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Comparison of Cognitive, Affective, and Activities of Daily Living Functions in Patients with Parkinson’s Disease and Progressive Supranuclear Palsy

Koji Abe*, Nozomi Hishikawa, Yusuke Fukui, Kota Sato, Mami Takemoto, Toru Yamashita, and Yasuyuki Ohta

Department of Neurology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan

*Corresponding Author:
Koji Abe
Department of Neurology
Okayama University Graduate School of Medicine
Dentistry and Pharmaceutical Sciences
Okayama, 700-8558, Japan
Tel: +81-86-235-7365;
Email: [email protected]

Received Date: December 10, 2018; Accepted Date: December 24, 2018; Published Date: January 01, 2018

Citation: Abe K, Hishikawa N, Fukui Y, Sato K, Takemoto M et al.(2019) Comparison of Cognitive, Affective, and Activities of Daily Living Functions in Patients with Parkinson’s Disease and Progressive Supranuclear Palsy. J Brain Behav Cogn Sci Vol.2 No.1:2.

Copyright: © 2019 Abe K, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

 
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Abstract

Aim: The purpose of this study was to compare the cognitive/affective and Activities of Daily Living (ADL) functions of Parkinson’s Disease (PD) and Progressive Supranuclear Palsy (PSP). Methods: We retrospectively recruited 324 PD patients, 109 PSP patients, and 111 control subjects, and investigated their cognitive/affective and ADL functions, especially in PD patients when compared with PSP patients. Results: Cognitive functional scores (MMSE, HDS-R, FAB, and MoCA) of total PD and PSP were lower than the control. In particular, recent and working memory, initiation, executive functions, and attention of PSP were significantly lower than total PD. Affective functional scores (geriatric depression scale, Apathy Score: AS, and Abe’s BPSD score) of total PD and PSP were worse than the control, and AS of PSP was significantly worse than total PD. Within PD, cognitive/affective, and ADL functions were expressed in an H-Y stage-dependent manner. Conclusion: Our results demonstrate that the PSP cognitive functions and AS were significantly worse than the PD. Moreover, the cognitive/affective and ADL functions of PD were similar to, or worse, than PSP in severe H-Y stages of PD, suggesting greater dysfunctions of both motor symptoms and cognitive/affective functions in an advanced stage of PD than PSP.

Keywords

Activities of daily living functions; Affective functions; Cognitive functions; Hoehn and Yahr stage; Parkinson’s disease; Progressive supranuclear palsy

Introduction

Parkinson’s disease (PD) is considered as the second most prevalent neurodegenerative disease after Alzheimer’s Disease (AD) [1] both of which are increasing worldwide due to rapid aging society [2]. PD is mainly characterized by motor symptoms such as resting tremor, bradykinesia, rigidity, and postural instability, and by non-motor symptoms including cognitive dysfunctions (executive, visual perception, attention), autonomic failure, sleep disorder, behavioural and psychiatric symptoms (e.g. depression, apathy, psychosis, hallucination) [3-5]. Their symptoms are related to the neuronal degeneration of mainly dopaminergic neurons associated with the accumulation of α-synuclein as Lewy bodies.

aging society [2]. PD is mainly characterized by motor symptoms such as resting tremor, bradykinesia, rigidity, and postural instability, and by non-motor symptoms including cognitive dysfunctions (executive, visual perception, attention), autonomic failure, sleep disorder, behavioural and psychiatric symptoms (e.g. depression, apathy, psychosis, hallucination) [3-5]. Their symptoms are related to the neuronal degeneration of mainly dopaminergic neurons associated with the accumulation of α-synuclein as Lewy bodies. Progressive Supranuclear Palsy (PSP) is the second most extrapyramidal disorder after PD, [6] which is classically characterized by early postural instability, supranuclear gaze palsy, and parkinsonism, as well as cognitive and affective impairments [5,7-10]. The neuropathology of PSP includes degeneration of not only the subthalamic nucleus, globus pallidus, substantia nigra, ventral tegmentum of midbrain and pons, dentate nucleus, but also the precentral gyrus, and premotor and supplementary motor areas, accompanied by the accumulations of tau protein in the neuron and glial cells [11-14].

Although PD is neuropathologically different from PSP, they sometimes show similar clinical manifestations especially in cognitive and affective functions. Our previous studies showed the supplemental diagnostic method for distinguishing PD and PSP during the early stage by using the MRI, iodine-123 Meta- Iodobenzyl Guanidine (123I-MIBG) myocardial scintigraphy, Single Photon Emission Computed Tomography (SPECT), and MRI-based dynamic cerebrospinal fluid flow [15,16]. In the present clinic-based cross-sectional study, we compared the cognitive, affective, and Activities of Daily Living (ADL) functions of PD and PSP with age-matched control subjects for a possible different features.

