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Original Article
Neuropsychiatric Symptoms in Parkinson’s Disease Dementia Are Associated with Increased Caregiver Burden
Yoon-Sang Oh1, Ji E. Lee2, Phil Hyu Lee2, Joong-Seok Kim1
Journal of Movement Disorders 2015;8(1):26-32.
DOI: https://doi.org/10.14802/jmd.14019
Published online: January 13, 2015
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1Department of Neurology, College of Medicine, The Catholic University of Korea, Seoul, Korea

2Department of Neurology, Yonsei University College of Medicine, Seoul, Korea

Corresponding author: Joong-Seok Kim, MD, PhD, Department of Neurology, The Catholic University of Korea, Seoul St. Mary’s Hospital, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Korea/Tel: +82-2-2258-6078/Fax: +82-2-599-9686/E-mail: neuronet@catholic.ac.kr
• Received: July 24, 2014   • Revised: September 4, 2014   • Accepted: September 18, 2014

Copyright © 2015 The Korean Movement Disorder Society

  • Objective
    Neuropsychiatric symptoms are common in Parkinson’s disease dementia (PDD). Frequent and severe neuropsychiatric symptoms create high levels of distress for patients and caregivers, decreasing their quality of life. The aim of this study was to investigate neuropsychiatric symptoms that may contribute to increased caregiver burden in PDD patients.
  • Methods
    Forty-eight PDD patients were assessed using the 12-item Neuropsychiatric Inventory (NPI) to determine the frequency and severity of mental and behavioral problems. The Burden Interview and Caregiver Burden Inventory were used to evaluate caregiver burden.
  • Results
    All but one patient showed one or more neuropsychiatric symptoms. The three most frequent neuropsychiatric symptoms were apathy (70.8%) and anxiety (70.8%), followed by depression (68.7%). More severe neuropsychiatric symptoms were significantly correlated with increased caregiver burden. The domains of delusion, hallucination, agitation and aggression, anxiety, irritability and lability, and aberrant motor behavior were associated with caregiver stress. After controlling for age and other potential confounding variables, total NPI score was significantly associated with caregiver burden.
  • Conclusions
    The results of this study confirm that neuropsychiatric symptoms are frequent and severe in patients with PDD and are associated with increased caregiver distress. A detailed evaluation and management of neuropsychiatric symptoms in PDD patients appears necessary to improve patient quality of life and reduce caregiver burden.
Neuropsychiatric symptoms are frequently observed in Parkinson’s disease (PD), even during the early, untreated stage 1. PD patients with dementia show more frequent and severe neuropsychiatric symptoms than those without dementia [24]. In patients with Parkinson’s disease dementia (PDD), almost 90% present with at least one neuropsychiatric symptom, and 77% show two or more symptoms [3]. Olfactory dysfunction, a common non-motor symptom, has also been associated with an increased number of neuropsychiatric symptoms [5].
Caregivers are more distressed when PDD neuropsychiatric symptoms are more frequent and severe [2,3,6]. Neuropsychiatric symptoms are associated with reduced quality of life [7,8], difficulty in performing activities of daily living [9], increased admission to nursing homes [10], and increased mortality in nursing-home patients [11].
Dementia and mild cognitive impairment in PD have been shown to increase caregiver burden and decrease quality of life [12]. In addition, other factors, such as age, age of disease onset, duration of illness, and severity of motor symptoms, are known to be associated with caregiver distress [1315]. Furthermore, the caregiver’s age, gender, health status, and caregiving duration also influence their quality of life and stress [16]. Because many factors interact to independently or dependently influence caregiver burden and distress, this study asked whether neuropsychiatric and motor symptoms cause increased caregiver burden in the case of PDD. Neuropsychiatric symptoms and motor or cognitive dysfunction relating to caregiver burden were assessed using the Burden Interview (BI) and Caregiver Burden Inventory (CBI) [1720].
This study was approved by the ethics committee of Seoul St. Mary’s Hospital. Each patient provided written, informed consent prior to participating.
Forty-eight patients diagnosed with PDD at the movement disorder outpatient clinic of the university hospitals based on the UK Parkinson’s Disease Society Brain Bank clinical diagnostic criteria and the clinical diagnostic criteria for probable PDD were enrolled [21,22]. Clinical information included age, gender, disease duration, history of hypertension, diabetes mellitus, heart disease, dyslipidemia, and current medication. Data from complete physical and neurological examinations, laboratory tests, and brain magnetic resonance imaging were obtained. Patients 1) with a previous stroke or other neurological and psychiatric disorders, 2) atypical PD or secondary Parkinsonism or 3) secondary causes of dementia were excluded.
All patients were on anti-parkinsonian medications. The levodopa equivalent daily dose was calculated as follows: dose of levodopa plus dose of dopamine agonists multiplied by equivalents (= 1 × levodopa dose + 0.75 × controlled release dose + 0.33 × entacapone + 20 × ropinirole dose + 100 × pramipexole + 10 × selegiline + 1 × amantadine) [23]. When enrolled in this study, all patients had been diagnosed for the first time with dementia. No PD patient had ever taken anti-dementia drugs, antipsychotics, antidepressants or anxiolytics prior to this study.
