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Copyright 2010 The Authors Journal compilation 2010 Blackwell Munksgaard
Acta Neurol Scand 2010: 122: 418–424 DOI: 10.1111/j.1600-0404.2010.01332.x
ACTA NEUROLOGICA SCANDINAVICA
Caregiver distress associated with neuropsychiatric problems in patients with early ParkinsonÕs disease: the Norwegian ParkWest study Leiknes I, Tysnes O-B, Aarsland D, Larsen JP. Caregiver distress associated with neuropsychiatric problems in patients with early ParkinsonÕs disease: the Norwegian ParkWest study. Acta Neurol Scand: 2010: 122: 418–424. 2010 The Authors Journal compilation 2010 Blackwell Munksgaard. Objectives – We investigated caregiver distress associated with neuropsychiatric problems in patients with newly diagnosed ParkinsonÕs disease (PD). Materials and methods – Persons who were next of kins of 198 patients and 168 healthy individuals completed the Neuropsychiatric Inventory Caregiver Distress Scale. Results – Even at the time of diagnosis PD has a considerable impact on the next of kinsÕ experience of distress. Nearly 50% reported distress, significantly more than in the control group, and more than one-quarter reported moderate severe distress. Except the more rarely reported neuropsychiatric symptoms, apathy was the symptom that most frequently caused caregiver distress in PD patientÕs next of kin (94.5%), followed by depression (88.2%), anxiety (86.2%) and irritability (83.3%). Conclusions – The study underlines the importance of focusing on neuropsychiatric aspects in patients and associated caregiver distress even in early PD management.
Introduction
Caring for a person suffering from ParkinsonÕs disease (PD) may be associated with distress for the caregiver. A variety of variables like the caregiverÕs relation to the care recipients (1, 2), their mood and coping (3), time spent on providing care (4) and family income (2, 5), in addition to the patientÕs situation contribute to the total burden in PD caregivers. PD is a chronic neurodegenerative disease that affects the patientÕs health, both physically and mentally. The progression of the disease may cause disability and increasing need for caregiver support and assistance with activities of daily living (ADL). Previous research concerning caregiving in PD shows conflicting results. Caregiver burden seems however to be closely associated with diseaserelated factors like disease severity (6, 7), the patientÕs functional status and disability (3, 8–10) 418
I. Leiknes1, O.-B. Tysnes2,3, D. Aarsland1,3,4, J. P. Larsen1,3,5 1 The Norwegian Centre for Movement Disorders, Stavanger University Hospital, Stavanger, Norway; 2 Department of Neurology, Haukeland University Hospital, Bergen, Norway; 3School of Medicine, University of Bergen, Bergen, Norway; 4Department of Psychiatry, Stavanger University Hospital, Stavanger, Norway; 5Department of Neurology, Stavanger University Hospital, Stavanger, Norway
Key words: caregivers; Neuropsychiatric Inventory Caregiver Distress Scale; neuropsychiatric symptoms; next of kin; ParkinsonÕs disease Ingrid Leiknes, The Norwegian Centre for Movement Disorders, Stavanger University Hospital, PO Box 8100, 4068 Stavanger, Norway Tel.: 0047 51515601 Fax: 0047 51515515 e-mail: [email protected] Accepted for publication January 5, 2010
and psychiatric symptoms (1, 7, 10). Some studies have found that the ability of the person with PD to perform ADL was the strongest single predictor of the overall caregiver burden (2, 8). Unlike, Aarsland et al. (1) found that the patientÕs mental symptoms had the strongest impact on distress. This finding has been supported by more recent studies (4, 7, 11–13). Previous studies have examined caregiver distress associated with neuropsychiatric problems in clinicbased patient populations with more advanced disease (1, 14, 15). Psychiatric symptomsÕ impact on caregiver distress in the early phase of the disease has received less attention. The aim of this study was to explore distress associated with neuropsychiatric symptoms in persons who were next of kins of patients with newly diagnosed PD. This study is part of the Norwegian ParkWest study, a multicentre population-based longitudinal cohort study of the incidence and prognosis of patients with PD.
Caregiver distress in early ParkinsonÕs disease Burden is in the caregiver literature defined as the extent to which caregivers perceive that their health, social life and financial status are suffering because of their caregiving experience (16). However, as the focus of this study is caregiver distress at the time of diagnosis, it is not expected that the feelings of burden generated by the demands of caregiving, has introduced major limitation on next of kinsÕ social activities and financial situation. This led us to use the Neuropsychiatric Inventory (NPI) Caregiver Distress Scale which assesses the emotional caregiver distress associated with the mental health status of the patients.
