Clinical Neurology and Neurosurgery 115 (2013) 2524–2527
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Clinical correlates of anhedonia in patients with Parkinson’s disease Kiyohiro Matsui a , Hisao Tachibana a,∗ , Toshiyuki Yamanishi a , Miyako Oguru a , Kazuo Toda b , Bungo Okuda c , Nobuyuki Oka d a
Department of Internal Medicine, Hyogo College of Medicine, Nishinomiya, Japan Toda Internal Medicine-Rehabilitation Clinic, Akashi, Japan Department of Neurology, Ehime Prefectural Central Hospital, Matsuyama, Japan d Department of Rehabilitation, NHO South Kyoto Hospital, Joyo, Japan b c
a r t i c l e
i n f o
Article history: Received 6 February 2013 Received in revised form 12 August 2013 Accepted 19 October 2013 Available online 31 October 2013 Keywords: Parkinson’s disease Anhedonia Anxiety Depression QOL
a b s t r a c t Objective: To investigate the prevalence and clinical correlates of anhedonia in patients with Parkinson’s disease (PD) and to also examine the relationship between anhedonia and the QOL. Methods: One hundred and seventeen patients with PD completed the Snaith–Hamilton Pleasure Scale (SHAPS), the State–Trait Anxiety Inventory (STAI), the Beck Depression Inventory Second Edition (BDIII), Starkstein’s Apathy Scale (AS) and a quality of life (QOL) battery. Hoehn and Yahr (HY) staging, the Unified Parkinson’s Disease Rating Scale (UPDRS) and the Mini-Mental State Examination (MMSE) were administered on the same day. Results: Anhedonia (SHAPS score ≥ 3) was diagnosed in 15% of the patients. The SHAPS score was found to be significantly correlated with the HY stage and the UPDRS (I, IVB , IVC , total), BDI-II, AS and STAI (State, Trait) scores. A multivariate analysis revealed that the BDI-II and STAI (Trait) scores significantly influenced the SHAPS scores. The SHAPS scores were found to be negatively correlated with the QOL. Conclusions: These findings indicate that anhedonia is associated with depression and anxiety. In addition, recognizing anhedonia in patients with PD is important since it may have a negative effect on the QOL. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Although Parkinson’s disease (PD) is primarily a movement disorder, it is also accompanied by various nonmotor symptoms, including psychiatric and behavioral problems. Depression is the most common neuropsychiatric disorder [1] in patients with PD. Identifying depression is based on the subjective perception of depressive symptoms, including feelings of incapacity, reduced reactions to emotional stimuli and anhedonia [2]. Anhedonia, defined as a reduced ability to experience physical or social pleasure, is generally considered to be a key symptom of several psychiatric illnesses other than depression, including schizophrenia, apathy, abstinence and intoxication with several substances of abuse [3]. Anhedonia is reported to be primary symptoms of depression in patients with PD [4]. Some studies have investigated the relationship between anhedonia and neuropsychological symptoms and found correlations with the frontal lobe function (3). Reports on the relationships between anhedonia and illness
∗ Corresponding author at: Department of Internal Medicine, Hyogo College of Medicine, 1-1 Mukogawa-cho, Nishinomiya, Hyogo 663-8501, Japan. Tel.: +81 798 45 6865; fax: +81 798 45 6977. E-mail addresses: [email protected], fl[email protected] (H. Tachibana). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.10.013
severity or motor symptoms are rather inconclusive. No definitive conclusions can be drawn on this topic. In addition, there are no reports on the relationship between anhedonia and the quality of life (QOL), although the effects of depression on the QOL in patients with PD have been intensively studied [5–7]. The purpose of this study was to examine the prevalence of anhedonia in a case series of PD patients, the relationships between anhedonia and disease-related factors such as the severity of motor and non-motor symptoms, levodopa therapy, complications of pharmacotherapy and disease duration and the relationship between anhedonia and the QOL.
