Neuropsychiatric Symptoms and Caregiver's Burden in Parkinson's Disease Patients in a Tertiary Care Teaching Hospital in South India: A Cross-Sectional Study
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.333437
Source of Support: None, Conflict of Interest: None
Keywords: Activities of daily living, caregiver burden, caregivers, cognitive dysfunction, cognitive impairment, depressive disorder, neuropsychiatric symptoms, Parkinson disease, psychological burnout
Parkinson's disease (PD) over the years results in progressive motor and non-motor symptoms leading to progressive handicap and disability, often leading to the need for caregiver assistance. Neuropsychiatric symptoms (NPS) as a non-motor phenomenon are more frequent in those PD patients with dementia (PDD), which occurs in up to 60% of patients with PD. NPS contributes to poor quality of life for patients, and increased need for admission to a nursing home. Caregiving is a hugely demanding activity, often resulting in caregiver burden (CB). NPS, in particular, contribute to caregiver distress, leading to increased CB., There are very few reports from India on the profile of NPS in patients living with PD and its effects on CB.,,, This study aims to outline the various NPS in PD patients and study its association with the CB.
This is a cross-sectional study on 104 consecutive patients with PD who have an informal caregiver attending the Movement Disorder Clinic, Department of Neurology, Government Medical College Thiruvananthapuram, from March 1, 2018 to August 31, 2018. Approval from the Institutional Human Ethics Committee and informed consent from the patients/caregivers were obtained for the study. PD was diagnosed using the UK Parkinson's Disease Society Brain Bank criteria. The baseline clinical features, socio-demographic characteristics, PD disease stage, and PD motor severity were measured. In addition to the baseline socioeconomic and demographic data, Montreal Cognitive Assessment scale (MoCA), Everyday Abilities Scale for India (EASI), and REM sleep Behavior Disorder Screening Questionnaire (RBDSQ) were administered to PD patients to screen for cognition, disability and REM sleep behavior disorders, respectively. A neurologist categorized the cognitive status of PD patients as healthy, mild cognitive impairment, and dementia. EASI consists of 12 questions to check the activity of daily living (ADL) and offers a rapid assessment of the functional state of the patient. RBDSQ questionnaire reflects the presence or absence of REM sleep behavioral disorder with a cutoff score of five.
The NPS in PD patients was estimated using the Neuro-Psychiatric Inventory (NPI-12 item questionnaire) administered to the caregivers. The Neuro-Psychiatric Inventory (NPI) assessed the neuropsychiatric disturbances of the patient under 12 domains. Each domain's screening questions are followed by estimation of frequency (rated on a scale of one to four) and severity (rated on a scale of one to three). The frequency and severity product gives the total score, ranging from 1 to 12 for each NPS (maximum overall score: 144). NPI has established validity and reliability.,
The CB was estimated using the modified Zarit Caregiver Burden Inventory (ZBI). Modified ZBI is a 22-item questionnaire administered to caregivers, using a five-point Likert scale from zero (never) to four (always). ZBI aims to assess the patient's disease or disability's impact on the caregiver's physical, emotional, social, and financial situation. The sum of the individual items' scores gives the total score (Maximum score: 88). A higher score reflects a higher burden.
The data collected were anonymized, and statistical analysis was done using SPSS 16.0 (Statistical Package for Social Sciences, SPSS Inc). Appropriate summary statistics (mean [SD], median [IQR], and proportion) were used to describe the baseline data (demographic, socioeconomic and covariates, NPI score, and modified ZBI score). The variable scores for NPI score and modified ZBI score were analyzed as continuous variables as well as categorized (present or absent) using predefined cutoff. Pearson's correlation coefficients were used to analyze the relationship between NPS and ZBI. The difference in the mean scores of the NPI and ZBI among various categories of the covariates were estimated using the t-test or ANOVA using the respective scores and category. We quantified the proportion of NPS as a percentage. The CB was measured in mean (SD) using the modified ZBI. Univariate linear regression was done between the risk factor (NPS assessed by NPI score) and the outcome of interest (CB assessed by modified ZBI score). Multivariate linear regression was done to look at the association between the NPI score and the modified ZBI score adjusting for potential confounders/covariates. All P values were two-tailed, and P < 0.05 was considered statistically significant.
There were a total of 104 patients and caregivers enrolled in the study. The baseline data are presented in [Table 1]. Forty-three percent of the PD patients were in the ages between 61 and 70 years, 25% between the ages of 51 and 60 years, 16.6% between the ages of 41 and 50 years, 12.5% above the ages of 70 years, and 2.9% ≤40 years of age. Forty-six percent of patients with PD had 8 to 10 years of formal education, 23.1% had 1 to 4 years, 22.1% had 5 to 7 years, and 7.7% had ≥11 years of formal education. Only 1% were illiterate. Widows constituted 8.7%, separated 4.8%, and single 1.9%.