Materials and methods Patients and controls
All patients within four counties of western and southern Norway, diagnosed with incident PD according to acknowledged criteria (17) in the period between November 2004 and August 2006, were invited to participate in the Norwegian ParkWest study. A total of 212 patients were included. In addition, 205 individuals were recruited to serve as control subjects. Most of them were spouses or friends of the patients. The rest were unrelated persons from the study area. Control subjects should not have Parkinsonism and should be able to perform the baseline examination. The patients and controls gave their written informed consent to participate in the study. The study was approved by the Regional Ethics Committee, the University of Bergen. The characteristics of the PD cohort have been reported elsewhere (18). Next of kins
Each patient and control subject was asked to have one of their next of kin interviewed as a part of the data collection in the ParkWest study. To serve as an informant, the next of kin had to see the patient ⁄ control on a regular basis, at least once a week, and be a reasonably good observer of the patientÕs behaviour. A total of 193 patients and 198 controls had a next of kin who volunteered participate in the study. Data collection
Caregiver distress – To explore caregiver distress, we used the NPI Caregiver Distress Scale. NPI was developed to assess psychopathology and caregiver distress in patients with dementia (19), but has also been used in several studies of neuropsychiatric
disturbances and caregiver distress in patients with PD (14, 15, 20). The NPI is based on a structured interview with a caregiver who is familiar with the patientÕs behaviour. It assesses 12 behavioural domains and caregiver distress related to each of the domains. The 12 neuropsychiatric domains are: delusions, hallucinations, agitation, depression, anxiety, euphoria, apathy, disinhibition, irritability, aberrant motor behaviour, sleep disturbance and appetite disturbance. The caregivers are asked about behaviours that differed from the patientÕs usual behaviour and had occurred during the past 4 weeks. Each domain has one screening question. A negative answer to the screening question completes the examination of that domain. A positive answer to the screening question results in further exploration of the domain with seven or eight subquestions. Then the caregivers are asked to rate the level of emotional distress experienced with each of the 12 neuropsychiatric domains on a six-point scale from 0 (no distress) to 5 (very or extreme distress). The NPI Caregiver Distress Scale has been proven to be a reliable and valid measure of subjective caregiver distress in relation to neuropsychiatric symptoms (21) and with high reliability in PD (22). To obtain standardization and a high quality in the assessments the interviewer received comprehensive training in assessment procedures. The next of kins were interviewed at the outpatient clinic or by telephone. The validity of using telephone interview has been established (23). Neurological and neuropsychiatric examination – A neurologist evaluated the patientÕs severity of Parkinsonism and disability by the Unified ParkinsonÕs Disease Rating Scale (UPDRS II ADL subscale and UPDRS III motor subscale; 24) including the modified Hoehn & Yahr staging (25) and the Schwab & England scale (26). A trained study nurse administered the NPI according to the aforedescribed guidelines. Statistical analysis
Data were analysed using the SPSS program (version 15.0). Descriptive statistics were used to show the frequencies (%) of caregiver distress scores. SpearmanÕs rank order correlation was used to calculate the strength of the relationship between patientsÕ disease severity and caregiver distress scores. Differences between groups were analysed using Mann–Whitney U-test for nonnormally distributed continuous variables and chi-square test for categorical variables. A value of P < 0.05 was considered significant. 419
Leiknes et al.
Numbers represent mean scores (ranges) or number of patients. UPDRS, Unified ParkinsonÕs Disease Rating scale; ADL, activities of daily living.
more NPI symptoms (Table 3). More NPI symptoms were associated with caregiver distress in female next of kins in the patient group (P = 0.05). Fifty-three (56.4%) of the PD patientsÕ next of kin (77.4% women and 22.6% men) with non-zero distress scores, reported neuropsychiatric symptoms to be causing at least moderately severe distress, that is, a score of ‡3 (Table 4). This is 28% of all PD patientsÕ next of kins in the study. There was a positive correlation between the patientsÕ disease severity scores (UPDRS motor and ADL subscales, Hoehn & Yahr and Schwab & England), and the next of kinsÕ number of NPI scores associated with distress (P < 0.05), but there was no significant correlation between the patientsÕ disease severity scores and the caregiver distress scores of at least moderate severity (‡3). In the control group, 15.5% of the next of kins reported distress on the NPI Caregiver Distress Scale (Table 3). Distress for only one symptom was scored by 13.1%. Of these, 6% only reported neuropsychiatric symptoms to be causing at least moderately severe distress. The frequency of caregiver distress, caregiver distress with a clinically significant severity (‡3) and the number of symptoms associated with caregiver distress differed significantly between PD patientsÕ next of kins and the control group (all Ps < 0.001). Table 4 shows the frequency of caregiver distress in relation to NPI symptoms. Depression was the most frequently reported NPI item giving caregiver distress. Exactly, 31.7% of next of kins experienced distress related to depression among patients. This was followed by apathy (27.5%), anxiety (13.2%), sleep disturbance and disturbance in appetite (10.6% each) and irritability (7.9%). Delusion, agitation, disinhibition and aberrant motor behaviour were uncommon in patients although they were always associated with distress. Among the more frequently reported neuropsychiatric symptoms of clinical importance, apathy was the