Clinical evaluation
Information on memory problems and other subjective cognitive deficits was obtained from caregiver interviews.
To assess neuropsychiatric symptoms, the Neuropsychiatric Inventory (NPI) was used [24]. The NPI comprises sub-questions in 12 different categories covering four major neuropsychiatric symptom domains: mood, apathy, agitation, and psychosis. Symptom frequency was rated on a scale of 1 to 4, and severity was rated on a scale of 1 to 3. A composite score ranging from 1 to 12, defined as the product of frequency and severity, was calculated. In addition, NPI sub-scores for each patient were analyzed using five different clusters of neuropsychiatric symptoms: 1) few and mild neuropsychiatric symptoms (n = 19), 2) high scores on depression, anxiety, apathy and low scores on the other items (“mood” group, n = 9), 3) high scores on apathy and low scores on the remaining items including depression (“apathy” group, n = 7), 4) moderate or severe sub-scores on the majority of items including irritability and agitation items (“agitation” group, n = 11), and 5) high scores on hallucinations and delusions together with low scores on the majority of other items (“psychosis” group, n = 2) [25].
The general cognitive status and dementia severity were evaluated using the Korean version of the Mini-Mental State Examination (MMSE) and the Clinical Dementia Rating (CDR) scale and Global Deterioration Scale. Parkinsonian motor symptoms were evaluated using the Unified Parkinson’s Disease Rating Scale (UPDRS) part III and the modified Hoehn and Yahr (H&Y) scale when patients were on medications. All patients were divided into tremor-dominant and akinetic rigid-dominant groups based on previous methods [26].
Caregiver burden was evaluated using BI and CBI. BI is a 22-item questionnaire used to measure caregiver stress caused by patient disabilities [17]. Each item is scored from 0 to 4. Total score is calculated as the sum of all scores and ranges from 0 to 88. CBI is a 24-item multidimensional questionnaire comprised of 5 different subscales [1820] that quantify caregiver burden: 1) time-dependence burden: time spent on caregiving (items 1–5), 2) developmental burden: caregiver feelings during care (items 6–10), 3) physical burden: status of general health problems (items 11–14), 4) social burden: problems in the family and social life (items 15–19), and 5) emotional burden: negative feelings about the patient (items 20–24). Each individual item is scored from 0 to 4, the total score is the sum of all sub-scores and ranges from 0 to 96. The responder for these questionnaires was selected from one of the family members using the following criteria: 1) being a relative of the patient and older than 18 years; and 2) serving as the primary caregiver and with an intimate knowledge of the patient that developed over time.
Statistical analyses
Demographics were described using the mean, standard deviation (SD), number, and percentage. Correlation analyses were conducted to evaluate the relationship between neuropsychiatric symptoms, other motor and cognitive features, and caregiver burdens. Independent-sample t-tests were used to compare caregiver burdens and neuropsychiatric symptoms between tremor- and akinetic rigid-dominant groups. Burden differences among NPI clusters were also compared using a one-way analysis of variance. Multiple linear regression analyses were performed to evaluate the effect of associated variables on caregiver burden. A p value < 0.05 was considered significant. Statistical analyses were performed using SPSS software version 15.0 (SPSS Inc., Chicago, IL, USA).
Of the 48 patients, 28 were men and 20 women. Their mean age (± SD) was 74.7 ± 6.6 years and the mean duration of PD was 3.9 ± 4.4 years. Fourteen patients (29.2%) had diabetes, 21 (43.8%) had hypertension, 7 (14.6%) had heart disease, and 2 (4.2%) had an abnormal lipid profile. Eight patients were current smokers, 3 were ex-smokers, and 37 were non-smokers. The severity of parkinsonian motor and cognitive symptoms was as follows: mean UPDRS part III score, 28.1 ± 12.4; mean H&Y stage score, 2.4 ± 0.8; mean MMSE score, 19.8 ± 4.0; and mean CDR score, 1.1 ± 0.7 (Table 1). All patients were on anti-parkinsonian medications with levodopa only or with dopamine agonists, amantadine, entacapone or selegiline. The mean levodopa equivalent daily dose was 490.3 ± 318.6 mg.
With the exception of 1 patient, all presented with one or more neuropsychiatric symptoms. The most frequent neuropsychiatric symptoms were anxiety and apathy (70.8%), followed by depression (68.7%), nighttime behavior disorder (58.3%), and appetite change (47.9%). Delusion, hallucination, agitation and aggression, disinhibition, irritability and lability, and aberrant motor behavior were present in 20–40% of patients. Euphoria occurred relatively infrequently (8.3%).
The total NPI score did not differ between male and female patients (male vs. female = 24.4 ± 24.2 vs. 22.6 ± 24.3, p = 0.729), and we observed no associations with age (r = −0.004, p = 0.980), disease duration (r = 0.062, p = 0.678), levodopa equivalent daily dose (r = 0.032, p = 0.827) or MMSE score (r = 0.090, p = 0.542). However, the total NPI score did correlate with CDR (r = 0.444, p = 0.002), H&Y stage score (r = 0.326, p = 0.024), and UPDRS part III (r = 0.312, p = 0.031).
All caregivers reported mild to moderate burdens, ranging from 0 to 79 using BI (mean; 37.8 ± 22.2) and 3 to 87 using CBI scores (mean; 35.7 ± 23.0). The mean CBI sub-scale scores were: time-dependence burden, 13.0 ± 6.2; developmental burden, 7.6 ± 6.4; physical burden, 6.2 ± 5.1; social burden, 4.4 ± 4.0; and emotional burden, 4.5 ± 4.7.
