere significantly with functional independence and is accompanied by impairment on at least 2 different neuropsychological tests. We have used here only patients’ neuropsychological performances to categorize them as having MCI. Level I MDS criteria for MCI do not allow the identification of specific subtypes of MCI (ie, executive, visuospatial, etc). However, having our patients been extensively tested for memory functions, we also subcategorized patients with MCI into 2 groups: (1) patients with amnesic MCI (ie, with memory deficits) and (2) patients with nonamnesic MCI (ie, without memory deficits). Subjective cognitive complaints have been screened according to the item 12 (ie, ‘‘Problems remembering things that have happened recently or forgetting to do things’’) of the nonmotor symptoms questionnaire, a validated and recommended tool for detection of nonmotor symptoms in PD.40 This has allowed us to categorize patients as having or not memory complaints, regardless of performances on the neuropsychological battery. Depression and anxiety were assessed by mean of the Hospital

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Table 1. Baseline Demographic and Clinical Features in Our Patients. Total Number ¼ 76 Gender, M:F Age, mean + SD (min-max), years Age at onset, mean + SD (min-max), years Disease duration, mean + SD (min-max), months UPDRS-III, mean + SD (min-max)

47:29 60.5 + 8.3 (48-71) 58.6 + 8.2 (45-70) 14.8 + 6.2 (8-22) 14.6 + 6.9 (6-28)

Abbreviations: F, female; M, male; max, maximum; min, minimum; SD, standard deviation; UPDRS-III, Unified Parkinson’s Disease Rating Scale, part III—motor subscale.

Anxiety Depression Scale (HADS), HADS depression subscale (HADS-D), and HADS anxiety subscale.41

Statistical Analysis After Kolmogorov-Smirnov testing for normal distribution, t-test and w2 test, or Fisher exact when expected values were small, were performed for group comparisons as appropriate and P < .05 deemed as statistical significant. Finally, multiple logistic regression analyses with forward stepping (likelihood ratio method) were applied to assess whether SMI was an independent correlate of MCI. In this model, MCI was used as dependent categorical variable, and SMI, age, age at onset, disease duration, UPDRS-III, and HADS scores were used as independent variables. Statistical analyses were done with SPSS, version 19.

Results Sample Characteristics

33 patients without subjective memory complaints and MCI (subMCI).

Two-Year Follow-Up Neuropsychological Testing Eleven patients refused the neuropsychological testing (3 subþ MCIþ, 2 subþMCI, 3 sub-MCIþ, and 3 sub-MCI), thus 65 patients were included in the follow-up analyses: 10 subþMCIþ, 8 subþMCI, 17 sub-MCIþ, and 30 sub-MCI. Among the 38 patients cognitively unimpaired at baseline assessment, 16 developed MCI at follow-up: 6 of the 8 patients belonged to subþMCI group and 10 of the 30 patients belonged to subMCI group. Twenty-two patients did not develop MCI at follow-up: 2 patients belonged to subþMCI group and 20 patients belonged to subMCI group. Chi-square test showed a significant association between baseline subjective memory complaints and presence of MCI at follow-up (w2 ¼ 4.498, P ¼ .034). We applied regression analyses (with forward conditional method) on the 38 cognitively unimpaired patients at baseline to identify possible predictors of development of MCI at follow-up. The regression model showed that presence of SMI at baseline was an independent predictor of development of MCI at follow-up, after controlling for confounder factors such as age, age at onset, disease duration, UPDRS, HY, and HADS scores (B ¼ 1.792, Wald ¼ 3.931, Exp(B) ¼ 6.000, P ¼ .047). Subtypes of new-onset MCI were not significantly different between patients with and without subjective complaints (amnesic vs nonamnesic: 4 vs 2 in subþMCI and 6 vs 4 in subMCI group; Fisher w2 ¼ 4.59, P ¼ .10).

Discussion

We enrolled 76 newly diagnosed, untreated patients with PD (47 M and 29 F) with a mean (+standard deviation [SD]) age of 60.5 + 8.3 years. Mean (+SD) age at onset was 58.6 + 8.2 years. Demographic and clinical features of the patients are detailed in Table 1.