Table 2 Gender and relation of next of kin of patients with ParkinsonÕs disease (PD) and controls
Table 3 Frequency of Neuropsychiatric Inventory (NPI) symptoms in patients with ParkinsonÕs disease (PD) and controls and associated caregiver distress scores
Results
A total of 189 patients had a next of kin who completed the NPI Caregiver Distress Scale without missing data and were thus included in the present study. For the purpose of this study, all patients and control subjects in the ParkWest study were matched for age and sex. A total of 168 control subjects and their next of kins were thus included. Mean age was 67.8 years (range: 88.1– 42.3) for the patients and 67.3 (range: 84.5–39.4) for the controls; 59.8% of the patients and 60.7% in the control group were men. Mean time from motor onset to baseline examination was 2.3 years (range: 10.0–0.4; 2.6 for men and 2.0 for women). PatientsÕ disease severity scores are presented in Table 1. The majority of next of kins in both groups were spouses, followed by daughters and sons. Most next of kins (70.9% in the PD patient group and 64.3% in the control group) were women (Table 2). Caregiver distress related to neuropsychiatric problems was assessed with the NPI Caregiver Distress Scale. Ninety-four next of kins (49.8%) of the patients with PD reported distress on this scale. Of these were 77.7% women and 22.3% men. One NPI symptom was scored by 19.6%, 12.2% scored for two symptoms and 18% scored for three or Table 1 PatientsÕ motor symptoms, functional impairment and use of antiParkinsonian drugs
Patient characteristics
All patients, (n = 189)
UPDRS-ADL subscore UPDRS-motor subscore Hoehn & Yahr stage Schwab & England score Using anti-Parkinsonian drugs
9.0 23.2 1.9 87.9 5
Characteristics Gender Female Male Relation Spouse Daughter ⁄ son Other relative Others (friend, neighbour)
420
(25–1) (55–4) (4–1) (100–50)
Next of kin of PD patients, n = 189 (%)
Women, (n = 76)
Men, (n = 113)
9.0 21.6 1.9 87.2 1
9.0 24.3 1.9 88.4 4
Next of kin of controls, n = 168 (%)
NPI symptoms
134 (70.9) 55 (29.1)
108 (64.3) 60 (35.7)
Number
134 31 18 6
147 11 6 4
1 2 3 4 5 6
(70.9) (16.4) (9.5) (3.2)
(87.5) (6.5) (3.6) (2.4)
Patients, n = 189 (%) 42 22 23 12 5 6
(22.2) (11.6) (12.2) (6.3) (2.6) (3.2)
Caregiver distress scores
Controls, n = 168 (%) 26 8 0 2
(15.5) (4.8) (0.0) (1.2)
PD next of kin, n = 189 (%) 37 23 17 7 6 4
(19.6) (12.2) (9.0) (3.7) (3.2) (2.1)
Next of kin of controls, n = 168 (%) 22 2 1 1
(13.1) (1.2) (0.6) (0.6)
Caregiver distress in early ParkinsonÕs disease Table 4 Neuropsychiatric Inventory (NPI) symptoms in patients and related distress in next of kin of patients with ParkinsonÕs disease (PD) Caregiver distress score Number of patients with NPI symptoms, n = 189 (%)
NPI item Delusions Hallucinations Agitation ⁄ aggression Depression Anxiety Euphoria Apathy Disinhibition Irritability ⁄ lability Aberrant motor behaviour Sleep disturbance Appetite disturbance Total score
2 2 9 68 29 0 55 7 18 5 38 31 110
(1.1) (1.1) (4.8) (36.0) (15.3) (0.0) (29.1) (3.7) (9.5) (2.6) (20.1) (16.4) (58.2)
Number (%)* with distress 2 1 9 60 25 0 52 7 15 5 20 20 94
Percentage with distress**
(100.0) (50.0) (100.0) (88.2) (86.2) (0.0) (94.5) (100.0) (83.3) (100.0) (52.6) (64.5) (84.5)
Number (%)*** with score ‡3
1.1 0.5 4.8 31.7 13.2 0.0 27.5 3.7 7.9 2.6 10.6 10.6 49.8
2 0 5 33 17 0 27 4 7 0 7 8 53
Percentage with score ‡3**
(100.0) (0.0) (55.0) (68.0) (51.9) (0.0) (46.7) (57.1) (38.9) (0.0) (35.0) (40.0) (56.4)
1.1 0.0 2.6 17.5 9.0 0.0 14.3 2.1 3.7 0.0 3.7 4.2 28.0
*Percentage with non-zero distress scores of patients showing symptoms. **Percentage of all (n = 189). ***Percentage with scores ‡3 of next of kins with distress.
symptom that most often caused caregiver distress; 94.5% of the next of kins of patients with apathy experienced distress related to the symptom. This was followed by depression (88.2%), anxiety (86.2%) and irritability (83.3%). Of all present neuropsychiatric symptoms associated with caregiver distress only depression and apathy distress scores correlated positively with the patientÕs disease stage (Hoehn & Yahr; P < 0.05). Table 5 shows the proportion of caregiver distress according to gender and in spouses and nonspouses for the four NPI items causing most distress: depression, apathy, anxiety and irritability. In both spouses and non-spouses, the proportion of reported caregiver distress was high when
symptoms occurred (76.9% or more). Apathy is highly associated with caregiver distress (‡81.8) for both gender and both groups of next of kin. Female next of kins in general and female spouses show a non-significant trend to have more distress than male next of kins. Discussion
This study demonstrates that even at the time of diagnosis PD has a considerable impact on experienced distress by persons who are living close to the patients. Next of kins of patients with PD reported three times more frequently burden associated with neuropsychiatric symptoms as
Table 5 Number and proportion of next of kins with distress according to relationship to patients and to gender Number and proportion (%) with caregiver distress
NPI items
Patients with NPI symptoms, n = 189
All next of kins, n = 189
Depression
68
60
Anxiety
Apathy
Irritability
29
55
18
Category
n (%)*
Spouses Non-spouses
46 (90.2) 14 (82.4)
Spouses Non-spouses
18 (85.7) 7 (87.5)
Spouses Non-spouses
39 (97.5) 13 (86.7)
Spouses Non-spouses
10 (76.9) 5 (100.0)
25
P**
Category
0.302
All Spouses Non-spouses All Spouses Non-spouses All Spouses Non-spouses All Spouses Non-spouses
1.000
52
0.479
15
0.769
Women, n = 134 (%)* 46 35 11 20 16 4 41 32 9 13 9 4
(92.0) (94.6) (84.6) (90.9) (94.1) (80.0) (93.2) (97.0) (81.8) (92.9) (90.0) (100.0)
Men, n = 55 (%)* 14 11 3 5 2 3 11 7 4 2 1 1
(77.8) (78.6) (75.0) (71.4) (50.0) (100.0) (100.0) (100.0) (100.0) (50.0) (33.3) (100.0)
P** 0.302 0.324 0.734 0.35 0.094 0.376 0.155 0.063 0.734 0.238 0.281 1.00
*Percentage with non-zero distress scores of patients showing symptoms in the present group. **Chi-square test.