2. Methods 2.1. Patients One hundred and twenty-five consecutive patients with idiopathic PD who attended four outpatient clinics (Hyogo College of Medicine Hospital, Toda Internal Medicine-Rehabilitation Clinic, NHO South Kyoto Hospital and Ehime Prefectural Central Hospital) between April 2010 and September 2010 were included in this study. PD was diagnosed according to the UK Parkinson’s Disease Society Brain Bank Criteria [8]. Treatment with antiparkinsonian drugs improved the parkinsonian signs and symptoms in all treated
K. Matsui et al. / Clinical Neurology and Neurosurgery 115 (2013) 2524–2527
patients. Patients with either secondary parkinsonism or evidence of more generalized neurological disease were excluded. Participants were excluded if they declined to participate later or were unable to complete the self-administered questionnaires due to dementia. Therefore, data were obtained from 117 patients with PD. None of the patients underwent deep brain stimulation (DBS) surgery during the course of the study. Written informed consent was obtained from all study participants. The study protocol was approved by the human research ethics committees at the participating institutions, and this study was conducted according to the Declaration of Helsinki. 2.2. Assessment instruments/questionnaires The patients were clinically assessed using assessment instruments that included both neurologist-administered rating scales and self-administered questionnaires. The neurologistadministered assessments included the modified Hoehn and Yahr Scale (HY) [9] to stage PD severity according to the patient’s best “on” state, the Unified Parkinson’s Disease Rating Scale (UPDRS) [10] and the Mini-Mental State Examination (MMSE) [11]. These examinations were all performed by a neurologist on the same day. The self-administered scales included the Snaith–Hamilton Pleasure scale (SHAPS) [12], the State–Trait Anxiety Inventory (STAI) [13], the Beck Depression Inventory (BDI) [14], an apathy scale (AS) [15] and the QOL instrument the 39-item Parkinson’s disease questionnaire (PDQ-39) [16]. The self-administered questionnaires were given in the same order to each patient. The patients were told to take as much time as they needed to answer these questionnaires in order to control for test-induced fatigue. Anhedonia was evaluated with the Japanese version of the SHAPS [16,17]. The SHAPS comprises 14 items covering four domains of pleasure experience and food/drink. Higher SHAPS scores represents a reduction in hedonic tone, with a cutoff score of 3 or more for anhedonia and a normal hedonic tone being defined as a score of 0. The SHAPS has recently become widely used for assessing anhedonia in PD patients. The Japanese version of the SHAPS has been shown to have good validity, test–retest reliability and internal consistency [17]. Anxiety was evaluated with the Japanese version of the STAI [18]. The STAI consists of two scales designed to differentiate between the temporary condition of the state of anxiety (Form X1) and the more general and long-standing quality of trait anxiety (Form X-2). Each item on the STAI scale is scored on four levels of anxiety intensity from 1 = “not at all” to 4 = “very much,” with a sum score between 20 and 80. Twenty items are designed to record the presence of anxiety symptoms, while the other items are scored to record the absence of anxiety symptoms. The latter are inverted for the purpose of calculating the sum score. The cutoff score for the STAI was set at 41 for males and 42 for females [18]. The STAI has been used in many studies of PD patients. These studies indicate that the instrument is appropriate for use in screening anxiety, studying biological markers and as an outcome measure [19], although further validation such studies in PD populations is still needed. Depression was evaluated using the Japanese version of the BDI Second Edition (BDI-II) [19], which is widely used in Japan to assess depression and is reported to have excellent reliability and validity. The BDI-II is a 21-item scale. The items are rated from 0 to 3, with a sum score between 0 and 63. The resulting scores are added across the items to yield an overall measure of the intensity of depressive symptomatology. The cutoff score for the BDI-II was set at 14, as is standard in Japan and also indicated in the original version [20]. The Japanese version [21] of Starkstein’s Apathy Scale was used to assess apathy. This scale was chosen based on a review of apathy and anhedonia rating scales in patients with PD conducted by
2525