Methods

Participants

In the present retrospective study, we recruited 324 patients with PD (178 males and 146 females; mean age: 73.9 ± 6.3 years) and 109 patients with PSP (66 males and 43 females; mean age: 73.7 ± 6.5 years) at the Department of Neurology Okayama University Hospital and its affiliated hospitals. Clinical diagnoses were based on the consensus criteria for probable PD [17] and the National Institute of Neurological Disorders and Stroke and the Society for PSP, Inc. (NINDS-SPSP) criteria [6]. In addition, PD patients were divided into 5 subgroups by Hoehn and Yahr (H-Y) stage, stage(6 males and 7 females; mean age: 71.8 ± 5.9 years), stage(28 males and 27 females; mean age: 72.9 ± 6.3 years), stage (54 males and 69 females; mean age: 73.6 ± 6.2 years), stage (83 males and 36 females; mean age: 74.8 ± 6.3 years), and stage (7 males and 7 females; mean age: 75.9 ± 6.3 years). Age- and gender- matched 111 control individuals were also included (66 males and 45 females; mean age: 74.1 ± 6.5 years) who underwent medical examinations and found no neurological nor psychiatric diseases. In the present study, their medical records were reviewed, and cognitive, affective and ADL functions have been assessed for the above 324 PD patients, 109 PSP patients, and 111 control subjects (Table 1).

Table 1: Demographic and characteristic data of control subjects, PD, and PSP patients. ¶¶ Data are represented as mean ± SD. † p<0.05, PSP vs. Total PD; ¶¶ p<0.01, PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP. M/F: Male/Female; NA: Not Applicable; H-Y stage: Hoehn and Yahr stage; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Table 1: Demographic and characteristic data of control subjects, PD, and PSP patients. ¶¶ Data are represented as mean ± SD. † p<0.05, PSP vs. Total PD; ¶¶ p<0.01, PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP. M/F: Male/Female; NA: Not Applicable; H-Y stage: Hoehn and Yahr stage; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Control Total PD PSP H-Y stage of PD
Number 111 324 109 13 55 123 119 14
Gender 66\45 178\146 66\43 6\7 28\27 54\69 83\36 7\7
Age (years) 74.1 ± 6.5 73.9 ± 6.3 73.7 ± 6.5 71.8 ± 5.9 72.9 ± 6.3 73.6 ± 6.2 74.8 ± 6.3 75.9 ± 7.6
Duratoin (months) NA 69.5 ± 58.9 31.3 ± 21.0† 16.4 ± 3.2 36.6 ± 32.6 61.5 ± 51.5 108.6 ± 58.7 ¶¶ ¶¶ 142.4 ± 69.4

Ethical permission for this study was given by the Ethics Committee on Epidemiological Studies of the Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Science (approval # 1603-031), and informed consents were obtained from participants in this study.

Assessments of cognitive, affective, and ADL functions

According to our previous reports, cognitive functions were assessed using Mini-Mental State Examination (MMSE), Hasegawa Dementia Score-Revised (HDS-R), Frontal Assessment Battery (FAB), and Montreal Cognitive Assessment (MoCA). As affective functions, depression, apathy and Behavioural and Psychological Symptoms of Dementia (BPSD) were evaluated using the Geriatric Depression Scale (GDS), Apathy Scale (AS) and the Abe’s BPSD score (ABS), [18] respectively. Activities of Daily Living (ADL) of the patients were also assessed using the Alzheimer’s Disease Cooperative Study-Activities of Daily Living (ADCS-ADL).

Statistical analysis

Statistical analyses were performed using statistical software IBM SPSS Statistics for Windows, Version 22.0 (IBM Corporation, Armonk, N.Y., USA). After checking normality, we carried out the Kruskal-Wallis tests to compare each cognitive, affective and ADL functional assessments, subscales of cognitive, affective and ADL functional assessments with control, PD, and PSP groups. Pvalues less than 0.05 were considered significant.

Results

and characteristic data of participants (111 control subjects, 324 total PD patients, and 109 PSP patients) is presented in table 1. Cognitive functional scores (MMSE, HDS-R, FAB, and MoCA) of total PD and PSP were significantly lower than control, and all of these scores of PSP were significantly lower than total PD (Figures 1a-d). Affective functional scores (GDS, AS, and ABS) of total PD and PSP were significantly worser than control (**p<0.01) (Figures 1e-g). AS of PSP were significantly worser than total PD (†† p<0.01) (Figure 1f). The ADL score of total PD and PSP were also significantly lower than control (**p<0.01) (Figure 1h), but no difference between PSP and PD. Within PD, cognitive, affective, and ADL functions were worser in an H-Y stage-dependent manner and cognitive and AS functions were worser in PSP than PD with H-Y stageand (Figures 1a-h).

brain-behaviour-and-cognitive-sciences-functional

Figure 1: (a-h left side) Comparison of cognitive, affective and ADL functional scores among the three groups; control: white bars, total PD: black bars, and PSP: striped bars. The results are expressed as full scores (*p<0.05, **p<0.01: Total PD or PSP vs. control, † p<0.05, †† p<0.01: Total PD vs. PSP). (a-h right side) Comparison of cognitive, affective and ADL functional scores among the six groups; PSP: striped bars, and PD with Hoehn and Yahr (H-Y) stageⅠ-Ⅴ(gray bars). The results are expressed as full scores (§ p<0.05, §§ p<0.01: PD with H-Y stage (Ⅰ-Ⅴ) vs. control, ¶ p<0.05, ¶¶ p<0.01: PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP).