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Leiknes et al. compared with the control group and the severity of the reported burden was significantly higher in the PD group. In addition, 30.2% of the PD patientsÕ next of kins reported burden related to two or more items on the NPI, whereas this was the case for only 2.4% in the control group. These findings indicate that the management of patients with early PD should also include attention to the situation of their close relatives or friends. This is the first study focusing on caregiver burden at the time of PD diagnosis. Our findings are in line with the results of other studies with caregiver distress present at all stages of the disease, although in these studies the extent of burden was strongly associated with disease severity (3, 6, 7, 9). In our study, patientsÕ disease severity correlated with the number of neuropsychiatric symptoms associated with caregiver distress scores (P < 0.05), but did not cause more severe distress in the next of kin. This may be a result of the relative low impact of the disease of the patientsÕ functional ability in our population (mean Schwab & England was 87.9%). However, the reported burden in our study with early PD was relatively high compared with a recently published Spanish study of neuropsychiatric symptoms and caregiver distress among non-demented patients with more severe Parkinsonism (15). When a family member or another close friend is diagnosed with a chronic disease the situation may feel unsafe. Uncertainty concerning medical treatment, disease severity and a potentially incapacitating disease may influence the scores of experienced distress among close relatives and friends of patients with early disease. In a longitudinal study of caregiver burden in relation to PD, the burden was reduced from diagnosis to the 2-year follow-up examination (16). This suggests that next of kinsÕ ability to tolerate problem behaviour is reduced at the time of receiving the diagnosis. They may be more sensitive to the patientsÕ emotional behaviour and the presence of neuropsychiatric symptoms which could be a reason for higher scores on the caregiver distress scale in the early phase of the disease. Another possibility is that next of kins may change their strategies for coping with everyday problems as they develop experience and adaptation. In addition, cultural differences between countries may also influence experience of distress and explain the differences between studies. Except from the more rarely reported neuropsychiatric items delusion, agitation ⁄ aggression, disinhibition and aberrant motor behaviour, the symptoms most frequently associated with caregiver distress in this study were apathy, depression, 422
anxiety and irritability. In the aforementioned Spanish study (15), delusions, agitation, hallucination and depression were the NPI symptoms causing most burdens. This profile of distress is in agreement with that found in caregivers of demented patients with PD (14). These findings indicate that neuropsychiatric symptoms that impose distress in next of kins change over time when more severe neuropsychiatric symptoms develop. As the only neuropsychiatric caregiver distress scores that correlated with the patientsÕ disease stage were depression and apathy, it seems that close relatives or friends are more sensitive to this behaviour than to other neuropsychiatric problems in early PD. Although caregiver distress associated with depression was the most frequently reported item in our study, apathy was also frequent and even closer associated with burden. Its impact on caregiver burden has until recently received less attention than depression, although the important consequences of apathy on caregivers of both nondemented (27) and demented PD patients (14) have been shown. The loss of vitality and enjoyment related to apathy can make the relationship between the person with PD and the next of kin challenging and also force changes in the partnersÕ relationship and responsibility. Apathy and depression are closely related. Apathy as a syndrome may occur on its own or as a part of depression (28, 29). Furthermore, there is a lack of generally accepted diagnostic criteria for apathy as a syndrome (28) and this can make it difficult to differentiate these two syndromes in clinical research context. The NPI is one of several suggested rating scales of apathy (28) which gives an opportunity to separate between the two conditions as the NPI depression subscale excludes items related to apathy, and the apathy subscale has no items related to sadness (30), which is a typical symptom in depression. NPI may therefore also be a suitable instrument for assessing caregiver burden associated with depression and apathy. PD spouses did not differ significantly from nonspouses in reported caregiver burden in any of the assessed neuropsychiatric domains in this study. To our knowledge there are few studies analysing the impact of the next of kinÕs relation to the patient when assessing caregiver burden. Some previous studies have found that the spouses reported higher levels of caregiver stress and emotional distress compared with other caregivers (1, 9). This study defines a non-spouse next of kin to be a close relative or friend. The results from this study suggest that the situation is burdensome also for those individuals. Furthermore, female next of
Caregiver distress in early ParkinsonÕs disease kins reported slightly more neuropsychiatric symptoms to be associated with distress, but the relatively low number of subjects in different groups leads to low statistical power to detect gender differences for the four NPI items most often associated with distress: depression, apathy, anxiety and irritability. The small gender differences in reported caregiver distress in our population are in line with other studies of gender differences in PD caregiving (3, 7, 9, 31, 32). The use of different instruments to measure caregiver burden may produce differences in results between studies. The NPI is limited to measure the 12 neuropsychiatric aspectsÕ impact on emotional caregiver distress. This is a limitation of our study as compared with studies that apply instruments with a broader range of measurements. By using the NPI in this study of patients with early PD we have therefore studied the impact of neuropsychiatric symptoms that in previous studies have been found to be important contributors to caregiver distress in more advanced PD (1, 7, 13, 31). In conclusion, this study shows that even at the time of diagnosis, distress is a common problem for family members and close friends of patients with PD. Although the burden associated with neuropsychiatric problems varies, presence of apathy, depression, anxiety and irritability in patients are highly associated with distress in next of kins. This underlines the importance of focusing on neuropsychiatric aspects in early PD management. The severity of reported caregiver burden suggests that health-care professional should also identify the burden of next of kins at the early phase of the disease and offer extended education and support to those who are in need. Future studies should focus on designing and examining the effect of different kinds of support to relieve the burden of next of kins.