Neuropsychiatric symptoms correlated significantly with greater caregiver burden (Table 2). Delusion, hallucination, agitation and aggression, anxiety, irritability and lability, and aberrant motor behavior were associated with greater caregiver stress (Table 2 and 3). For the NPI clusters, caregivers of groups with irritability, agitation and psychotic symptoms (clusters 4 and 5), reported more severe stress or burden (Table 4).
Increasing age, longer disease duration, and lower MMSE scores did not affect caregiver burden. Burden correlated with more severe motor symptoms and cognitive dysfunction quantified using UPDRS part III and H&Y stage scores and CDR. Caregiver burden tended to be greater for the akinetic rigid-dominant group, although there were no differences in neuropsychiatric symptoms between tremor-dominant and akinetic rigid-dominant groups with the exception of the apathy domain (Table 5).
Linear regression analyses revealed that NPI score associated independently with caregiver burden in patients with PDD, as measured using BI and CBI, regardless of age, gender, vascular risk factors, and motor and cognitive status (Table 6).
Parkinson’s disease dementia patients included in this study presented with frequently occurring neuropsychiatric symptoms. All but one patient showed at least one or more neuropsychiatric symptoms. The frequency and severity of neuropsychiatric symptoms were similar to previous studies [2,3]; the most frequent and severe symptoms were apathy, anxiety, and depression. In contrast, euphoria was the rarest symptom.
A number of demographics and factors were associated with increased caregiver burden. Parkinsonian motor-symptom status or dementia severity in patients was associated with greater caregiver distress. However, neither patient age nor disease duration increased neuropsychiatric symptoms or family burden. This finding may be because the patients in this study had relatively short durations of PD: (3.9 ± 4.4 years) compared with a previous study (10.9 ± 7.7 years);14 the shorter disease duration may cause selection bias, and it is therefore possible that the longer disease duration group was underrepresented.
Severe neuropsychiatric symptoms correlated with caregiver distress; caregivers reported greater burden as neuropsychiatric symptoms became more frequent and severe. Only euphoria, which was the most rare and mildest symptom, was not associated with caregiver burden. Both sub-items and scales for depression and anxiety (Beck Depression Inventory and Beck Anxiety Inventory) showed a borderline association between mood and caregiver burden. Psychotic symptoms, such as hallucination, delusion, and agitation or irritability, correlated with more-severe caregiver distress. After controlling for age and other potential confounding factors, total NPI score associated significantly with PDD caregiver burden. This finding is consistent with recent studies showing neuropsychiatric symptoms were associated with increased caregiver stress or nursing home placement [2732]. These data suggest that caregiving for PDD patients may impair psychological health due to fatigue and also deprive the caregiver of time to do activities that are desired and expected at that moment in life. Thus, the caregiver role may be characterized by perceived disruption-of-life expectations.
Neuropsychiatric symptoms were similar between Parkinsonian motor phenotype groups; however, the akinetic-rigid group showed higher NPI scores and more apathy. Caregiver burdens were marginally influenced by motor phenotype suggesting bradykinesia and rigidity were more stressful to caregivers than tremor symptoms.
This study has several strengths and weaknesses. The major strength was that both BI and CBI were used to estimate caregiver or family distress, which provided more precise and detailed results from a total of 46 items between these two assessments. In addition, PD patients diagnosed with dementia for the first time at enrollment were included. They had not taken any anxiolytics, antipsychotics, antidepressants, or anti-dementia drugs. Because these drugs improve symptoms, the total NPI score may have been reduced in patients using these medications. Several limitations were identified. First, all patients were taking anti-parkinsonian medications. Anti-parkinsonian medications are associated with behavioral disturbances and neuropsychiatric symptoms [33]. Hallucination and psychosis are frequent complications of anti-parkinsonian medications. However, a recent study showed that hallucination may correlate with cognitive decline rather than adverse dopaminergic events [34]. Other studies suggest that psychosis in PD patients results from multiple etiologies [35,36]. Moreover, the mean score and frequency of delusion and hallucination in this study were not very different from those of a previous study [3]. Second, this study was cross sectional. The frequency and severity of neuropsychiatric symptoms may not generalize to other populations; however, many cross-sectional studies have been performed and their outcomes accepted [24].
In conclusion, the results from this study confirm neuropsychiatric symptoms are frequent and severe in patients with PDD and that they are associated with increased caregiver distress. These data suggest that the detailed evaluation and management of neuropsychiatric symptoms in PDD patients may improve patient quality of life and reduced caregiver burden.
This research was supported by grants from Novartis Korea.