Subscale analysis of the above cognitive tests were significantly worser than control in the tasks of orientation of time and place (MMSE, HDS-R, MoCA), calculation (MMSE, HDSR), recall (MMSE, HDS-R, MoCA), 3-stage commands (MMSE), digit span (HDS-R, MoCA), write a composition (MMSE), copy a figure (MMSE, MoCA), visual retention (HDS-R), word fluency (HDS-R), letter fluency (FAB), conflict (FAB), go/no-go (inhibitory control) (FAB), Trail Making Test (TMT) (MoCA), clock drawing (MoCA), target tapping (MoCA), serial 7 subtraction (MoCA), and repeat sentences (MoCA) (*p<0.05, **p<0.01, total PD or PSP vs control) (Table 2). Furthermore, these cognitive tests of PSP showed significant decreases than those of PD, and a tend to worse with progression of H-Y stage fromto in orientation of time, place and age (MMSE, HDS-R), registration (MMSE, HDSR), calculation (MMSE, HDS-R), recall (HDS-R, MoCA), repeat sentence (MMSE), obey a written command (MMSE), copy a figure (MMSE, MoCA), digit span (HDS-R, MoCA), visual retention (HDS-R), word fluency (HDS-R), conceptualization (FAB), letter fluency (FAB), programming (FAB), conflict (FAB), and verbal abstraction (MoCA) († p<0.05, †† p<0.01, total PD vs. PSP) (Table 2).