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Acta Neurol Scand 2010: 122: 418–424 DOI: 10.1111/j.1600-0404.2010.01332.x
ACTA NEUROLOGICA SCANDINAVICA
Caregiver distress associated with neuropsychiatric problems in patients with early ParkinsonÕs disease: the Norwegian ParkWest study Leiknes I, Tysnes O-B, Aarsland D, Larsen JP. Caregiver distress associated with neuropsychiatric problems in patients with early ParkinsonÕs disease: the Norwegian ParkWest study. Acta Neurol Scand: 2010: 122: 418–424. 2010 The Authors Journal compilation 2010 Blackwell Munksgaard. Objectives – We investigated caregiver distress associated with neuropsychiatric problems in patients with newly diagnosed ParkinsonÕs disease (PD). Materials and methods – Persons who were next of kins of 198 patients and 168 healthy individuals completed the Neuropsychiatric Inventory Caregiver Distress Scale. Results – Even at the time of diagnosis PD has a considerable impact on the next of kinsÕ experience of distress. Nearly 50% reported distress, significantly more than in the control group, and more than one-quarter reported moderate severe distress. Except the more rarely reported neuropsychiatric symptoms, apathy was the symptom that most frequently caused caregiver distress in PD patientÕs next of kin (94.5%), followed by depression (88.2%), anxiety (86.2%) and irritability (83.3%). Conclusions – The study underlines the importance of focusing on neuropsychiatric aspects in patients and associated caregiver distress even in early PD management.
Introduction
Caring for a person suffering from ParkinsonÕs disease (PD) may be associated with distress for the caregiver. A variety of variables like the caregiverÕs relation to the care recipients (1, 2), their mood and coping (3), time spent on providing care (4) and family income (2, 5), in addition to the patientÕs situation contribute to the total burden in PD caregivers. PD is a chronic neurodegenerative disease that affects the patientÕs health, both physically and mentally. The progression of the disease may cause disability and increasing need for caregiver support and assistance with activities of daily living (ADL). Previous research concerning caregiving in PD shows conflicting results. Caregiver burden seems however to be closely associated with diseaserelated factors like disease severity (6, 7), the patientÕs functional status and disability (3, 8–10) 418
I. Leiknes1, O.-B. Tysnes2,3, D. Aarsland1,3,4, J. P. Larsen1,3,5 1 The Norwegian Centre for Movement Disorders, Stavanger University Hospital, Stavanger, Norway; 2 Department of Neurology, Haukeland University Hospital, Bergen, Norway; 3School of Medicine, University of Bergen, Bergen, Norway; 4Department of Psychiatry, Stavanger University Hospital, Stavanger, Norway; 5Department of Neurology, Stavanger University Hospital, Stavanger, Norway
Key words: caregivers; Neuropsychiatric Inventory Caregiver Distress Scale; neuropsychiatric symptoms; next of kin; ParkinsonÕs disease Ingrid Leiknes, The Norwegian Centre for Movement Disorders, Stavanger University Hospital, PO Box 8100, 4068 Stavanger, Norway Tel.: 0047 51515601 Fax: 0047 51515515 e-mail: [email protected] Accepted for publication January 5, 2010
and psychiatric symptoms (1, 7, 10). Some studies have found that the ability of the person with PD to perform ADL was the strongest single predictor of the overall caregiver burden (2, 8). Unlike, Aarsland et al. (1) found that the patientÕs mental symptoms had the strongest impact on distress. This finding has been supported by more recent studies (4, 7, 11–13). Previous studies have examined caregiver distress associated with neuropsychiatric problems in clinicbased patient populations with more advanced disease (1, 14, 15). Psychiatric symptomsÕ impact on caregiver distress in the early phase of the disease has received less attention. The aim of this study was to explore distress associated with neuropsychiatric symptoms in persons who were next of kins of patients with newly diagnosed PD. This study is part of the Norwegian ParkWest study, a multicentre population-based longitudinal cohort study of the incidence and prognosis of patients with PD.
Caregiver distress in early ParkinsonÕs disease Burden is in the caregiver literature defined as the extent to which caregivers perceive that their health, social life and financial status are suffering because of their caregiving experience (16). However, as the focus of this study is caregiver distress at the time of diagnosis, it is not expected that the feelings of burden generated by the demands of caregiving, has introduced major limitation on next of kinsÕ social activities and financial situation. This led us to use the Neuropsychiatric Inventory (NPI) Caregiver Distress Scale which assesses the emotional caregiver distress associated with the mental health status of the patients.
