Clinical Neurology and Neurosurgery 130 (2015) 98–100

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A comparison of Montreal Cognitive Assessment between patients with visual hallucinations and without visual hallucinations in Parkinson’s disease Eun Joo Chung a , Kyngha Seok b , Sang Jin Kim a,∗ a b

Department of Neurology, Busan Paik Hospital, Inje University College of Medicine, Busan, Republic of Korea Institute of Statistical Information, Department of Data Science, Inje University, Kimhae, Republic of Korea

a r t i c l e

i n f o

Article history: Received 26 April 2014 Received in revised form 25 December 2014 Accepted 28 December 2014 Available online 6 January 2015 Keywords: Visual hallucination Parkinson’s disease Language impairment

a b s t r a c t Background: Visual hallucination (VH) is closely associated with cognitive impairment in Parkinson’s disease (PD). The aim of this study is to analyze the domain of cognitive impairment related to the VH by analyzing cognition in PD. Method: Twenty-six of 58 patients had VH (PD-VH), whereas 32 patients had no hallucinations (PD-NH); patients assigned to the PD-VH on the basis of having at least one VH per week for one month before participation in the study. All of the patients were administered the Montreal Cognitive AssessmentKorean test (MoCA-K). We analyzed the differences in cognition between PD-VH and PD-NH. Results: The Hoehn–Yahr (HY) stage and the Beck Depression Inventory version I (BDI) scores in PD-VH were significantly different from those in PD-NH. After adjusting for the HY stage and BDI, the language domain of the MoCA-K cognitive domains presents a significant difference between PD-VH and PD-NH. Conclusion: Sentence processing and naming as the composition of the language domain in the MoCA-K have been associated in common with posterior cortical dysfunction. Although our result shows that the language domain of MoCA-K is sensitive to cognitive deficit in PD-VH patients, it needs further neuroimaging analysis for certifying the relationship between language impairment and posterior cortical deficit as the pathophysiology of PD-VH. © 2015 Published by Elsevier B.V.

1. Introduction Visual hallucinations (VH) in Parkinson’s disease (PD) are a chronic complication in more than 50% of all of the PD patients with advanced disease [1]. VH in PD is associated with decreased cognition [2]. The prevalence rate of VH in PD without dementia is between 7 and 15%, which is much lower than that in PDD, which ranged from 41 to 87% [3]. The patients without dementia who have hallucinations show a faster rate of cognitive decline than those without hallucinations [4–9]. Thus, PD patients with VH (PD-VH) showed a lower cognitive status than those without hallucinations (PDNH) [2,10]. The cognitive deficits in PD-VH affect several cognitive domains such as visual and verbal memory, language comprehension and visuoperceptive-visuospatial tasks (e.g., object and space

∗ Corresponding author at: Department of Neurology, Inje University College of Medicine, 75 Bokji-ro, Buanjin-gu, Busan 614-735, Republic of Korea. Tel.: +82 51 890 6425; fax: +82 51 895 6367. E-mail address: [email protected] (S.J. Kim). 0303-8467/© 2015 Published by Elsevier B.V.

perception) and frontal/executive function including verbal fluency, inhibition and attention [4,5,8,9,11–15]. The Montreal Cognitive Assessment (MoCA) is a well-known screening tool for the diagnosis of cognitive impairment in PD [16–21]. MoCA uses numerous demanding tasks to assess executive function, higher-level language abilities, memory and complex visuospatial processing [19,21]. Herein, we investigated the domain of cognitive impairment related to the VH by analyzing the MoCA in PD.

2. Methods 2.1. Subjects Twenty-six PD-VH patients diagnosed with PD according to the UK Brain Bank Criteria were prospectively enrolled [22]. The gating question to assess the presence or absence of VH was recorded using the neuropsychiatric inventory (NPI) [23]. The patients with a frequency score ≥2 were considered to have hallucinations as follows: (2. Sometimes: approximately once per week; 3. Often:

E.J. Chung et al. / Clinical Neurology and Neurosurgery 130 (2015) 98–100


Table 1 Demographic characteristics of the patients. Clinical variables

PD-VH (n = 26)

Age (y) Onset age (y) Disease duration (m) Education (y) HY stage BDI MMSE LEDD (mg)

68.4 62.0 77.5 6.7 2.6 28.2 24.2 710.6

± ± ± ± ± ± ± ±

PD-NH (n = 32)

7.7 8.2 43.2 3.9 0.4 12.6 2.8 535.8

64.8 58.5 77.0 7.3 2.2 21.2 26.2 560.4

± ± ± ± ± ± ± ±

8.6 10.0 38.0 3.8 0.3 11.1 2.3 396.9

P-value 0.106 0.157 0.965 0.496 0.001 0.031 0.066 0.225

PD-VH, Parkinson’s disease patients with visual hallucinations; PD-NH, Parkinson’s disease patients without hallucinations; y, year; m, month; HY stage, Hoehn–Yahr stage; BDI, Beck Depression Inventory; MMSE, Mini Mental State Examination; LEDD, l-dopa equivalent dose; mg, milligram. Bold values indicate P < 0.05 statistically significant.