Table 2: Cognitive function (MMSE, HDS-R, FAB, MoCA) subscale analysis data of control, PD, and PSP. Data are represented as mean ± SD Kruskal-Wallis test was performed respectively *p<0.05 and **p<0.01, Total PD or PSP versus control; † p<0.05 and †† p<0.01, PSP vs. Total PD; § p<0.05 and §§ p<0.01, PD with H-Y stage (Ⅰ-Ⅴ) vs. control; ¶ p<0.05 and ¶¶ p<0.01, PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP. FAB: Frontal Assessment Battery; GDS: Geriatric Depression Scale; HDS-R: Hasegawa Dementia Scale-Revised; H-Y stage: Hoehn and Yahr stage; MMSE: Mini-Mental State Examination; MoCA: Montreal Cognitive Assessment; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Table 2: Cognitive function (MMSE, HDS-R, FAB, MoCA) subscale analysis data of control, PD, and PSP. Data are represented as mean ± SD Kruskal-Wallis test was performed respectively *p<0.05 and **p<0.01, Total PD or PSP versus control; † p<0.05 and †† p<0.01, PSP vs. Total PD; § p<0.05 and §§ p<0.01, PD with H-Y stage (Ⅰ-Ⅴ) vs. control; ¶ p<0.05 and ¶¶ p<0.01, PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP. FAB: Frontal Assessment Battery; GDS: Geriatric Depression Scale; HDS-R: Hasegawa Dementia Scale-Revised; H-Y stage: Hoehn and Yahr stage; MMSE: Mini-Mental State Examination; MoCA: Montreal Cognitive Assessment; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Control Total PD PSP Control Total PD PSP PD with H-Y stage
MMSE subscale
Orientation (time) 4.9 ± 0.4 4.3 ± 1.2** 3.6 ± 1.6**, †† 4.8 ± 0.6 4.7 ± 0.9 ¶¶ 4.6 ± 0.9 ¶¶ 3.8 ± 1.3 §§ 3.5 ± 1.3 §§
Orientation (place) 4.9 ± 0.3 4.6 ± 0.9* 4.1 ± 1.5**, † 4.8 ± 0.4 4.8 ± 0.5 ¶ 4.7 ± 0.7 ¶¶ 4.2 ± 1.2 §§ 4.7 ± 0.6
registration 3.0 ± 0.0 2.9 ± 0.4 2.8 ± 0.8**, † 3.0 ± 0.0 3.0 ± 0.0 ¶ 3.0 ± 0.1 ¶ 2.8 ± 0.6 §§ 2.8 ± 0.6
calculation 4.5 ± 1.1 3.4 ± 1.8** 2.4 ± 1.9**, †† 3.7 ± 1.7 3.9 ± 1.6 ¶¶ 3.6 ± 1.8 §, ¶¶ 3.1 ± 1.9 §§ 2.1 ± 2.0 §§
recall 2.5 ± 1.1 2.2 ± 1.0* 2.0 ± 1.1** 2.2 ± 1.0 2.5 ± 0.7 ¶ 2.4 ± 0.8 1.9 ± 1.1 §§ 1.5 ± 1.0§
naming 2.0 ± 0.0 2.0 ± 0.2 1.9 ± 0.5* 2.0 ± 0.0 2.0 ± 0.0 2.0 ± 0.0 ¶ 1.9 ± 0.4 2.0 ± 0.0
repeat sentence 0.9 ± 0.3 0.9 ± 0.3 0.8 ± 0.4 † 1.0 ± 0.0 0.8 ± 0.4 1.0 ± 0.2 ¶¶ 0.9 ± 0.3 0.8 ± 0.4
3-stage commands 2.9 ± 0.3 2.6 ± 0.8** 2.5 ± 0.9* 3.0 ± 0.0 2.6 ± 0.7 2.7 ± 0.6 2.4 ± 0.9 §§ 1.9 ± 0.8 §§, ¶
obey a written command 1.0 ± 0.0 1.0 ± 0.2 0.9 ± 0.3**, †† 1.0 ± 0.0 1.0 ± 0.0 ¶ 1.0 ± 0.0 ¶¶ 0.9 ± 0.2 1.1 ± 0.3 ¶
write a composition 1.0 ± 0.2 0.8 ± 0.4** 0.7 ± 0.4** 0.9 ± 0.3 0.8 ± 0.4 0.9 ± 0.3 § 0.7 ± 0.4 ¶¶ 0.5 ± 0.5 ¶¶
copy a figure 1.0 ± 0.1 0.8 ± 0.4** 0.7 ± 0.5**, † 1.0 ± 0.0 0.8 ± 0.4 § 1.0 ± 0.2 ¶¶ 0.7 ± 0.5 §§ 0.5 ± 0.5 §§
HDS-R subscale
 Orientation (age) 1.0 ± 0.0 1.0 ± 0.2 0.9 ± 0.3**,†† 1.0 ± 0.0 1.0 ± 0.0 ¶¶ 1.0 ± 0.2 ¶¶ 0.9 ± 0.3 0.9 ± 0.3