Materials and methods Patients and controls
All patients within four counties of western and southern Norway, diagnosed with incident PD according to acknowledged criteria (17) in the period between November 2004 and August 2006, were invited to participate in the Norwegian ParkWest study. A total of 212 patients were included. In addition, 205 individuals were recruited to serve as control subjects. Most of them were spouses or friends of the patients. The rest were unrelated persons from the study area. Control subjects should not have Parkinsonism and should be able to perform the baseline examination. The patients and controls gave their written informed consent to participate in the study. The study was approved by the Regional Ethics Committee, the University of Bergen. The characteristics of the PD cohort have been reported elsewhere (18). Next of kins
Each patient and control subject was asked to have one of their next of kin interviewed as a part of the data collection in the ParkWest study. To serve as an informant, the next of kin had to see the patient ⁄ control on a regular basis, at least once a week, and be a reasonably good observer of the patientÕs behaviour. A total of 193 patients and 198 controls had a next of kin who volunteered participate in the study. Data collection
Caregiver distress – To explore caregiver distress, we used the NPI Caregiver Distress Scale. NPI was developed to assess psychopathology and caregiver distress in patients with dementia (19), but has also been used in several studies of neuropsychiatric
disturbances and caregiver distress in patients with PD (14, 15, 20). The NPI is based on a structured interview with a caregiver who is familiar with the patientÕs behaviour. It assesses 12 behavioural domains and caregiver distress related to each of the domains. The 12 neuropsychiatric domains are: delusions, hallucinations, agitation, depression, anxiety, euphoria, apathy, disinhibition, irritability, aberrant motor behaviour, sleep disturbance and appetite disturbance. The caregivers are asked about behaviours that differed from the patientÕs usual behaviour and had occurred during the past 4 weeks. Each domain has one screening question. A negative answer to the screening question completes the examination of that domain. A positive answer to the screening question results in further exploration of the domain with seven or eight subquestions. Then the caregivers are asked to rate the level of emotional distress experienced with each of the 12 neuropsychiatric domains on a six-point scale from 0 (no distress) to 5 (very or extreme distress). The NPI Caregiver Distress Scale has been proven to be a reliable and valid measure of subjective caregiver distress in relation to neuropsychiatric symptoms (21) and with high reliability in PD (22). To obtain standardization and a high quality in the assessments the interviewer received comprehensive training in assessment procedures. The next of kins were interviewed at the outpatient clinic or by telephone. The validity of using telephone interview has been established (23). Neurological and neuropsychiatric examination – A neurologist evaluated the patientÕs severity of Parkinsonism and disability by the Unified ParkinsonÕs Disease Rating Scale (UPDRS II ADL subscale and UPDRS III motor subscale; 24) including the modified Hoehn & Yahr staging (25) and the Schwab & England scale (26). A trained study nurse administered the NPI according to the aforedescribed guidelines. Statistical analysis
Data were analysed using the SPSS program (version 15.0). Descriptive statistics were used to show the frequencies (%) of caregiver distress scores. SpearmanÕs rank order correlation was used to calculate the strength of the relationship between patientsÕ disease severity and caregiver distress scores. Differences between groups were analysed using Mann–Whitney U-test for nonnormally distributed continuous variables and chi-square test for categorical variables. A value of P < 0.05 was considered significant. 419
Leiknes et al.
Numbers represent mean scores (ranges) or number of patients. UPDRS, Unified ParkinsonÕs Disease Rating scale; ADL, activities of daily living.
more NPI symptoms (Table 3). More NPI symptoms were associated with caregiver distress in female next of kins in the patient group (P = 0.05). Fifty-three (56.4%) of the PD patientsÕ next of kin (77.4% women and 22.6% men) with non-zero distress scores, reported neuropsychiatric symptoms to be causing at least moderately severe distress, that is, a score of ‡3 (Table 4). This is 28% of all PD patientsÕ next of kins in the study. There was a positive correlation between the patientsÕ disease severity scores (UPDRS motor and ADL subscales, Hoehn & Yahr and Schwab & England), and the next of kinsÕ number of NPI scores associated with distress (P < 0.05), but there was no significant correlation between the patientsÕ disease severity scores and the caregiver distress scores of at least moderate severity (‡3). In the control group, 15.5% of the next of kins reported distress on the NPI Caregiver Distress Scale (Table 3). Distress for only one symptom was scored by 13.1%. Of these, 6% only reported neuropsychiatric symptoms to be causing at least moderately severe distress. The frequency of caregiver distress, caregiver distress with a clinically significant severity (‡3) and the number of symptoms associated with caregiver distress differed significantly between PD patientsÕ next of kins and the control group (all Ps < 0.001). Table 4 shows the frequency of caregiver distress in relation to NPI symptoms. Depression was the most frequently reported NPI item giving caregiver distress. Exactly, 31.7% of next of kins experienced distress related to depression among patients. This was followed by apathy (27.5%), anxiety (13.2%), sleep disturbance and disturbance in appetite (10.6% each) and irritability (7.9%). Delusion, agitation, disinhibition and aberrant motor behaviour were uncommon in patients although they were always associated with distress. Among the more frequently reported neuropsychiatric symptoms of clinical importance, apathy was the