Conflicts of Interest

The authors have no financial conflicts of interest.

Table 1
Clinical and neuropsychological characteristics of patients
Age (yr) 74.7 ± 6.6
Sex, male (%) 28 (58.3)
Hypertension (%) 21 (43.8)
Diabetes mellitus (%) 14 (29.2)
Heart disease (%) 7 (14.6)
Dyslipidemia (%) 2 (4.2)
Current or ex-smoker (%) 11 (22.9)
Disease duration (yr) 3.9 ± 4.4
UPDRS part III 28.1 ± 12.4
Hoehn and Yahr stage 2.4 ± 0.8
MMSE 19.8 ± 4.0
CDR 1.1 ± 0.7
GDS 3.8 ± 0.9
Levodopa equivalent dose (mg) 490.3 ± 318.6
Neuropsychiatric Inventory 23.6 ± 24.0
 Delusion 1.2 ± 2.1
 Hallucination 1.2 ± 2.5
 Agitation and aggression 1.9 ± 3.3
 Depression and dysphoria 2.4 ± 3.0
 Anxiety 3.6 ± 4.4
 Euphoria 0.5 ± 1.9
 Apathy 3.4 ± 3.8
 Disinhibition 1.4 ± 2.9
 Irritability and lability 2.1 ± 3.4
 Aberrant motor behavior 1.7 ± 3.1
 Nighttime behavior disorder 2.6 ± 3.4
 Appetite change 1.8 ± 2.5
Beck Anxiety Inventory 39.8 ± 12.8
Beck Depression Inventory 19.4 ± 12.3
Burden Interview 37.8 ± 22.2
Caregiver Burden Inventory 35.7 ± 23.0
 Time-dependence burden 13.0 ± 6.2
 Developmental burden 7.6 ± 6.4
 Physical burden 6.2 ± 5.1
 Social burden 4.4 ± 4.0
 Emotional burden 4.5 ± 4.7

Data denoted the mean ± standard deviation or numbers with percentages in parenthesis. UPDRS: Unified Parkinson’s Disease Rating Scale, MMSE: Mini Mental Status Examination, CDR: Clinical Dementia Rating scale, GDS: Global Deterioration Scale.