Orientation (place) 2.0 ± 0.1 1.9 ± 0.4* 1.7 ± 0.7**, †† 2.0 ± 0.0 2.0 ± 0.3 ¶¶ 2.0 ± 0.1 ¶¶ 1.8 ± 0.5 §§ 1.9 ± 0.3
Orientation (time) 3.9 ± 0.3 3.3 ± 1.0** 2.9 ± 1.4**, † 3.9 ± 0.3 3.6 ± 0.9 ¶¶ 3.6 ± 0.7 ¶¶ 2.9 ± 1.2 §§ 2.6 ± 1.3 §§
Registration 3.0 ± 0.0 2.9 ± 0.4 2.7 ± 0.9**, † 3.0 ± 0.0 3.0 ± 0.3 ¶ 3.0 ± 0.1 ¶¶ 2.8 ± 0.6 §§ 2.7 ± 0.7
Calculation 1.9 ± 0.3 1.6 ± 0.7** 1.3 ± 0.8**, † 1.8 ± 0.4 1.7 ± 0.5 ¶ 1.7 ± 0.6 ¶¶ 1.4 ± 0.9 §§ 1.1 ± 0.9 §§
Recall 5.3 ± 1.0 4.8 ± 1.6* 4.0 ± 2.1**, †† 5.0 ± 1.4 5.4 ± 1.1 ¶¶ 5.1 ± 1.3 ¶¶ 4.2 ± 1.9 §§ 3.8 ± 1.9
Digit span 1.7 ± 0.6 1.4 ± 0.8** 1.0 ± 0.8**, †† 1.8 ± 0.4 1.5 ± 0.8 ¶ 1.5 ± 0.8 ¶¶ 1.3 ± 0.8 §§ 0.6 ± 0.8 §§
Visual retention 4.8 ± 0.5 4.3 ± 1.1** 3.6 ± 1.7**, †† 4.9 ± 0.3 ¶ 4.6 ± 0.8 ¶¶ 4.6 ± 0.7 ¶¶ 4.0 ± 1.3 §§ 3.3 ± 1.6 §
Word fluency 4.9 ± 0.6 4.3 ± 1.5** 2.8 ± 2.2**, †† 4.8 ± 0.6 ¶ 4.6 ± 1.2 ¶¶ 4.6 ± 1.1 ¶¶ 3.9 ± 1.8 §§, ¶¶ 2.8 ± 2.3 §
FAB subscale
Conceptualization 2.7 ± 0.6 2.4 ± 0.9 2.1 ± 1.2**, † 2.5 ± 1.0 2.4 ± 1.0 2.6 ± 0.7 ¶ 2.3 ± 1.0 1.9 ± 1.2
Letter fluency 2.6 ± 0.7 2.0 ± 1.0** 1.6 ± 1.1**, † 2.5 ± 0.7 2.3 ± 0.8 ¶¶ 2.1 ± 1.0 §§ 1.8 ± 1.0 §§ 1.6 ± 1.2
Programming 2.7 ± 0.5 2.5 ± 0.9 1.9 ± 1.3**, †† 2.7 ± 0.7 2.8 ± 0.6 ¶¶ 2.7 ± 0.6 ¶¶ 2.1 ± 1.1 §§ 2.2 ± 1.3
Conflict 2.9 ± 0.3 2.3 ± 1.1** 1.7 ± 1.4**, †† 2.7 ± 0.9 2.5 ± 1.0 ¶ 2.5 ± 0.9 ¶¶ 2.1 ± 1.3 §§ 1.8 ± 1.5
Go/no-go 2.2 ± 1.0 1.5 ± 1.4** 1.4 ± 1.3** 2.5 ± 1.0 2.0 ± 1.2 1.7 ± 1.3 1.0 ± 1.3 §§ 0.7 ± 1.1§
Forced grasping 3.0 ± 0.1 2.8 ± 0.6* 2.8 ± 0.7 3.0 ± 0.0 3.0 ± 0.1 2.9 ± 0.4 2.6 ± 0.9 §§ 2.7 ± 1.0
MoCA subscale
 Trail making test 0.8 ± 0.4 0.4 ± 0.5** 0.3 ± 0.5** 0.9 ± 0.4 0.4 ± 0.5 §§ 0.5 ± 0.5 §§ 0.4 ± 0.5 §§ 0.0 ± 0.0 §§
Copy a figure 0.9 ± 0.3 0.7 ± 0.5** 0.5 ± 0.5**, †† 1.0 ± 0.0 0.7 ± 0.4 0.8 ± 0.4 ¶¶ 0.5 ± 0.5 §§ 0.4 ± 0.5 §
Clock drawing 2.6 ± 0.6 2.1 ± 0.9** 1.9 ± 1.1** 2.7 ± 0.5 2.2 ± 0.9 2.3 ± 0.8 1.9 ± 1.0 §§ 1.4 ± 1.1 §§
Naming 2.9 ± 0.4 2.7 ± 0.7 2.7 ± 0.6 3.0 ± 0.0 2.8 ± 0.5 2.8 ± 0.5 2.6 ± 0.9 2.1 ± 1.1 §
Digit span 1.8 ± 0.5 1.5 ± 0.7* 1.3 ± 0.7**, †† 2.0 ± 0.0 1.7 ± 0.5 ¶ 1.6 ± 0.6 ¶¶ 1.3 ± 0.8 §§ 1.4 ± 0.7
Target tapping 1.0 ± 0.2 0.7 ± 0.4** 0.6 ± 0.5** 0.9 ± 0.4 0.8 ± 0.4 0.8 ± 0.4 ¶ 0.6 ± 0.5§§ 0.6 ± 0.5
Serial 7 subtraction 2.8 ± 0.6 2.2 ± 1.0** 2.0 ± 1.0** 2.4 ± 1.0 2.4 ± 0.9 2.4 ± 0.9 1.9 ± 1.0 §§ 1.5 ± 1.2 §§
Repeat sentences 1.3 ± 0.6 0.9 ± 0.6** 0.8 ± 0.7** 1.0 ± 0.0 1.2 ± 0.7 0.8 ± 0.6 §§ 0.8 ± 0.5§§ 0.6 ± 0.7
Phonemic fluency 0.6 ± 0.5 0.5 ± 0.5 0.4 ± 0.5* 0.6 ± 0.5 0.7 ± 0.5 0.5 ± 0.5 0.5 ± 0.5 0.3 ± 0.5
Verbal abstraction 1.9 ± 0.3 1.8 ± 0.5 1.6 ± 0.7**, † 2.0 ± 0.0 1.9 ± 0.3 1.9 ± 0.4 ¶ 1.6 ± 0.6 § 1.5 ± 0.5
Recall 3.2 ± 1.5 2.4 ± 1.8** 1.5 ± 1.5**, †† 2.0 ± 1.8 2.5 ± 1.6 2.8 ± 1.8 ¶¶ 2.0 ± 1. §§ 1.4 ± 1.8
Orientation (time, place) 5.9 ± 0.3 5.3 ± 1.2** 4.8 ± 1.6** 5.9 ± 0.4 5.4 ± 1.0 5.5 ± 0.9 § 5.0 ± 1.5 §§ 4.6 ± 1.6