Table 2 Gender and relation of next of kin of patients with ParkinsonÕs disease (PD) and controls
Table 3 Frequency of Neuropsychiatric Inventory (NPI) symptoms in patients with ParkinsonÕs disease (PD) and controls and associated caregiver distress scores
Results
A total of 189 patients had a next of kin who completed the NPI Caregiver Distress Scale without missing data and were thus included in the present study. For the purpose of this study, all patients and control subjects in the ParkWest study were matched for age and sex. A total of 168 control subjects and their next of kins were thus included. Mean age was 67.8 years (range: 88.1– 42.3) for the patients and 67.3 (range: 84.5–39.4) for the controls; 59.8% of the patients and 60.7% in the control group were men. Mean time from motor onset to baseline examination was 2.3 years (range: 10.0–0.4; 2.6 for men and 2.0 for women). PatientsÕ disease severity scores are presented in Table 1. The majority of next of kins in both groups were spouses, followed by daughters and sons. Most next of kins (70.9% in the PD patient group and 64.3% in the control group) were women (Table 2). Caregiver distress related to neuropsychiatric problems was assessed with the NPI Caregiver Distress Scale. Ninety-four next of kins (49.8%) of the patients with PD reported distress on this scale. Of these were 77.7% women and 22.3% men. One NPI symptom was scored by 19.6%, 12.2% scored for two symptoms and 18% scored for three or Table 1 PatientsÕ motor symptoms, functional impairment and use of antiParkinsonian drugs
Patient characteristics
All patients, (n = 189)
UPDRS-ADL subscore UPDRS-motor subscore Hoehn & Yahr stage Schwab & England score Using anti-Parkinsonian drugs
9.0 23.2 1.9 87.9 5
Characteristics Gender Female Male Relation Spouse Daughter ⁄ son Other relative Others (friend, neighbour)
420
(25–1) (55–4) (4–1) (100–50)
Next of kin of PD patients, n = 189 (%)
Women, (n = 76)
Men, (n = 113)
9.0 21.6 1.9 87.2 1
9.0 24.3 1.9 88.4 4
Next of kin of controls, n = 168 (%)
NPI symptoms
134 (70.9) 55 (29.1)
108 (64.3) 60 (35.7)
Number
134 31 18 6
147 11 6 4
1 2 3 4 5 6
(70.9) (16.4) (9.5) (3.2)
(87.5) (6.5) (3.6) (2.4)
Patients, n = 189 (%) 42 22 23 12 5 6
(22.2) (11.6) (12.2) (6.3) (2.6) (3.2)
Caregiver distress scores
Controls, n = 168 (%) 26 8 0 2
(15.5) (4.8) (0.0) (1.2)
PD next of kin, n = 189 (%) 37 23 17 7 6 4
(19.6) (12.2) (9.0) (3.7) (3.2) (2.1)
Next of kin of controls, n = 168 (%) 22 2 1 1
(13.1) (1.2) (0.6) (0.6)
Caregiver distress in early ParkinsonÕs disease Table 4 Neuropsychiatric Inventory (NPI) symptoms in patients and related distress in next of kin of patients with ParkinsonÕs disease (PD) Caregiver distress score Number of patients with NPI symptoms, n = 189 (%)
NPI item Delusions Hallucinations Agitation ⁄ aggression Depression Anxiety Euphoria Apathy Disinhibition Irritability ⁄ lability Aberrant motor behaviour Sleep disturbance Appetite disturbance Total score
2 2 9 68 29 0 55 7 18 5 38 31 110
(1.1) (1.1) (4.8) (36.0) (15.3) (0.0) (29.1) (3.7) (9.5) (2.6) (20.1) (16.4) (58.2)
Number (%)* with distress 2 1 9 60 25 0 52 7 15 5 20 20 94
Percentage with distress**
(100.0) (50.0) (100.0) (88.2) (86.2) (0.0) (94.5) (100.0) (83.3) (100.0) (52.6) (64.5) (84.5)
Number (%)*** with score ‡3
1.1 0.5 4.8 31.7 13.2 0.0 27.5 3.7 7.9 2.6 10.6 10.6 49.8
2 0 5 33 17 0 27 4 7 0 7 8 53
Percentage with score ‡3**
(100.0) (0.0) (55.0) (68.0) (51.9) (0.0) (46.7) (57.1) (38.9) (0.0) (35.0) (40.0) (56.4)
1.1 0.0 2.6 17.5 9.0 0.0 14.3 2.1 3.7 0.0 3.7 4.2 28.0
*Percentage with non-zero distress scores of patients showing symptoms. **Percentage of all (n = 189). ***Percentage with scores ‡3 of next of kins with distress.
symptom that most often caused caregiver distress; 94.5% of the next of kins of patients with apathy experienced distress related to the symptom. This was followed by depression (88.2%), anxiety (86.2%) and irritability (83.3%). Of all present neuropsychiatric symptoms associated with caregiver distress only depression and apathy distress scores correlated positively with the patientÕs disease stage (Hoehn & Yahr; P < 0.05). Table 5 shows the proportion of caregiver distress according to gender and in spouses and nonspouses for the four NPI items causing most distress: depression, apathy, anxiety and irritability. In both spouses and non-spouses, the proportion of reported caregiver distress was high when
symptoms occurred (76.9% or more). Apathy is highly associated with caregiver distress (‡81.8) for both gender and both groups of next of kin. Female next of kins in general and female spouses show a non-significant trend to have more distress than male next of kins. Discussion
This study demonstrates that even at the time of diagnosis PD has a considerable impact on experienced distress by persons who are living close to the patients. Next of kins of patients with PD reported three times more frequently burden associated with neuropsychiatric symptoms as
Table 5 Number and proportion of next of kins with distress according to relationship to patients and to gender Number and proportion (%) with caregiver distress
NPI items
Patients with NPI symptoms, n = 189
All next of kins, n = 189
Depression
68
60
Anxiety
Apathy
Irritability
29
55
18
Category
n (%)*
Spouses Non-spouses
46 (90.2) 14 (82.4)
Spouses Non-spouses
18 (85.7) 7 (87.5)
Spouses Non-spouses
39 (97.5) 13 (86.7)
Spouses Non-spouses
10 (76.9) 5 (100.0)
25
P**
Category
0.302
All Spouses Non-spouses All Spouses Non-spouses All Spouses Non-spouses All Spouses Non-spouses
1.000
52
0.479
15
0.769
Women, n = 134 (%)* 46 35 11 20 16 4 41 32 9 13 9 4
(92.0) (94.6) (84.6) (90.9) (94.1) (80.0) (93.2) (97.0) (81.8) (92.9) (90.0) (100.0)
Men, n = 55 (%)* 14 11 3 5 2 3 11 7 4 2 1 1
(77.8) (78.6) (75.0) (71.4) (50.0) (100.0) (100.0) (100.0) (100.0) (50.0) (33.3) (100.0)
P** 0.302 0.324 0.734 0.35 0.094 0.376 0.155 0.063 0.734 0.238 0.281 1.00
*Percentage with non-zero distress scores of patients showing symptoms in the present group. **Chi-square test.