Table 2
Correlation between caregiver burden and neuropsychiatric parameters
Variables Burden Interview Caregiver Burden Inventory
Age -0.121 (0.411) 0.100 (0.497)
Disease duration 0.077 (0.604) 0.132 (0.370)
UPDRS part III score 0.358 (0.012)* 0.285 (0.050)*
Hoehn and Yahr stage 0.327 (0.023)* 0.417 (0.003)
MMSE -0.011 (0.938) 0.085 (0.564)
CDR 0.515 (< 0.001) 0.421 (0.003)
GDS 0.341 (0.018)* 0.365 (0.011)*
Levodopa equivalent dose 0.098 (0.506) 0.085 (0.564)
Beck Anxiety Inventory 0.378 (0.008) 0.187 (0.203)
Beck Depression Inventory 0.294 (0.043)* 0.149 (0.313)
Neuropsychiatric Inventory 0.675 (< 0.001) 0.605 (< 0.001)
 Delusion 0.425 (0.001) 0.503 (< 0.001)
 Hallucination 0.435 (0.002) 0.367 (0.010)
 Agitation and aggression 0.472 (0.001) 0.454 (0.001)
 Depression and dysphoria 0.363 (0.011)* 0.203 (0.166)
 Anxiety 0.581 (< 0.001) 0.457 (0.001)
 Euphoria 0.013 (0.932) 0.196 (0.182)
 Apathy 0.409 (0.004) 0.195 (0.185)
 Disinhibition 0.510 (< 0.001) 0.447 (0.001)
 Irritability and lability 0.518 (< 0.001) 0.465 (0.001)
 Aberrant motor behavior 0.438 (0.002) 0.336 (0.020)*
 Nighttime behavior disorder 0.219 (0.135) 0.333 (0.021)*
 Appetite change 0.214 (0.144) 0.316 (0.029)*

Data denote r (p value) of the correlation.

* < 0.05,

< 0.01.

UPDRS: Unified Parkinson’s Disease Rating Scale, MMSE: Mini Mental Status Examination, CDR: Clinical Dementia Rating scale, GDS: Global Deterioration Scale.

Table 3
Correlation between CBI sub-score and neuropsychiatric parameters
Variables CBI time-dependent burden CBI developmental burden CBI physical burden CBI social burden CBI emotional burden
Delusion 0.487 (< 0.001) 0.520 (< 0.001) 0.426 (0.003) 0.404 (0.004) 0.371 (0.010)*
Hallucination 0.353 (0.014)* 0.372 (0.009) 0.239 (0.102) 0.288 (0.047)* 0.306 (0.034)*
Agitation and aggression 0.403 (0.005) 0.485 (< 0.001) 0.418 (0.003) 0.314 (0.030)* 0.409 (0.004)
Depression and dysphoria 0.107 (0.469) 0.271 (0.063) 0.099 (0.504) 0.275 (0.059) 0.155 (0.292)
Anxiety 0.433 (0.002) 0.486 (< 0.001) 0.405 (0.004) 0.454 (0.001) 0.320 (0.026)*
Euphoria 0.061 (0.679) 0.223 (0.128) 0.180 (0.220) 0.275 (0.059) 0.237 (0.105)
Apathy 0.285 (0.050)* 0.155 (0.292) 0.300 (0.039)* 0.067 (0.650) 0.088 (0.554)
Disinhibition 0.452 (0.001) 0.515 (< 0.001) 0.432 (0.002) 0.286 (0.049)* 0.323 (0.025)*
Irritability and lability 0.398 (0.005) 0.499 (< 0.001) 0.476 (0.001) 0.331 (0.022)* 0.409 (0.004)
Aberrant motor behavior 0.299 (0.039)* 0.417 (0.003) 0.293 (0.043)* 0.329 (0.022)* 0.277 (0.057)
Nighttime behavior disorder 0.261 (0.073) 0.300 (0.038)* 0.448 (0.001) 0.299 (0.039)* 0.269 (0.065)
Appetite change 0.277 (0.056) 0.320 (0.027)* 0.374 (0.009) 0.273 (0.061) 0.229 (0.118)

Data denote r (p value) of the correlation.

* < 0.05,

< 0.01.

CBI: Caregiver Burden Inventory.