Baseline Neuropsychological Testing At baseline, 23 of the 76 (30.3%) patients complained about memory issues, while 53 (69.7%) patients did not. Such 2 groups did not differ with regard to age, age at onset, disease duration, motor disability, and on HADS score (Table 2). A total of 33 (43.4%) patients fulfilled the criteria for MCI. It was not more prevalent in patients with subjective memory complaints than in those without (13/23 vs 20/53, respectively, Pearson chi-square [w2] ¼ 2.304, P ¼ .129). Table 2 also details baseline prevalence of MCI in patients with and without subjective memory complaints. According to both neuropsychological results and response at item 12 of NMSQ, we found 13 patients with subjective memory complaints and MCI (subþMCIþ); 10 patients with subjective memory complaints and without MCI (subþMCI); 20 patients without subjective memory complaints but with MCI (subMCIþ);

The present study shows that approximately 25% of de novo patients with PD complain about SMI. Our result is lower than the figure by Dujardin et al (32.2%).16 In fact, they also assessed the presence of blunted affect, inertia, and loss of volition or interest, which explains the higher proportion of patients with subjective cognitive complaints.16 Moreover, they did not involve newly diagnosed, untreated patients, which also might explain to some extent such discrepancy. In our study, subjective memory complaints were able to predict future development of MCI over 2 years. The latter result was confirmed by the regression model, suggesting that subjective memory complaints might be an independent predictor of MCI. A few studies assessing the relationship between subjective and objective cognitive decline in PD have been performed so far, with conflicting results.14-16 Although Dujardin and colleagues found a positive correlation between subjective complaints and objective cognitive decline,16 Koerts failed to confirm such relationship, at least with regard to executive functions.14,15 In a way, our results are partly consistent with all previous reports. In fact, at baseline, we did not find any association between subjective complaints and presence of MCI. Such lack of relationship may simply be due to the cross-sectional type of analysis. It may

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Table 2. Baseline characteristics of the patients, according to the presence of memory complaints. Patients With Memory Complaints ¼ 23 Gender, M:F Age, mean + SD (min-max), years Age at onset, mean + SD (min-max), years Disease duration, mean + SD (min-max), months UPDRS-III, mean + SD HADS, mean + SD HADS-D, mean + SD HADS-A, mean + SD MCI, total, % Amnesic-MCI/nonamnesic MCI, %

14:9 7.8 (50-71) 7.7 (45-69) 7.5 (8-21) 5.9 8.1 3.9 4.7 56.5 46.1/53.9

60.5 + 58.6 + 15.1 + 14.1 + 11.8 + 6.5 + 5.4 +

Patients Without Memory Complaints ¼ 53

P Value

32:20 59.8 + 8.3 (48-71) 58.5 + 8.4 (47-70) 14.7 + 5.7 (8-22) 14.6 + 7.3 11.9 + 7.4 5.8 + 4.2 6.1 + 4.1 37.7 80/20

.956 .728 .968 .815 .751 .941 .527 .469 .129 .032

Abbreviations: M, male; F, female; SD, standard deviation; UPDRS-III, Unified Parkinson’s Disease Rating Scale, part III—motor subscale; HADS, Hospital Anxiety Depression Scale; HADS-D, Hospital Anxiety Depression Scale, Depression subscale; HADS-A, Hospital Anxiety Depression Scale, Anxiety subscale; MCI, mild cognitive impairment.

also reflect the difference in baseline cognitive levels from which individual patients decline (ie, patients with high baseline performance may experience a mild decline subjectively, even if the decline still falls within the normal range). Moreover, neuropsychological tests may not always reflect cognitive functioning in daily life (ie, low ecological validity), a hypothesis that has also been raised for the lack of agreement between subjective and objective executive deficits.14,15 As such, our results are in line with Koerts et al.14,15 On the other hand, this is the first prospective study addressing such topic, and we show here that patients with subjective memory complaints are more likely to develop MCI over 2 years than patients without, confirming previous findings based on the cross-sectional study by Dujardin et al.16 However, it should be noted that, although we have specifically focused on memory complaints, there was not a clear association between subjective reports and one specific type of MCI (ie, amnesic) nor patients with subjective memory complaints were more impaired on specific memory tests than patients without (data not shown). Subjective ‘‘memory’’ complaints predicted future development of both amnesic and nonamnesic types of MCI. This may indicate that patients with PD may experience different cognitive issues (for instance, difficulty keeping track of complex cognitive tasks) and report them as memory disturbances. It has been indeed demonstrated that memory deficits in PD are also associated with impairment of attention allocation, formulation of retrieval strategies, and effortful learning associated with frontal lobe dysfunction.42 It may also be argued that we relied on a single question screening to detect subjective complaints, and this may be in contrast to the observed cognitive heterogeneity of patients with PD. However, we have deliberately focused on memory complaints since deficits in posterior functions (ie, memory and visuospatial functions) are supposed to be the strongest predictors of future development of dementia in PD, reflecting a possible different and additional underlying process43,44 than disruption of the frontal–striatal pathway, which instead is considered responsible for the executive