Table 2: Cognitive function (MMSE, HDS-R, FAB, MoCA) subscale analysis data of control, PD, and PSP. Data are represented as mean ± SD Kruskal-Wallis test was performed respectively *p<0.05 and **p<0.01, Total PD or PSP versus control; † p<0.05 and †† p<0.01, PSP vs. Total PD; § p<0.05 and §§ p<0.01, PD with H-Y stage (-) vs. control; ¶ p<0.05 and ¶¶ p<0.01, PD with H-Y stage (-) vs. PSP. FAB: Frontal Assessment Battery; GDS: Geriatric Depression Scale; HDS-R: Hasegawa Dementia Scale-Revised; H-Y stage: Hoehn and Yahr stage; MMSE: Mini-Mental State Examination; MoCA: Montreal Cognitive Assessment; PD: Parkinson's Disease; PSP: Progressive Supranuclear .

Most GDS subscales showed that total PD and PSP were significantly worser than control (*p<0.05, **p<0.01), especially in H-Y stage and (# p<0.05, ## p<0.01). The subscale of “problems in memory” in total PD was significantly worser than PSP († p<0.05) (Table 3).

Table 3:  Affective function (GDS, AS, ABS) subscale analysis data of control, PD, and PSP. Data are represented as mean ± SD. Kruskal-Wallis test was performed respectively. *p<0.05, **p<0.01; Total PD or PSP vs. control, † p<0.05, †† p<0.01; PSP vs. Total PD, § p<0.05, §§ p<0.01; PD with H-Y stage (Ⅰ-Ⅴ) vs. control, ¶ p<0.05, ¶¶ p<0.01 PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP. ABS, Abe's behavioural and psychological symptoms of dementia score; ADCS-ADL: Alzheimer’s Disease Cooperative Study-Activities of Daily Living; AS: Apathy Scale; GDS: Geriatric Depression Scale; H-Y stage: Hoehn and Yahr Stage; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Table 3:  Affective function (GDS, AS, ABS) subscale analysis data of control, PD, and PSP. Data are represented as mean ± SD. Kruskal-Wallis test was performed respectively. *p<0.05, **p<0.01; Total PD or PSP vs. control, † p<0.05, †† p<0.01; PSP vs. Total PD, § p<0.05, §§ p<0.01; PD with H-Y stage (Ⅰ-Ⅴ) vs. control, ¶ p<0.05, ¶¶ p<0.01 PD with H-Y stage (Ⅰ-Ⅴ) vs. PSP. ABS, Abe's behavioural and psychological symptoms of dementia score; ADCS-ADL: Alzheimer’s Disease Cooperative Study-Activities of Daily Living; AS: Apathy Scale; GDS: Geriatric Depression Scale; H-Y stage: Hoehn and Yahr Stage; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Control Total PD PSP Control Total PD PSP PD with H-Y stage
GDS subscale
Satisfied with life 0.1 ± 0.3 0.2 ± 0.4** 0.4 ± 0.5** 0.1 ± 0.3 0.1 ± 0.3 0.3 ± 0.5 §§ 0.3 ± 0.5 §§ 0.1 ± 0.3
Feel happy 0.2 ± 0.4 0.4 ± 0.5* 0.4 ± 0.5** 0.2 ± 0.4 0.3 ± 0.5 ¶ 0.3 ± 0.5 0.4 ± 0.5§ 0.5 ± 0.5
Good mood 0.3 ± 0.5 0.5 ± 0.5** 0.6 ± 0.5** 0.2 ± 0.4 0.5 ± 0.5 §§ 0.5 ± 0.5 § 0.6 ± 0.5 §§ 0.8 ± 0.4 §
Worth living 0.1 ± 0.2 0.2 ± 0.4** 0.2 ± 0.4** 0.0 ± 0.0 0.2 ± 0.4 0.3 ± 0.5§§ 0.2 ± 0.4 0.0 ± 0.0
Filled with energy 0.3 ± 0.5 0.5 ± 0.5** 0.6 ± 0.5** 0.1 ± 0.3 ¶ 0.4 ± 0.5 0.4 ± 0.5 0.5 ± 0.5 § 0.8 ± 0.4 §
Less activity 0.4 ± 0.5 0.6 ± 0.5** 0.7 ± 0.5** 0.3 ± 0.5 0.5 ± 0.5 §§ 0.6 ± 0.5 § 0.7 ± 0.5 §§ 0.6 ± 0.5
Better tp be inside 0.2 ± 0.4 0.5 ± 0.5** 0.5 ± 0.5** 0.5 ± 0.5 0.5 ± 0.5§§ 0.6 ± 0.5 §§ 0.4 ± 0.5 §§ 0.6 ± 0.5
Feel empty 0.0 ± 0.2 0.2 ± 0.4** 0.2 ± 0.4** 0.0 ± 0.0 0.2 ± 0.4 0.3 ± 0.5§§ 0.2 ± 0.4 § 0.4 ± 0.5
Bored 0.1 ± 0.3 0.2 ± 0.4* 0.3 ± 0.5** 0.2 ± 0.4 0.1 ± 0.3 0.2 ± 0.4 0.3 ± 0.4 § 0.5 ± 0.5