Table 4
Comparisons of caregiver burdens among NPI clusters
Cluster 1 (n = 19) Cluster 2, 3 (n = 16) Cluster 4, 5 (n = 13) p Post-hoc tests
BI 25.6 ± 18.6 37.9 ± 17.6 55.5 ± 21.1 < 0.001 Cluster 4, 5 > cluster 1 = cluster 2, 3
CBI 25.9 ± 20.6 30.8 ± 18.0 56.0 ± 20.1 < 0.001 Cluster 4, 5 > cluster 1 = cluster 2, 3
 CBI time-dependence burden 10.5 ± 6.6 12.3 ± 5.8 17.4 ± 3.6 0.005 Cluster 4, 5 > cluster 1 = cluster 2, 3
 CBI developmental burden 4.8 ± 6.0 6.3 ± 5.0 13.2 ± 5.2 < 0.001 Cluster 4, 5 > cluster 1 = cluster 2, 3
 CBI physical burden 4.1 ± 4.6 5.7 ± 4.7 9.9 ± 4.6 0.004 Cluster 4, 5 > cluster 1 = cluster 2, 3
 CBI social burden 3.1 ± 3.2 3.5 ± 3.1 7.5 ± 4.7 0.003 Cluster 4, 5 > cluster 1 = cluster 2, 3
 CBI emotional burden 3.5 ± 3.9 3.0 ± 2.4 8.0 ± 6.2 0.005 Cluster 4, 5 > cluster 1 = cluster 2, 3

Data denote the mean ± standard deviation. Analyses were performed using one-way analysis of variance and LSD post-hoc tests were used for comparisons. BI: Burden Interview, CBI: Caregiver Burden Inventory, NPI: Neuropsychiatric Inventory.

Table 5
Comparison of caregiver burden and neuropsychiatric parameters based on Parkinsonian motor phenotype
Variables Tremor-dominant (n = 26) Akinetic rigid-dominant (n = 22) p value
Burden Interview 31.8 ± 20.9 44.9 ± 22.0 0.041*
Caregiver Burden Inventory 30.5 ± 20.7 41.8 ± 24.5 0.089
 Time-dependence burden 11.7 ± 6.6 14.5 ± 5.5 0.127
 Developmental burden 6.3 ± 6.1 9.0 ± 6.6 0.155
 Physical burden 5.4 ± 5.0 7.1 ± 5.2 0.244
 Social burden 3.5 ± 2.9 5.6 ± 4.9 0.082
 Emotional burden 3.6 ± 3.6 5.6 ± 5.6 0.155
Neuropsychiatric Inventory 19.7 ± 20.4 28.3 ± 27.4 0.218
 Delusion 1.2 ± 2.1 1.2 ± 2.2 0.987
 Hallucination 1.2 ± 2.7 1.1 ± 2.3 0.849
 Agitation and aggression 1.6 ± 3.2 2.1 ± 3.5 0.594
 Depression and dysphoria 1.8 ± 2.5 3.1 ± 3.5 0.173
 Anxiety 3.5 ± 4.2 3.8 ± 4.7 0.805
 Euphoria 0.3 ± 1.2 0.8 ± 2.5 0.366
 Apathy 1.9 ± 2.1 5.1 ± 4.7 0.007
 Disinhibition 1.1 ± 2.3 1.7 ± 3.5 0.475
 Irritability and lability 1.5 ± 2.7 2.8 ± 4.0 0.186
 Aberrant motor behavior 1.2 ± 2.4 2.3 ± 3.7 0.250
 Nighttime behavior disorder 2.6 ± 3.3 2.5 ± 3.6 0.909
 Appetite change 1.7 ± 2.4 1.8 ± 2.7 0.907

Data denote the mean ± standard deviation.

* < 0.05,

< 0.01.

Table 6
Associations of caregiver burden with demographics or neuropsychiatric variables based on linear regression analysis
Variables Burden Interview Caregiver Burden Inventory

B (SE) 95% CI B (SE) 95% CI
Age −0.570 (0.467) −1.522, 0.381 0.050 (0.446) −0.858, 0.958

Gender 2.927 (5.816) −0.896, 14.760 2.582 (5.550) −8.710, 13.874

Diabetes mellitus −3.136 (6.414) −16.185, 9.912 −7.954 (6.121) −20.407, 4.498

Hypertension 8.069 (6.184) −4.513, 20.651 8.661 (5.902) −3.346, 20.668

Heart disease −4.218 (8.257) −21.018, 12.582 −5.101 (7.880) −21.133, 10.931

Dyslipidemia 14.494 (13.579) −13.134, 42.121 15.639 (12.959) −10.726, 42.005

Disease duration 1.049 (0.703) −0.381, 2.479 1.449 (0.671) 0.084, 2.814*

Hoehn & Yahr stage 3.459 (3.876) −4.427, 11.345 6.963 (3.699) −0.563, 14.489

Levodopa equivalent dose 0.013 (0.010) −0.008, 0.033 0.010 (0.010) −0.010, 0.029

Beck Anxiety Inventory 0.071 (0.275) −0.487, 0.630 −0.143 (0.262) −0.696, 0.390

Beck Depression Inventory −0.170 (0.259) −0.698, 0.358 −0.305 (0.248) −0.809, 0.199

MMSE 0.814 (0.820) −0.853, 2.481 1.080 (0.782) −0.511, 2.671

CDR 1.488 (6.261) −11.250, 14.226 −3.936 (5.975) −16.092, 8.220

Neuropsychiatric Inventory 0.619 (0.151) 0.313, 0.926 0.758 (0.144) 0.466, 1.051

Data denote the coefficient B and standard error (SE) of the correlation.