Table 2 Comparison of subtests in the MoCA-K between PD-VH and PD-NH before and after adjusting for the HY stages and BDI scores. MoCA

PD-VH (n = 26)

PD-NH (n = 32)

P-value before adjustment

P-value after adjustment

Total score MoCA items Orientation Executive function Attention Visuospatial function Language Memory

20.0 ± 4.6

23.3 ± 4.3



0.032 0.800 0.060 0.052 0.005 0.114

0.787 0.995 0.166 0.12 0.009 0.254

5.5 1.8 3.8 2.3 3.9 2.1

± ± ± ± ± ±

0.6 0.9 1.7 1.0 1.5 1.5

5.8 1.9 4.6 2.8 4.9 2.7

± ± ± ± ± ±

0.5 1.0 1.4 1.0 0.9 1.4

MoCA, Montreal Cognitive Assessment; PD, Parkinson’s disease; VH, visual hallucination. Bold values indicate P < 0.05 statistically significant.

several times per week but less than every day; 4. Very often: once or more per day) for the previous four weeks was obtained on the hallucinations item of the NPI. For a match with the PD-VH patients, we adjusted on the basis of sex, age, disease duration and education in the PD-NH patients. Thirty-two patients without hallucinations were enrolled in the PD-NH group. Patients with other types of hallucination without VH were excluded, as were patients with dementia with Lewy bodies (DLB) based on the revised criteria for the clinical diagnosis of DLB [24]. Patients with Parkinson’s-plus syndromes, secondary or atypical Parkinsonism, other neurological diseases, psychiatric disorders and past medical history of dementia were excluded. Possible medical comorbidities were excluded by laboratory tests including the thyroid function, vitamin B12 and folic acid level and VDRL tests. Severity of parkinsonian motor sign was assessed by the Hoehn–Yahr (HY) stage [25]. The l-dopa equivalent dose was calculated for all of the anti-PD medications by the established protocol [26]. The study was approved by the Institutional Review Board of Busan Paik Hospital. We obtained written informed consent from all of the subjects participating in this study.

2.2. Assessment of cognitive functions and depression All of the PD patients performed cognitive assessment during the “on” state. All of the patients were administered the Korean Mini-Mental State Examination (K-MMSE) [27], the MoCA-Korean test (MoCA-K) [28] and the Beck Depression Inventory version I (BDI) [29,30]. The BDI is one of the most frequently used self-rating scales for depression [30]. We divided the specific items of MoCA-K as follows: visuospatial abilities (a clock drawing task, three points; a three-dimensional cube copy, one point) (four points); memory (five points for delayed recall); language (confrontation naming, three points; repetition, two points; semantic fluency, one point) (six points); frontal executive (trail making B task, one point; verbal abstraction, two points) (three points); concentration (attention; six points); and

orientation (six points). One point is added if the subject has ≤6 years of education. 2.3. Statistical analysis The demographic and clinical characteristics, including the KMMSE and BDI scores, of the PD with VH and without VH patients were compared using an independent-sample t-test or chi square test. We performed an analysis of covariance (ANCOVA) to evaluate whether the MoCA-K means are equal across the VH levels, while statistically controlling for the effect of the covariates. P < 0.05 was considered statistically significant. The data were analyzed using IBM SPSS Statistics 20.0 software (IBM Corporation, Chicago, IL). 3. Results Demographic characteristics are listed in Table 1. There were no significant differences in the age, age at onset, disease duration, education and MMSE scores between the PD-VH and PD-NH patients. However, despite of no statistical significance, PD-VH showed older age, less education, higher age onset, more severe cognition, and higher daily levodopa dose than PD-NH. As shown in Table 1, the PD-VH group was differentiated from the PD-NH group in the HY stage (P = 0.001) and the BDI (P = 0.031). We compared scores of each domain as well as the total scores in the MoCA-K between PD-VH and PD-NH before and after controlling for the effect of the HY stages and the BDI scores. PD-VH patients obtained worse scores in the total MoCA-K, orientation and language than those of PD-NH patients before adjusting for HY stage and BDI score. However, the scores of the language domain of the MoCA-K only showed statistical differences between the two groups (3.9 ± 1.5 vs. 4.9 ± 0.9, P = 0.009) after adjustment (Table 2). 4. Discussion PD-VH patients in this study show worse parkinsonian motor sign, more severe depression and lower MoCA-K scores compared to PD-NH. These results in PD-VH are similar to previous reports