Anticipatory anxiety 0.1 ± 0.3 0.3 ± 0.5** 0.3 ± 0.5** 0.2 ± 0.4 0.3 ± 0.5 0.3 ± 0.5 §§ 0.4 ± 0.5§§ 0.5 ± 0.5 §
Powerlessness 0.1 ± 0.3 0.4 ± 0.5** 0.4 ± 0.5** 0.4 ± 0.5 0.3 ± 0.5 0.4 ± 0.5§§ 0.5 ± 0.5 §§ 0.4 ± 0.5
Problems with memory 0.2 ± 0.4 0.4 ± 0.5 0.5 ± 0.5**, † 0.4 ± 0.5 0.3 ± 0.5 0.4 ± 0.5 0.4 ± 0.5 0.2 ± 0.4
Worthlessness 0.0 ± 0.2 0.3 ± 0.5** 0.3 ± 0.5** 0.0 ± 0.0 0.2 ± 0.4 0.3 ± 0.5 §§ 0.3 ± 0.5 §§ 0.2 ± 0.4
Situation cannot be done 0.2 ± 0.4 0.5 ± 0.5** 0.6 ± 0.5** 0.3 ± 0.5 0.3 ± 0.5 ¶ 0.5 ± 0.5 §§ 0.5 ± 0.5 §§ 0.8 ± 0.4 §§
Feeling of poverty 0.0 ± 0.2 0.2 ± 0.4** 0.2 ± 0.4** 0.0 ± 0.0 0.1 ± 0.3 0.3 ± 0.4 §§ 0.2 ± 0.4 0.3 ± 0.5
AS subscale
Learning new things 1.4 ± 0.8 1.2 ± 0.9 1.7 ± 1.0 †† 1.7 ± 0.7 1.1 ± 0.9 ¶ 1.1 ± 1.0 ¶¶ 1.4 ± 0.8 1.8 ± 0.7
Having some interest 1.0 ± 0.8 1.3 ± 0.9** 1.6 ± 1.0** 1.3 ± 0.9 1.2 ± 0.9 1.4 ± 1.0 1.4 ± 0.9 1.4 ± 0.8
Concern about condition 0.7 ± 0.7 0.9 ± 0.8 0.9 ± 1.0 0.8 ± 0.8 0.6 ± 0.7 0.8 ± 0.8 1.1 ± 0.8 1.0 ± 0.9
Engrossed in some things 1.2 ± 0.8 1.2 ± 0.9 1.7 ± 0.9**, †† 1.7 ± 0.9 1.1 ± 0.9 ¶¶ 1.1 ± 0.9 ¶¶ 1.4 ± 0.8 1.7 ± 0.9
Looking for something 1.0 ± 0.7 1.2 ± 0.9 1.4 ± 1.0** 1.2 ± 0.7 1.0 ± 0.9 1.2 ± 1.0 1.3 ± 0.9 1.2 ± 0.7
Plans for the future 1.4 ± 0.8 1.6 ± 0.9* 1.9 ± 0.9** 2.0 ± 0.5 1.4 ± 0.9 1.5 ± 1.0 1.8 ± 0.9§ 1.9 ± 0.9
Motivations 1.2 ± 0.8 1.3 ± 0.9** 1.6 ± 0.9**,† 1.6 ± 0.5 1.2 ± 0.9 1.3 ± 1.0 1.4 ± 0.9 1.4 ± 1.0
Energy for daily activities 1.1 ± 0.7 1.3 ± 0.9 1.5 ± 0.9** 1.3 ± 0.7 1.1 ± 0.8 1.3 ± 0.8 1.5 ± 0.9 § 1.5 ± 0.8
No idea about what to do 0.1 ± 0.3 0.7 ± 0.9** 1.0 ± 1.0** 0.1 ± 0.3 0.3 ± 0.6 ¶¶ 0.7 ± 0.8 §§ 0.9 ± 1.0 §§ 0.8 ± 0.7 §§
Indifference 0.1 ± 0.3 0.5 ± 0.8** 1.0 ± 1.1**, †† 0.1 ± 0.3 ¶ 0.4 ± 0.7 ¶¶ 0.5 ± 0.9 §§, ¶¶ 0.7 ± 0.9 §§ 0.9 ± 0.9 §§
Lack of concern 0.0 ± 0.2 0.5 ± 0.9** 1.0 ± 1.0**, †† 0.0 ± 0.0 ¶¶ 0.3 ± 0.8 ¶¶ 0.4 ± 0.8 §§, ¶¶ 0.7 ± 0.9 §§ 0.8 ± 1.0 §
Need a push to get started 0.1 ± 0.4 0.5 ± 0.8** 0.9 ± 1.1**, †† 0.0 ± 0.0 ¶ 0.3 ± 0.6 ¶¶ 0.4 ± 0.9 ¶¶ 0.7 ± 0.9 §§ 0.8 ± 0.7 §§
Apathy 0.3 ± 0.7 0.6 ± 0.8** 1.2 ± 1.0**, †† 0.2 ± 0.4 0.5 ± 0.7 ¶¶ 0.6 ± 0.8 ¶¶ 0.8 ± 0.9 §§ 1.1 ± 0.8 §§
Spiritless 0.2 ± 0.4 0.7 ± 0.8** 1.2 ± 1.1**, †† 0.3 ±0.7 0.4 ± 0.7¶¶ 0.6 ± 0.7 §§, ¶¶ 0.9 ± 0.9 §§ 1.4 ± 0.9 §§
ABS subscale
Wandering in/outside home 0.0 ± 0.0 0.3 ± 1.0 0.4 ± 1.4 0.0 ± 0.0 0.2 ± 1.0 0.1 ± 0.6 0.5 ± 1.3 §§ 0.0 ± 0.0
Eating or toilet problem 0.0 ± 0.0 0.4 ± 1.3** 0.2 ± 0.8 0.0 ± 0.0 0.2 ± 1.1 0.2 ± 0.7 0.6 ± 1.5 §§ 1.9 ± 2.7 §§
Delusion or hallucination 0.0 ± 0.2 0.6 ± 1.5** 0.3 ± 0.9 0.0 ± 0.0 0.6 ± 1.5 0.4 ± 1.0 0.9 ± 1.8 0.3 ± 0.7
Offensive and abusive words 0.1 ± 0.5 0.4 ± 0.9* 0.5 ± 1.0* 0.0 ± 0.0 0.6 ± 1.2 0.3 ± 0.7 0.5 ± 0.8 §§ 1.0 ± 1.1
Day-night reversal 0.0 ± 0.2 0.4 ± 1.0** 0.6 ± 1.4** 0.0 ± 0.0 0.4 ± 1.1 0.1 ± 0.6 0.7 ± 1.2 §§ 0.0 ± 0.0
Excitation and agitation 0.0 ± 0.2 0.2 ± 0.5 0.2 ± 0.6 0.0 ± 0.0 0.2 ± 0.6 0.1 ± 0.3 0.3 ± 0.7 § 0.0 ± 0.0
Apathy and indifference 0.0 ± 0.2 0.2 ± 0.6* 0.2 ± 0.6 0.2 ± 0.4 0.2 ± 0.4 0.1 ± 0.4 0.3 ± 0.6 0.8 ± 0.9 §§
Depressive and gloomy 0.0 ± 0.1 0.1 ± 0.3 0.1 ± 0.3 0.0 ± 0.0 0.0 ± 0.2 0.1 ± 0.3 0.1 ± 0.3 0.1 ± 0.4
Violent force 0.0 ± 0.0 0.0 ± 0.1 0.0 ± 0.2 0.0 ± 0.0 0.0 ± 0.0 0.0 ± 0.0 0.0 ± 0.2 0.0 ± 0.4
High irritability 0.0 ± 0.2 0.0 ± 0.2 0.0 ± 0.2 0.0 ± 0.0 0.1 ± 0.3 0.0 ± 0.0 0.0 ± 0.2 0.0 ± 0.0