dysfunction observed in patients with PD. Moreover, very similar approaches have been already used in non-PD populations.9,10 Obviously, it is likely that the development of more structured scales, able to discriminate subjective complaints related to each subtype/pattern of cognitive impairment, might better identify those patients with PD who are more prone to develop dementia. Meta-memory, a construct that may be defined as an individual’s subjective perception of his or her own memory ability and the tendency to apply strategies to the problem of increased memory demands, seems to be intact in patients with PD,45 and this has led to believe that de novo patients with PD are able to judge their mental changes.46 However, there is also evidence that self-awareness of memory deficits can be negatively affected by depressive symptoms.47-49 In our study, patients with subjective memory complaints had higher scores on HADS-D than patients without, but this did not reach the statistical threshold. We have recently reported that subthreshold depression may also be associated with subjective memory complaints.18 However, here HADS scores have been used as covariates in the regression model failing to reach the statistical threshold, thus excluding any potential bias. We acknowledge that possible limitations of our study include the relatively small size of the cohort and the fact that it is not representative of the whole PD population since we have enrolled de novo patients per protocol. However, patients with more advanced PD seem to be more unaware of their own memory problems, as suggested by low patient-proxy consistency with more severe PD symptomatology.49 While addressing on the progression of cognitive decline in PD, it is crucial whether we can predict such decline. When disease-modifying therapies will be available, it will be relevant to early recognize patients who are at higher risk of future development of dementia. In this context, we provide here the preliminary evidence that subjective memory complaints might predict future development of MCI, which in turn is linked to dementia. Further research involving larger samples is warranted to confirm these results.

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Authors’ Note RE contributed in conception, execution, writing the first draft, and reviewing the article for important intellectual concepts; GS, MP, MA, KL, MM, and RA contributed in execution and reviewing the article for important intellectual concepts; PB contributed in conception and reviewing the article for important intellectual concepts; FG contributed in execution; and CV contributed in conception, execution, and reviewing the article for important intellectual concepts. Roberto Erro and Gabriella Santangelo contributed equally to the article.

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Declaration of Conflicting Interests The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: Dr Marcello Moccia, Marina Picillo, and Roberto Allocca receive honoraria from the Department of Neurological Sciences, University of Naples ‘‘Federico II’’, Italy. Dr Carmine Vitale has received honoraria for symposia from Boehringer Ingelheim, Lundbeck, Novartis, Schwarz Pharma/UCB, GSK. He has received salary from IDC Hermitage-Capodimonte and the University of Naples ‘‘Parthenope,’’ Italy. Dr Marianna Amboni and Katia Longo received salary from IDC Hermitage-Capodimonte, Italy. Dr Gabriella Santangelo has received honoraria for symposia from Lundbeck. She has received salary from the Department of Psychology, Second University of Naples, Caserta, Italy. Dr Maria Teresa Pellecchia has received salary from the University of Salerno. Prof Paolo Barone has received honoraria as a Consultant & Advisory Board Memberships for Novartis, Schwarz Pharma/UCB, Merck-Serono, Eisai, Solvay, General Electric and Lundbeck. He has received salary from the University of Salerno.

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Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Prof Paolo Barone has received research support from Boehringer Ingelheim, Novartis, Schwarz Pharma/UCB, Merck-Serono, Solvay, and Lundbeck.

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Do subjective memory complaints herald the onset of mild cognitive impairment in Parkinson disease?

Longitudinal studies on healthy participants have shown that subjective memory impairment (defined as subjective cognitive complaints with normal cogn...
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