Leentjens et al. [19] in which they recommended only this scale be used to assess apathy in PD patients. The cut off score was set at 16 rather than 14 as indicated in the original scale because the Japanese version demonstrates high reliability (sensitivity: 81.3%) with a cutoff score of 16 [21]. The Japanese version [22] of the PDQ-39, a 39-item questionnaire, was used for the QOL assessment. The PDQ-39 is a widely used disease-specific health-related QOL measure that was translated and validated in Japan by Kohmoto et al. [22]. The PDQ-39 contains 39 questions, each with five different answer options, from which eight subscores (mobility, activities of daily living [ADLs], emotional well-being, stigma, social support, cognition, communication and bodily discomfort) and one summary index (SI) can be calculated. The maximum score of 100 indicates the worst quality of life. 2.3. Statistical analysis Group differences were analyzed using nonparametric tests (Mann–Whitney U-tests). Spearman’s rank correlation coefficients were used to assess the degree of correlation between the SHAPS scores and the following variables: age, age at onset, disease duration, HY stage, UPDRS total and individual subscale scores, the MMSE score, the BDI-II score, the STAI score, the AS score, the levodopa equivalent dose (LED) and the PDQ-39 score. The daily LED was calculated as [23]: (regular levodopa dose × 1) + (pramipexole dose × 67) + (ropinirole dose × 16.67) + (pergolide dose × 100) + (bromocriptine dose × 10) + (regular levodopa dose × 0.25 if taking entacapone). A multivariate analysis using stepwise linear regression was performed to determine the factors associated with the SHAPS score. The SHAPS score was considered to be a dependent variable, and variables found to be significantly associated with the SHAPS score on the basis of Spearman’s rank correlations were included as independent (explanatory) variables. All data were analyzed using the Dr. SPSS software package (SPSS version 11.0). Statistical significance was set at P < 0.05. 3. Results Table 1 shows the clinical characteristics of the 117 PD study patients. There were no differences in the clinical variables between males and females, although this series included a larger number of females. Anhedonia (SHAPS score ≥ 3) was present in 18 of the 117 patients (15%), depression was present in 66 patients (56%), apathy was present in 60 patients (51%) and anxiety (Trait) in 64 patients (55%). Anhedonia coexisted with depression in 16 patients (14%), with apathy in 14 patients (12%) and with anxiety in 17 patients (15%). Table 2 shows the relationships between the SHAPS scores and several clinical variables. The SHAPS scores exhibited significant correlations with HY (rs = 0.269, P = 0.004), UPDRS I (rs = 0.349, P < 0.001), IVB (rs = 0.248, P = 0.007), IVC (rs = 0.291, P = 0.002), the UPDRS total score (rs = 0.198, P = 0.033), BDI-II (rs = 0.564, P < 0.001), AS (rs = 0.435, P < 0.001) and the STAI State (rs = 0.215, P = 0.021) and STAI Trait scores (rs = 0.362, P < 0.001). The SHAPS scores did not show any significant associations with gender, age, age at onset, duration of illness or LED. There were no significant differences in the mean SHAPS score between the 34 patients taking pramipexole (0.9 ± 1.6; mean ± SD) and those patients not taking pramipexole (1.1 ± 1.9). Multivariate analyses using stepwise regression were performed to determine which factors contribute to the SHAPS scores. Variables significantly associated with the SHAPS scores were
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K. Matsui et al. / Clinical Neurology and Neurosurgery 115 (2013) 2524–2527
Table 1 Characteristics of the Study Patients. Total (n = 117)
Male (n = 46)
Female (n = 71)
Mean
Mean
Mean
Age (yr) 69.4 61.4 Age at onset (yr) 8.3 Duration of disease (yr) 2.8 Hoehn–Yahr stage UPDRS I (mentation) 2.3 UPDRS II (ADL) 7.8 18.9 UPDRS III (motor) UPDRS IV (complications) 0.7 A dyskinesia 1.9 B motor fluctuation C othersa 0.7 UPDRS total 34.1 MMSE 27.6 1.0 SHAPS 15.8 BDI-II STAI 43.2 Form X-1 43.9 Form X-2 16.1 AS l-Dopa equivalent dose 450.2 PDQ-39 42.0 Mobility 35.5 ADL 37.3 Emotional well-being 23.9 Stigma 21.2 Social support Cognition 34.1 20.5 Communication Bodily discomfort 31.2 30.8 Summary index
SD
SD
SD
9.1 10.2 5.0 0.8 2.4 7.7 14.2
69.1 60.3 8.8 2.9 2.6 8.6 18.2
8.8 9.8 5.5 0.8 2.9 8.3 12.0
69.7 62.1 7.9 2.7 2.0 7.3 19.3
9.3 10.4 4.6 0.8 2.0 7.2 15.5
1.5 1.8 0.9 24.0 2.6 1.6 9.7
0.9 1.9 0.6 33.4 27.4 1.2 15.9
1.8 1.7 0.9 23.7 2.4 1.8 10.0
0.6 1.9 0.8 34.6 27.8 0.8 15.7
1.4 1.8 1.0 24.2 2.8 1.4 10.0
11.2 11.1 7.4 224.3
44.3 44.9 16.0 486.0
11.5 11.6 7.3 235.2
42.5 43.2 16.2 426.7
10.8 10.7 7.5 215.4
29.0 29.2 25.0 21.6 28.1 20.9 21.6 25.6 18.7
37.6 38.7 34.1 23.6 19.6 37.0 23.2 28.6 30.2
30.8 30.8 22.6 20.8 28.7 20.8 22.7 24.9 20.3
44.8 33.6 39.3 24.2 22.3 32.3 18.7 32.3 31.3
27.7 28.2 26.3 22.2 27.8 20.8 20.8 25.9 17.7
Notes: ADL, activity of daily living; UPDRS, Unified Parkinson’s disease rating scale; MMSE, Mini-Mental State Examination; SHAPS, Snaith–Hamilton pleasure scale; BDI-II, Beck Depression Inventory–II; STAI, State–Trait Anxiety Inventory; AS, Apathy Scale; PDQ-39 SI, Parkinson’s disease questionnaire. a Anorexia, nausea, vomiting, sleep disturbance, symptomatic orthostasis.