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[31–33], and the presence of VH in PD is probably related to both motor and non-motor symptoms. In a variety of cognitive dysfunction [8,9,15,34], neuropsychological tests in PD-VH commonly showed posterior cortical dysfunction (PCD) [5,6,35]. Recently, PCD has been identified as one of the main risk factors for dementia and hallucinations [36,37]. Contrast to before adjustment, language domain of the MoCA-K only shows significantly lower score in PD-VH than in PD-NH after adjusting for the HY stage and BDI score. The language deficit in PD-VH is typically caused by a dysfunction of verbal comprehension and naming [8]. Verbal comprehension could be related to an impairment in sentence processing [38], which has been associated with reduced activation of the anteromedial prefrontal cortex and posterolateral temporal regions [39]. Confrontation naming difficulty is associated with anterior temporal lobe atrophy [40]. The language domain of the MoCA is typically allotted to sentences and naming [41]. Our result shows that the language domain of subtests in the MoCA-K is sensitive to cognitive impairment in PD-VH patients. However, for analyzing the relationship between language deficit and PCD in PD-VH patients, we need to perform the neuroimaging analysis. A recent study showed very modest correlations between the MoCA subtests and specific neuropsychological instruments to evaluate such cognitive functions [42]. The poor results in language domain could serve as an indicator of dysfunction of temporal lobe, but we have to evaluate the language with wide and specific battery for language assessment to confirm the temporal dysfunction. Conflict of interest There is no conflict of interest to declare. References [1] Forsaa EB, Larsen JP, Wentzel-Larsen T, Goetz CG, Stebbins GT, Aarsland D, et al. A 12-year population-based study of psychosis in Parkinson disease. Arch Neurol 2010;67:996–1001. [2] Holroyd S, Currie L, Wooten GF. Prospective study of hallucinations and delusions in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2001;70:734–8. [3] Fenelon G, Alves G. Epidemiology of psychosis in Parkinson’s disease. J Neurol Sci 2010;289:12–7. [4] Ramirez-Ruiz B, Junque C, Marti MJ, Valldeoriola F, Tolosa E. Cognitive changes in Parkinson’s disease patients with visual hallucinations. Dement Geriatr Cogn Disord 2007;23:281–8. [5] Barnes J, Boubert L. Executive functions are impaired in patients with Parkinson’s disease with visual hallucinations. J Neurol Neurosurg Psychiatry 2008;79:190–2. [6] Santangelo G, Trojano L, Vitale C, Ianniciello M, Amboni M, Grossi D, et al. A neuropsychological longitudinal study in Parkinson’s patients with and without hallucinations. Mov Disord 2007;22:2418–25. [7] Ozer F, Meral H, Hanoglu L, Ozturk O, Aydemir T, Cetin S, et al. Cognitive impairment patterns in Parkinson’s disease with visual hallucinations. J Clin Neurosci 2007;14:742–6. [8] Ramirez-Ruiz B, Junque C, Marti MJ, Valldeoriola F, Tolosa E. Neuropsychological deficits in Parkinson’s disease patients with visual hallucinations. Mov Disord 2006;21:1483–7. [9] Grossi D, Trojano L, Pellecchia MT, Amboni M, Fragassi NA, Barone P. Frontal dysfunction contributes to the genesis of hallucinations in non-demented Parkinsonian patients. Int J Geriatr Psychiatry 2005;20:668–73. [10] Hobson P, Meara J. Risk and incidence of dementia in a cohort of older subjects with Parkinson’s disease in the United Kingdom. Mov Disord 2004;19:1043–9. [11] Botha H, Carr J. Attention and visual dysfunction in Parkinson’s disease. Parkinsonism Relat Disord 2012;18:742–7. [12] Barnes J, Boubert L. Visual memory errors in Parkinson’s disease patient with visual hallucinations. Int J Neurosci 2011;121:159–64. [13] Meppelink AM, Koerts J, Borg M, Leenders KL, van Laar T. Visual object recognition and attention in Parkinson’s disease patients with visual hallucinations. Mov Disord 2008;23:1906–12. [14] Imamura K, Wada-Isoe K, Kitayama M, Nakashima K. Executive dysfunction in non-demented Parkinson’s disease patients with hallucinations. Acta Neurol Scand 2008;117:255–9.

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A comparison of montreal cognitive assessment between patients with visual hallucinations and without visual hallucinations in Parkinson's disease.

Visual hallucination (VH) is closely associated with cognitive impairment in Parkinson's disease (PD). The aim of this study is to analyze the domain ...
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