Most subscales of AS were significantly worser in total PD than control for plans for future (*p<0.05), and have some interest, no idea what about to do, indifference, unconcern, need a push to get started, apathy, and spiritless (respectively, **p<0.01). PSP declined in the following subscales comparing with control; have some interest, engrossed in something’s, looking for something to do, plans for future, motivations, energy for daily activities, no idea what about to do, indifference, unconcern, need a push to get started, apathy, and spiritless (respectively, **p<0.01). Similarly, 8 subscales of PSP were significantly worser than total PD in motivations († p<0.05), learning new thing, engrossed in somethings, indifference, unconcern, need a push to get started, apathy, and spiritless (respectively, †† p<0.01) (Table 3).

Table 3: Affective function (GDS, AS, ABS) subscale analysis data of control, PD, and PSP. Data are represented as mean ± SD. Kruskal-Wallis test was performed respectively. *p<0.05, **p<0.01; Total PD or PSP vs. control, † p<0.05, †† p<0.01; PSP vs. Total PD, § p<0.05, §§ p<0.01; PD with H-Y stage (-) vs. control, ¶ p<0.05, ¶¶ p<0.01 PD with H-Y stage (-) vs. PSP. ABS, Abe's behavioural and psychological symptoms of dementia score; ADCS-ADL: Alzheimer’s Disease Cooperative Study- Activities of Daily Living; AS: Apathy Scale; GDS: Geriatric Depression Scale; H-Y stage: Hoehn and Yahr Stage; PD: Parkinson's Disease; PSP: Progressive Supranuclear Palsy.

Subscales analysis of ABS were significantly worser in total PD than control in offensive and abusive words, and apathy and indifference (respectively, *p<0.05), and eating or toilet problem, delusion or hallucination, and day-night reversal (respectively, **p<0.01). Those of PSP were significantly worser than control in offensive and abusive words (*p<0.05), and daynight reversal (**p<0.01). There was no significant difference between PD and PSP (Table 3).

Most ADL subscales of PD and PSP were significantly declined than control, and tended to be worse with progression of H-Y stages (data not shown). Subscale scores of clothes, bathing, and cash management in PSP were significantly worser than total PD († p<0.05).

Discussion

In this clinic-based cross-sectional study, we found that the cognitive, affective and ADL functions of PD and PSP were significantly decreased comparing with age-matched control subjects, and that the cognitive functions and apathy score of PSP were significantly worser than PD. Within PD, cognitive, affective and ADL functional declines became worser in an H-Y stage-dependent manner, and these functions of PSP were similar to PD with H-Y stages and .

Although both PD and PSP caused cognitive declines such as executive functions, attention, and memory [3,5,19,20] cognitive disturbance in PSP was more frequent and severer than PD [5]. Our present study also revealed that scores of all 4 standard cognitive functional tests were significantly worser in PSP than PD, especially in “orientation”, “registration”, “calculation”, “repeat sentence”, “obey a written command”, “figure copy”, “recall”, “backward digit span”, “visual retention”, “word and letter fluency”, “conceptualization”, “programming”, and “conflict”. Impairments to “recent and working memory”, “initiation”, “search strategies”, “executive functions”, and “attention/concentration” were severer in PSP than PD patients, probably because neurodegeneration in PSP was exaggerated not only in the midbrain, caudate nuclei, thalamus, hypothalamus, but also the frontal cortex and parahippocampal gyrus. A previous study reported a decrease of regional Cerebral Blood Flow (rCBF) in the pre-supplementary motor cortex and prefrontal cortex compared with normal control subjects and PD patients [15,21].

Previous studies showed more frequent prevalence of depression to be 4-70% in PD than apathy (15-50%), [22-24] but contrasting findings have also been reported [25,26]. On the other hand, PSP showed more apathy (35-91%), followed by depression, agitation, irritability, and disinhibition [8-10]. The present study basically confirmed the above previous reports, but the mean depressive scores were similar between PD and PSP (Figures 1e and Table 3). BPSD score measured by ABS was worser both in total PD and PSP than control, and was worser in H-Y stage-dependent manner within PD (Figures 1g and Table 3). Significant deteriorations of both instrumental and basic ADL in total PD and PSP suggested daily life problems, especially in the 3 items such as clothes, bathing, and cash management in PSP († p<0.05), corresponding to the frontal cerebral cortical dysfunction in PSP.

Among PD patients, there was no significant difference in cognitive, affective, and ADL functions in early stage PD (H-Y stage I) from the control, but these functions became worser at the advanced stage (H-Y stages IV and V) similar to PSP (Figures 1a-1h) (Tables 2 and 3). MoCA was worser in PD at stages II and more (Figure 1d and Table 2), and ABS and ADCS-ADL scores were worser at stage IV and more, suggesting more dysfunctions in PD relating to not only motor symptoms but also cognitive and affective functional declines after moderate stage [27,28].

In summary, the present study demonstrated that both PD and PSP were associated with cognitive, affective, and ADL functional declines than the age- and gender-matched control (Figures 1a-1h) (Tables 2 and 3). However, “recent and working memory”, “initiation”, “search strategies”, “executive functions”, and “attention, concentration” were worser in PSP than PD, and PSP was more apathetic than PD. The present study also showed that cognitive, affective, and ADL functions of PD become similar to or even worse than PSP in an H-Y stage-dependent manner.

References

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