entered as independent variables. The stepwise linear regression model revealed that the BDI-II, and STAI Trait scores (P = 0.010) significantly influenced the SHAPS scores (F = 18.501; P < 0.001) (Table 3). A significant correlation was noted between the SHAPS scores and the PDQ-39 SI (rs = 0.409, P < 0.001) (Table 4).
Table 2 Relationships between the SHAPS scores and clinical variables. Variables
rs
P
Gender Age Age at onset Duration of disease Hoehn–Yahr stage UPDRS I (mentation) UPDRS II (ADL) UPDRS III (motor) UPDRS IV (complications) A dyskinesia B motor fluctuation C others UPDRS total MMSE BDI-II AS STAI State Trait l-Dopa equivalent dose
−0.086 0 051 −0.050 0.066 0.269 0.349 0.141 0.172
0.367 0.584 0.593 0.480 0.004 0.000 0.131 0.064
0.113 0.248 0.291 0.198 −0.032 0.564 0.435
0.226 0.007 0.002 0.033 0.734
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Clinical correlates of anhedonia in patients with Parkinson’s disease Kiyohiro Matsui a , Hisao Tachibana a,∗ , Toshiyuki Yamanishi a , Miyako Oguru a , Kazuo Toda b , Bungo Okuda c , Nobuyuki Oka d a
Department of Internal Medicine, Hyogo College of Medicine, Nishinomiya, Japan Toda Internal Medicine-Rehabilitation Clinic, Akashi, Japan Department of Neurology, Ehime Prefectural Central Hospital, Matsuyama, Japan d Department of Rehabilitation, NHO South Kyoto Hospital, Joyo, Japan b c
a r t i c l e
i n f o
Article history: Received 6 February 2013 Received in revised form 12 August 2013 Accepted 19 October 2013 Available online 31 October 2013 Keywords: Parkinson’s disease Anhedonia Anxiety Depression QOL
a b s t r a c t Objective: To investigate the prevalence and clinical correlates of anhedonia in patients with Parkinson’s disease (PD) and to also examine the relationship between anhedonia and the QOL. Methods: One hundred and seventeen patients with PD completed the Snaith–Hamilton Pleasure Scale (SHAPS), the State–Trait Anxiety Inventory (STAI), the Beck Depression Inventory Second Edition (BDIII), Starkstein’s Apathy Scale (AS) and a quality of life (QOL) battery. Hoehn and Yahr (HY) staging, the Unified Parkinson’s Disease Rating Scale (UPDRS) and the Mini-Mental State Examination (MMSE) were administered on the same day. Results: Anhedonia (SHAPS score ≥ 3) was diagnosed in 15% of the patients. The SHAPS score was found to be significantly correlated with the HY stage and the UPDRS (I, IVB , IVC , total), BDI-II, AS and STAI (State, Trait) scores. A multivariate analysis revealed that the BDI-II and STAI (Trait) scores significantly influenced the SHAPS scores. The SHAPS scores were found to be negatively correlated with the QOL. Conclusions: These findings indicate that anhedonia is associated with depression and anxiety. In addition, recognizing anhedonia in patients with PD is important since it may have a negative effect on the QOL. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Although Parkinson’s disease (PD) is primarily a movement disorder, it is also accompanied by various nonmotor symptoms, including psychiatric and behavioral problems. Depression is the most common neuropsychiatric disorder [1] in patients with PD. Identifying depression is based on the subjective perception of depressive symptoms, including feelings of incapacity, reduced reactions to emotional stimuli and anhedonia [2]. Anhedonia, defined as a reduced ability to experience physical or social pleasure, is generally considered to be a key symptom of several psychiatric illnesses other than depression, including schizophrenia, apathy, abstinence and intoxication with several substances of abuse [3]. Anhedonia is reported to be primary symptoms of depression in patients with PD [4]. Some studies have investigated the relationship between anhedonia and neuropsychological symptoms and found correlations with the frontal lobe function (3). Reports on the relationships between anhedonia and illness