Most patients with PD (37.5%) were symptomatic for one to three years. The minimum duration of illness was half a year, and the maximum was 20 years. The majority of the PD patients belonged to modified Hoehn and Yahr stages 2.5 (53.8%) and three (40%). We had five patients (4.8%) with stage 4, one patient (0.96%) in stage 5, and two patients (1.9%) in stage 1.5. Based on Unified Parkinson's Disease Rating Scale (UPDRS) motor scores, 34.6% belonged to the mild category, 41.3% to the moderate category, and 24% to severe category. The minimum motor score was four, and the maximum was 91. One-third of patients (36.5%) were on levodopa for a duration of 1 to 3 years, 23.1% had duration 3 to 5 years, 22.1% had duration less than a year, 9.6% for 5 to 7 years, 6.7% for 7 to 9 years, 1.9% for more than nine years.
Forty patients (38.46%) showed no NPS, only one symptom in 21.1%, and multiple NPS in 40.44%: two symptoms in 15.4%, three symptoms in 11.5%, and more than three symptoms in 13.4%. The mean NPI total score was 6.37 ± 8.791 (ranged from 0 to a maximum value of 55). Most domains in NPI were affected [Table 2]. We did not observe the affection of euphoria and aberrant motor behavior domains. Univariate analysis showed an association of NPI score with age of the patient 70 years and over (P-value = 0.025), impaired cognition (MoCA score <15) (P-value = 0.023) and impaired instrumental activities of daily living (EASI score <3) (P-value = 0.001). There was no association of NPI total score with levodopa equivalent daily dose (LEDD), Hoehn and Yahr staging, and MDS-UPDRS part III score.
The primary caregivers were predominantly female; 80 (76.9%) out of the 104. Five (4.8%) primary caregivers were single, one (1%) widow, one (1%) separated, and 97 (93.3%) were married. Two (1.9%) of the primary caregivers were parents, 11 (10.6%) were siblings, 12 (11.5%) were sons-in-law/daughters-in-law, 26 (25%) were sons/daughters, and 53 (51%) were spouses. The mean ZBI score (SD) assessing the CB was 11.77 ± 12.177. There was little or no burden (ZBI 0–21) in 86 (82.7%) caregivers, mild to moderate burden (ZBI 21–40) among 14 (13.5%), moderate to severe burden (ZBI 41–60) in four (3.8%), and severe burden (ZBI 61–88) in none.
Association between Neuropsychiatric symptoms and Caregiver's burden
We found the total NPI score to correlate with the ZBI score (Pearson's correlation coefficient: +0.692) [Figure 1].
Risk factors for caregiver's burden
Univariate analysis showed ZBI score of caregivers to be associated with UPDRS score (P- value = 0.001), EASI score (P-value = 0.001), and RBDSQ score (P-value = 0.025), of patients with PD, years of caregiving (P-value = 0.001), and hours of caregiving per day (P -value = 0.001). Linear regression showed NPS (P-value = 0.001), EASI score (P-value = 0.038) and years of caregiving (P-value = 0.001) to be independent risk factors for CB [Table 3].
This study on 104 patients attending the movement disorders outpatient clinic of a tertiary care centre confirms that NPS is associated with CB. Most of our patients were ambulant (median modified Hoehn and Yahr 2.5) with normal cognition (75%). The prevalence and profile of NPS were consistent with existing literature., Depression was the commonest NPS. Similar to our findings, others have shown that NPS was associated with impaired cognition.,, Our study showed that NPS, as measured by the total NPI score correlated with the EASI, which assessed the instrumental activities of daily living.
All the patients with PD in this study had informal caregivers, half of them were spouses, and a quarter were sons or daughters. Some of the caregivers perceived mild to moderate burden (13.5%) and moderate to severe (3.8%) CB. The mean score of ZBI (11.77 ± 12.177) was found to be low when compared with a mean score by Pablo Martinez-martin et al. (21.87 ± 16.59) and Daniel Grun et al. (25.8 ± 17.1)., More significant CB was associated with NPS, affection of instrumental activities of daily living, and long years of caregiving. CB is more in patients with NPS, as recorded by Stella et al. and Martinez-Martin et al., EASI was found to be an independent risk factor for CB, which is similar to the observations by Edwards et al. Martinez-Martin et al. and Carod-Artal et al., showed cognitive impairment to increase CB contradictory to our observation which is supported by Grün et al. In a similar study from India, UPDRS motor scores were associated with CB even though we could not replicate it. RBD was found to be a risk factor in univariate but not multivariate analysis. Other researchers highlighted sleep-related disturbances affecting caregiving commitment., This could be explained by the increased nocturnal care given to the patient by the caregiver. Hours of caregiving was not a risk factor in the current study but correlated with the CB in another study.
The current study has its weakness in being a cross-sectional study. Therefore, a well-defined longitudinal study methodology with a larger sample size will improve the research findings' power. Since our samples were all ambulatory patients, fewer in the advanced stages of diseases (Hoehn and Yahr 4,5) might have reduced the overall rate of NPS and CB.
This study highlights the need to carry out a complete neuropsychiatric assessment of PD patients in clinical practice and motor symptoms. Since around one-third of the PD patients experience cognitive impairment, it should be identified early and managed by pharmacological and nonpharmacological strategies. Moreover, we recommend that the mental health of caregivers of chronically ill patients should be considered, and better supportive measures should be taken to alleviate the burden.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
[Table 1], [Table 2], [Table 3]