* < 0.05,

< 0.01.

MMSE: Mini Mental Status Examination, CDR: Clinical Dementia Rating scale.

  • 1. Aarsland D, Brønnick K, Alves G, Tysnes OB, Pedersen KF, Ehrt U, et al. The spectrum of neuropsychiatric symptoms in patients with early untreated Parkinson’s disease. J Neurol Neurosurg Psychiatry 2009;80:928–930.ArticlePubMed
  • 2. Stella F, Banzato CE, Quagliato EM, Viana MA, Christofoletti G. Psychopathological features in patients with Parkinson’s disease and related caregivers’ burden. Int J Geriatr Psychiatry 2009;24:1158–1165.ArticlePubMed
  • 3. Aarsland D, Brønnick K, Ehrt U, De Deyn PP, Tekin S, Emre M, et al. Neuropsychiatric symptoms in patients with Parkinson’s disease and dementia: frequency, profile and associated care giver stress. J Neurol Neurosurg Psychiatry 2007;78:36–42.ArticlePubMedPMC
  • 4. Kulisevsky J, Pagonabarraga J, Pascual-Sedano B, García-Sánchez C, Gironell A. Trapecio Group Study. Prevalence and correlates of neuropsychiatric symptoms in Parkinson’s disease without dementia. Mov Disord 2008;23:1889–1896.ArticlePubMed
  • 5. Morley JF, Weintraub D, Mamikonyan E, Moberg PJ, Siderowf AD, Duda JE. Olfactory dysfunction is associated with neuropsychiatric manifestations in Parkinson’s disease. Mov Disord 2011;26:2051–2057.ArticlePubMedPMC
  • 6. Aarsland D, Larsen JP, Karlsen K, Lim NG, Tandberg E. Mental symptoms in Parkinson’s disease are important contributors to caregiver distress. Int J Geriatr Psychiatry 1999;14:866–874.ArticlePubMed
  • 7. Karlsen KH, Tandberg E, Arsland D, Larsen JP. Health related quality of life in Parkinson’s disease: a prospective longitudinal study. J Neurol Neurosurg Psychiatry 2000;69:584–589.ArticlePubMedPMC
  • 8. McKinlay A, Grace RC, Dalrymple-Alford JC, Anderson T, Fink J, Roger D. A profile of neuropsychiatric problems and their relationship to quality of life for Parkinson’s disease patients without dementia. Parkinsonism Relat Disord 2008;14:37–42.ArticlePubMed
  • 9. Weintraub D, Moberg PJ, Duda JE, Katz IR, Stern MB. Effect of psychiatric and other nonmotor symptoms on disability in Parkinson’s disease. J Am Geriatr Soc 2004;52:784–788.ArticlePubMed
  • 10. Aarsland D, Larsen JP, Tandberg E, Laake K. Predictors of nursing home placement in Parkinson’s disease: a population-based, prospective study. J Am Geriatr Soc 2000;48:938–942.ArticlePubMed
  • 11. Goetz CG, Stebbins GT. Mortality and hallucinations in nursing home patients with advanced Parkinson’s disease. Neurology 1995;45:669–671.ArticlePubMed
  • 12. Leroi I, McDonald K, Pantula H, Harbishettar V. Cognitive impairment in Parkinson disease: impact on quality of life, disability, and caregiver burden. J Geriatr Psychiatry Neurol 2012;25:208–214.ArticlePubMed
  • 13. Martínez-Martín P, Forjaz MJ, Frades-Payo B, Rusiñol AB, Fernández-García JM, Benito-León J, et al. Caregiver burden in Parkinson’s disease. Mov Disord 2007;22:924–931.quiz 1060. ArticlePubMed
  • 14. Schrag A, Hovris A, Morley D, Quinn N, Jahanshahi M. Caregiver-burden in parkinson’s disease is closely associated with psychiatric symptoms, falls, and disability. Parkinsonism Relat Disord 2006;12:35–41.ArticlePubMed
  • 15. Ozdilek B, Gunal DI. Motor and non-motor symptoms in Turkish patients with Parkinson’s disease affecting family caregiver burden and quality of life. J Neuropsychiatry Clin Neurosci 2012;24:478–483.ArticlePubMed
  • 16. Morley D, Dummett S, Peters M, Kelly L, Hewitson P, Dawson J, et al. Factors influencing quality of life in caregivers of people with Parkinson’s disease and implications for clinical guidelines. Parkinsons Dis 2012;2012:190901.ArticlePubMedPMC