∗ Corresponding author at: Department of Internal Medicine, Hyogo College of Medicine, 1-1 Mukogawa-cho, Nishinomiya, Hyogo 663-8501, Japan. Tel.: +81 798 45 6865; fax: +81 798 45 6977. E-mail addresses: [email protected], fl[email protected] (H. Tachibana). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.10.013
severity or motor symptoms are rather inconclusive. No definitive conclusions can be drawn on this topic. In addition, there are no reports on the relationship between anhedonia and the quality of life (QOL), although the effects of depression on the QOL in patients with PD have been intensively studied [5–7]. The purpose of this study was to examine the prevalence of anhedonia in a case series of PD patients, the relationships between anhedonia and disease-related factors such as the severity of motor and non-motor symptoms, levodopa therapy, complications of pharmacotherapy and disease duration and the relationship between anhedonia and the QOL.
2. Methods 2.1. Patients One hundred and twenty-five consecutive patients with idiopathic PD who attended four outpatient clinics (Hyogo College of Medicine Hospital, Toda Internal Medicine-Rehabilitation Clinic, NHO South Kyoto Hospital and Ehime Prefectural Central Hospital) between April 2010 and September 2010 were included in this study. PD was diagnosed according to the UK Parkinson’s Disease Society Brain Bank Criteria [8]. Treatment with antiparkinsonian drugs improved the parkinsonian signs and symptoms in all treated
K. Matsui et al. / Clinical Neurology and Neurosurgery 115 (2013) 2524–2527
patients. Patients with either secondary parkinsonism or evidence of more generalized neurological disease were excluded. Participants were excluded if they declined to participate later or were unable to complete the self-administered questionnaires due to dementia. Therefore, data were obtained from 117 patients with PD. None of the patients underwent deep brain stimulation (DBS) surgery during the course of the study. Written informed consent was obtained from all study participants. The study protocol was approved by the human research ethics committees at the participating institutions, and this study was conducted according to the Declaration of Helsinki. 2.2. Assessment instruments/questionnaires The patients were clinically assessed using assessment instruments that included both neurologist-administered rating scales and self-administered questionnaires. The neurologistadministered assessments included the modified Hoehn and Yahr Scale (HY) [9] to stage PD severity according to the patient’s best “on” state, the Unified Parkinson’s Disease Rating Scale (UPDRS) [10] and the Mini-Mental State Examination (MMSE) [11]. These examinations were all performed by a neurologist on the same day. The self-administered scales included the Snaith–Hamilton Pleasure scale (SHAPS) [12], the State–Trait Anxiety Inventory (STAI) [13], the Beck Depression Inventory (BDI) [14], an apathy scale (AS) [15] and the QOL instrument the 39-item Parkinson’s disease questionnaire (PDQ-39) [16]. The self-administered questionnaires were given in the same order to each patient. The patients were told to take as much time as they needed to answer these questionnaires in order to control for test-induced fatigue. Anhedonia was evaluated with the Japanese version of the SHAPS [16,17]. The SHAPS comprises 14 items covering four domains of pleasure experience and food/drink. Higher SHAPS scores represents a reduction in hedonic tone, with a cutoff score of 3 or more for anhedonia and a normal hedonic tone being defined as a score of 0. The SHAPS has recently become widely used for assessing anhedonia in PD patients. The Japanese version of the SHAPS has been shown to have good validity, test–retest reliability and internal consistency [17]. Anxiety was evaluated with the Japanese version of the STAI [18]. The STAI consists of two scales designed to differentiate between the temporary condition of the state of anxiety (Form X1) and the more general and long-standing quality of trait anxiety (Form X-2). Each item on the STAI scale is scored on four levels of anxiety intensity from 1 = “not at all” to 4 = “very much,” with a sum score between 20 and 80. Twenty items are designed to record the presence of anxiety symptoms, while the other items are scored to record the absence of anxiety symptoms. The latter are inverted for the purpose of calculating the sum score. The cutoff score for the STAI was set at 41 for males and 42 for females [18]. The STAI has been used in many studies of PD patients. These studies indicate that the instrument is appropriate for use in screening anxiety, studying biological markers and as an outcome measure [19], although further validation such studies in PD populations is still needed. Depression was evaluated using the Japanese version of the BDI Second Edition (BDI-II) [19], which is widely used in Japan to assess depression and is reported to have excellent reliability and validity. The BDI-II is a 21-item scale. The items are rated from 0 to 3, with a sum score between 0 and 63. The resulting scores are added across the items to yield an overall measure of the intensity of depressive symptomatology. The cutoff score for the BDI-II was set at 14, as is standard in Japan and also indicated in the original version [20]. The Japanese version [21] of Starkstein’s Apathy Scale was used to assess apathy. This scale was chosen based on a review of apathy and anhedonia rating scales in patients with PD conducted by
2525
Leentjens et al. [19] in which they recommended only this scale be used to assess apathy in PD patients. The cut off score was set at 16 rather than 14 as indicated in the original scale because the Japanese version demonstrates high reliability (sensitivity: 81.3%) with a cutoff score of 16 [21]. The Japanese version [22] of the PDQ-39, a 39-item questionnaire, was used for the QOL assessment. The PDQ-39 is a widely used disease-specific health-related QOL measure that was translated and validated in Japan by Kohmoto et al. [22]. The PDQ-39 contains 39 questions, each with five different answer options, from which eight subscores (mobility, activities of daily living [ADLs], emotional well-being, stigma, social support, cognition, communication and bodily discomfort) and one summary index (SI) can be calculated. The maximum score of 100 indicates the worst quality of life. 2.3. Statistical analysis Group differences were analyzed using nonparametric tests (Mann–Whitney U-tests). Spearman’s rank correlation coefficients were used to assess the degree of correlation between the SHAPS scores and the following variables: age, age at onset, disease duration, HY stage, UPDRS total and individual subscale scores, the MMSE score, the BDI-II score, the STAI score, the AS score, the levodopa equivalent dose (LED) and the PDQ-39 score. The daily LED was calculated as [23]: (regular levodopa dose × 1) + (pramipexole dose × 67) + (ropinirole dose × 16.67) + (pergolide dose × 100) + (bromocriptine dose × 10) + (regular levodopa dose × 0.25 if taking entacapone). A multivariate analysis using stepwise linear regression was performed to determine the factors associated with the SHAPS score. The SHAPS score was considered to be a dependent variable, and variables found to be significantly associated with the SHAPS score on the basis of Spearman’s rank correlations were included as independent (explanatory) variables. All data were analyzed using the Dr. SPSS software package (SPSS version 11.0). Statistical significance was set at P < 0.05. 