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Leiknes et al. compared with the control group and the severity of the reported burden was significantly higher in the PD group. In addition, 30.2% of the PD patientsÕ next of kins reported burden related to two or more items on the NPI, whereas this was the case for only 2.4% in the control group. These findings indicate that the management of patients with early PD should also include attention to the situation of their close relatives or friends. This is the first study focusing on caregiver burden at the time of PD diagnosis. Our findings are in line with the results of other studies with caregiver distress present at all stages of the disease, although in these studies the extent of burden was strongly associated with disease severity (3, 6, 7, 9). In our study, patientsÕ disease severity correlated with the number of neuropsychiatric symptoms associated with caregiver distress scores (P < 0.05), but did not cause more severe distress in the next of kin. This may be a result of the relative low impact of the disease of the patientsÕ functional ability in our population (mean Schwab & England was 87.9%). However, the reported burden in our study with early PD was relatively high compared with a recently published Spanish study of neuropsychiatric symptoms and caregiver distress among non-demented patients with more severe Parkinsonism (15). When a family member or another close friend is diagnosed with a chronic disease the situation may feel unsafe. Uncertainty concerning medical treatment, disease severity and a potentially incapacitating disease may influence the scores of experienced distress among close relatives and friends of patients with early disease. In a longitudinal study of caregiver burden in relation to PD, the burden was reduced from diagnosis to the 2-year follow-up examination (16). This suggests that next of kinsÕ ability to tolerate problem behaviour is reduced at the time of receiving the diagnosis. They may be more sensitive to the patientsÕ emotional behaviour and the presence of neuropsychiatric symptoms which could be a reason for higher scores on the caregiver distress scale in the early phase of the disease. Another possibility is that next of kins may change their strategies for coping with everyday problems as they develop experience and adaptation. In addition, cultural differences between countries may also influence experience of distress and explain the differences between studies. Except from the more rarely reported neuropsychiatric items delusion, agitation ⁄ aggression, disinhibition and aberrant motor behaviour, the symptoms most frequently associated with caregiver distress in this study were apathy, depression, 422
anxiety and irritability. In the aforementioned Spanish study (15), delusions, agitation, hallucination and depression were the NPI symptoms causing most burdens. This profile of distress is in agreement with that found in caregivers of demented patients with PD (14). These findings indicate that neuropsychiatric symptoms that impose distress in next of kins change over time when more severe neuropsychiatric symptoms develop. As the only neuropsychiatric caregiver distress scores that correlated with the patientsÕ disease stage were depression and apathy, it seems that close relatives or friends are more sensitive to this behaviour than to other neuropsychiatric problems in early PD. Although caregiver distress associated with depression was the most frequently reported item in our study, apathy was also frequent and even closer associated with burden. Its impact on caregiver burden has until recently received less attention than depression, although the important consequences of apathy on caregivers of both nondemented (27) and demented PD patients (14) have been shown. The loss of vitality and enjoyment related to apathy can make the relationship between the person with PD and the next of kin challenging and also force changes in the partnersÕ relationship and responsibility. Apathy and depression are closely related. Apathy as a syndrome may occur on its own or as a part of depression (28, 29). Furthermore, there is a lack of generally accepted diagnostic criteria for apathy as a syndrome (28) and this can make it difficult to differentiate these two syndromes in clinical research context. The NPI is one of several suggested rating scales of apathy (28) which gives an opportunity to separate between the two conditions as the NPI depression subscale excludes items related to apathy, and the apathy subscale has no items related to sadness (30), which is a typical symptom in depression. NPI may therefore also be a suitable instrument for assessing caregiver burden associated with depression and apathy. PD spouses did not differ significantly from nonspouses in reported caregiver burden in any of the assessed neuropsychiatric domains in this study. To our knowledge there are few studies analysing the impact of the next of kinÕs relation to the patient when assessing caregiver burden. Some previous studies have found that the spouses reported higher levels of caregiver stress and emotional distress compared with other caregivers (1, 9). This study defines a non-spouse next of kin to be a close relative or friend. The results from this study suggest that the situation is burdensome also for those individuals. Furthermore, female next of
Caregiver distress in early ParkinsonÕs disease kins reported slightly more neuropsychiatric symptoms to be associated with distress, but the relatively low number of subjects in different groups leads to low statistical power to detect gender differences for the four NPI items most often associated with distress: depression, apathy, anxiety and irritability. The small gender differences in reported caregiver distress in our population are in line with other studies of gender differences in PD caregiving (3, 7, 9, 31, 32). The use of different instruments to measure caregiver burden may produce differences in results between studies. The NPI is limited to measure the 12 neuropsychiatric aspectsÕ impact on emotional caregiver distress. This is a limitation of our study as compared with studies that apply instruments with a broader range of measurements. By using the NPI in this study of patients with early PD we have therefore studied the impact of neuropsychiatric symptoms that in previous studies have been found to be important contributors to caregiver distress in more advanced PD (1, 7, 13, 31). In conclusion, this study shows that even at the time of diagnosis, distress is a common problem for family members and close friends of patients with PD. Although the burden associated with neuropsychiatric problems varies, presence of apathy, depression, anxiety and irritability in patients are highly associated with distress in next of kins. This underlines the importance of focusing on neuropsychiatric aspects in early PD management. The severity of reported caregiver burden suggests that health-care professional should also identify the burden of next of kins at the early phase of the disease and offer extended education and support to those who are in need. Future studies should focus on designing and examining the effect of different kinds of support to relieve the burden of next of kins.
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