  • 17. Zarit SH, Reever KE, Bach-Peterson J. Relatives of the impaired elderly: correlates of feelings of burden. Gerontologist 1980;20:649–655.ArticlePubMedPDF
  • 18. Caserta MS, Lund DA, Wright SD. Exploring the Caregiver Burden Inventory (CBI): further evidence for a multidimensional view of burden. Int J Aging Hum Dev 1996;43:21–34.ArticlePubMed
  • 19. Novak M, Guest C. Application of a multidimensional caregiver burden inventory. Gerontologist 1989;29:798–803.ArticlePubMedPDF
  • 20. Lai C, Luciani M, Morelli E, Galli F, Cappelluti R, Penco I, et al. Predictive role of different dimensions of burden for risk of complicated grief in caregivers of terminally ill patients. Am J Hosp Palliat Care 2014;31:189–193.ArticlePubMed
  • 21. Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 1988;51:745–752.ArticlePubMedPMC
  • 22. Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, et al. Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 2007;22:1689–1707.quiz 1837. ArticlePubMed
  • 23. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 2010;25:2649–2653.ArticlePubMed
  • 24. Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J. The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 1994;44:2308–2314.ArticlePubMed
  • 25. Bronnick K, Aarsland D, Larsen JP. Neuropsychiatric disturbances in Parkinson’s disease clusters in five groups with different prevalence of dementia. Acta Psychiatr Scand 2005;112:201–207.ArticlePubMed
  • 26. Lewis SJ, Foltynie T, Blackwell AD, Robbins TW, Owen AM, Barker RA. Heterogeneity of Parkinson’s disease in the early clinical stages using a data driven approach. J Neurol Neurosurg Psychiatry 2005;76:343–348.ArticlePubMedPMC
  • 27. Goetz CG, Stebbins GT. Risk factors for nursing home placement in advanced Parkinson’s disease. Neurology 1993;43:2227–2229.ArticlePubMed
  • 28. Comella CL, Nardine TM, Diederich NJ, Stebbins GT. Sleep-related violence, injury, and REM sleep behavior disorder in Parkinson’s disease. Neurology 1998;51:526–529.ArticlePubMed
  • 29. Aarsland D, Alves G, Larsen JP. Disorders of motivation, sexual conduct, and sleep in Parkinson’s disease. Adv Neurol 2005;96:56–64.PubMed
  • 30. Leroi I, Harbishettar V, Andrews M, McDonald K, Byrne EJ, Burns A. Carer burden in apathy and impulse control disorders in Parkinson’s disease. Int J Geriatr Psychiatry 2012;27:160–166.ArticlePubMed
  • 31. Global Parkinson’s Disease Survey Steering Committee. Factors impacting on quality of life in Parkinson’s disease: results from an international survey. Mov Disord 2002;17:60–67.ArticlePubMedPDF
  • 32. Leiknes I, Tysnes OB, Aarsland D, Larsen JP. Caregiver distress associated with neuropsychiatric problems in patients with early Parkinson’s disease: the Norwegian ParkWest study. Acta Neurol Scand 2010;122:418–424.ArticlePubMed
  • 33. Burn DJ, Tröster AI. Neuropsychiatric complications of medical and surgical therapies for Parkinson’s disease. J Geriatr Psychiatry Neurol 2004;17:172–180.ArticlePubMed
  • 34. Wada-Isoe K, Ohta K, Imamura K, Kitayama M, Nomura T, Yasui K, et al. Assessment of hallucinations in Parkinson’s disease using a novel scale. Acta Neurol Scand 2008;117:35–40.ArticlePubMed
  • 35. Wint DP, Okun MS, Fernandez HH. Psychosis in Parkinson’s disease. J Geriatr Psychiatry Neurol 2004;17:127–136.ArticlePubMed
  • 36. Weintraub D, Hurtig HI. Presentation and management of psychosis in Parkinson’s disease and dementia with Lewy bodies. Am J Psychiatry 2007;164:1491–1498.ArticlePubMedPMC

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    JMD : Journal of Movement Disorders