3. Results Table 1 shows the clinical characteristics of the 117 PD study patients. There were no differences in the clinical variables between males and females, although this series included a larger number of females. Anhedonia (SHAPS score ≥ 3) was present in 18 of the 117 patients (15%), depression was present in 66 patients (56%), apathy was present in 60 patients (51%) and anxiety (Trait) in 64 patients (55%). Anhedonia coexisted with depression in 16 patients (14%), with apathy in 14 patients (12%) and with anxiety in 17 patients (15%). Table 2 shows the relationships between the SHAPS scores and several clinical variables. The SHAPS scores exhibited significant correlations with HY (rs = 0.269, P = 0.004), UPDRS I (rs = 0.349, P < 0.001), IVB (rs = 0.248, P = 0.007), IVC (rs = 0.291, P = 0.002), the UPDRS total score (rs = 0.198, P = 0.033), BDI-II (rs = 0.564, P < 0.001), AS (rs = 0.435, P < 0.001) and the STAI State (rs = 0.215, P = 0.021) and STAI Trait scores (rs = 0.362, P < 0.001). The SHAPS scores did not show any significant associations with gender, age, age at onset, duration of illness or LED. There were no significant differences in the mean SHAPS score between the 34 patients taking pramipexole (0.9 ± 1.6; mean ± SD) and those patients not taking pramipexole (1.1 ± 1.9). Multivariate analyses using stepwise regression were performed to determine which factors contribute to the SHAPS scores. Variables significantly associated with the SHAPS scores were
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K. Matsui et al. / Clinical Neurology and Neurosurgery 115 (2013) 2524–2527
Table 1 Characteristics of the Study Patients. Total (n = 117)
Male (n = 46)
Female (n = 71)
Mean
Mean
Mean
Age (yr) 69.4 61.4 Age at onset (yr) 8.3 Duration of disease (yr) 2.8 Hoehn–Yahr stage UPDRS I (mentation) 2.3 UPDRS II (ADL) 7.8 18.9 UPDRS III (motor) UPDRS IV (complications) 0.7 A dyskinesia 1.9 B motor fluctuation C othersa 0.7 UPDRS total 34.1 MMSE 27.6 1.0 SHAPS 15.8 BDI-II STAI 43.2 Form X-1 43.9 Form X-2 16.1 AS l-Dopa equivalent dose 450.2 PDQ-39 42.0 Mobility 35.5 ADL 37.3 Emotional well-being 23.9 Stigma 21.2 Social support Cognition 34.1 20.5 Communication Bodily discomfort 31.2 30.8 Summary index
SD
SD
SD
9.1 10.2 5.0 0.8 2.4 7.7 14.2
69.1 60.3 8.8 2.9 2.6 8.6 18.2
8.8 9.8 5.5 0.8 2.9 8.3 12.0
69.7 62.1 7.9 2.7 2.0 7.3 19.3
9.3 10.4 4.6 0.8 2.0 7.2 15.5
1.5 1.8 0.9 24.0 2.6 1.6 9.7
0.9 1.9 0.6 33.4 27.4 1.2 15.9
1.8 1.7 0.9 23.7 2.4 1.8 10.0
0.6 1.9 0.8 34.6 27.8 0.8 15.7
1.4 1.8 1.0 24.2 2.8 1.4 10.0
11.2 11.1 7.4 224.3
44.3 44.9 16.0 486.0
11.5 11.6 7.3 235.2
42.5 43.2 16.2 426.7
10.8 10.7 7.5 215.4
29.0 29.2 25.0 21.6 28.1 20.9 21.6 25.6 18.7
37.6 38.7 34.1 23.6 19.6 37.0 23.2 28.6 30.2
30.8 30.8 22.6 20.8 28.7 20.8 22.7 24.9 20.3
44.8 33.6 39.3 24.2 22.3 32.3 18.7 32.3 31.3
27.7 28.2 26.3 22.2 27.8 20.8 20.8 25.9 17.7
Notes: ADL, activity of daily living; UPDRS, Unified Parkinson’s disease rating scale; MMSE, Mini-Mental State Examination; SHAPS, Snaith–Hamilton pleasure scale; BDI-II, Beck Depression Inventory–II; STAI, State–Trait Anxiety Inventory; AS, Apathy Scale; PDQ-39 SI, Parkinson’s disease questionnaire. a Anorexia, nausea, vomiting, sleep disturbance, symptomatic orthostasis.
entered as independent variables. The stepwise linear regression model revealed that the BDI-II, and STAI Trait scores (P = 0.010) significantly influenced the SHAPS scores (F = 18.501; P < 0.001) (Table 3). A significant correlation was noted between the SHAPS scores and the PDQ-39 SI (rs = 0.409, P < 0.001) (Table 4).
Table 2 Relationships between the SHAPS scores and clinical variables. Variables
rs
P
Gender Age Age at onset Duration of disease Hoehn–Yahr stage UPDRS I (mentation) UPDRS II (ADL) UPDRS III (motor) UPDRS IV (complications) A dyskinesia B motor fluctuation C others UPDRS total MMSE BDI-II AS STAI State Trait l-Dopa equivalent dose
−0.086 0 051 −0.050 0.066 0.269 0.349 0.141 0.172
0.367 0.584 0.593 0.480 0.004 0.000 0.131 0.064
0.113 0.248 0.291 0.198 −0.032 0.564 0.435
0.226 0.007 0.002 0.033 0.734
