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Motor and Non-Motor Symptoms in Turkish Patients With Parkinson’s Disease Affecting Family Caregiver Burden and Quality of Life
Betul Ozdilek, M.D.; Dilek Ince Gunal, M.D.
The Journal of Neuropsychiatry and Clinical Neurosciences 2012;24:478-483. doi:10.1176/appi.neuropsych.11100315
View Author and Article Information
Department of Neurology, Marmara University Hospital, Istanbul Turkey.

The authors report no conflict of interest.

Send correspondence to Betul Ozdilek, M.D., Erenkoy Research and Training Hospital for Neurology and Psychiatry; e-mail: betulozdilek@yahoo.com

Received October 26, 2011; Revised February 11, 2012; Accepted March 22, 2012.

Abstract

Parkinson’s disease (PD) decreases the quality of life (QoL) of both caregivers and patients by increasing stress and burden, and it has a negative impact on their psychological state. In the present study, the authors examined the impact of PD-patient motor and non-motor clinical symptoms on the psychological health, burden, and QoL of Turkish caregivers. The study included 50 patients with PD and their caregivers. Patients’ disease severity and disability, motor and non-motor symptoms, disease complications, sleep disturbances, anxiety, and depressive symptoms were assessed with various scales. Data were analyzed by multiple linear-regression models to identify variables associated with caregiver burden, psychological status, and QoL. Anxiety and depressive symptoms exhibited by the patients significantly affected the psychological state of the caregivers. Caregiver burden was increased by disease severity; the patient’s degree of disability, anxiety, and depressive symptoms; and excessive daytime sleepiness. Caregiver QoL was significantly affected by the presence of dyskinesia, sialorrhea, and anxiety symptoms in patients with PD. These findings indicate that caregiving for patients with PD, particularly those in later stages, with psychiatric symptoms, affects caregiver psychological status, QoL, and caregiver burden. These results can be used to develop treatment approaches to improve caregivers’ psychological status and QoL and decrease caregiver burden.

Abstract Teaser
Figures in this Article

Parkinson’s disease (PD) is a chronic and progressive neurodegenerative movement disorder characterized by resting tremor, rigidity, bradykinesia, and postural instability. In addition to these motor symptoms, non-motor symptoms, such as autonomic dysfunction; sleep problems; and affective, cognitive, and psychiatric disorders, occur frequently in PD.1 The progressive debilitating nature of the disease often makes having caregivers necessary.

In Turkey, much of the long-term care of these patients is provided by family members, particularly their spouses. Caring for a PD patient is an extremely demanding task that can result in caregiver burden, anxiety, and depression. These symptoms are present in caregivers dealing with all stages of the disease, and they have been shown to increase as the disease progresses.2 The impact of PD on quality of life (QoL) and caregiver burden has received growing attention in recent years. Caregiver burden is a multidimensional response to physical, psychological, emotional, social, and financial stressors associated with caring for a chronically ill patient.3,4

QoL, with regard to health, refers to an individual’s perception of his or her well-being in the physical and psychological, health, social, and environmental domains. The physical health domain measures perception of the effort necessary to perform daily activities. The social domain measures the degree to which an individual can get in touch and interact with family members, neighbors, colleagues, and individuals in other communities. The psychological health domain assesses psychological and emotional states such as depression, anxiety, fear, anger, and happiness.5

PD decreases the QoL of both the caregiver and patient by increasing stress and burden, and it has a negative impact on their psychological state.6 It is necessary to understand the extent of caregiver burden and the factors associated with it to support caregivers in their role. Thus, we conducted a study using multidimensional instruments to identify factors that affect anxiety and depression, caregiver burden, and QoL among caregivers of patients with PD.

The study included 50 outpatients diagnosed with clinically idiopathic PD and their primary caregivers, who volunteered to be interviewed after a routine clinic visit. Inclusion criteria were 1) patient’s age between 45 and 90 years, and caregiver’s age over 18 years, with at least 5 years of education; 2) patients in Stage 2, 3, 4, or 5 of the Hoehn & Yahr (HY) scale; 3) patient’s Mini-Mental State Exam (MMSE) score >24; 4) patient contact with a responsible caregiver at least 3 hours per day for at least the past 6 months; 5) patients who had used antiparkinsonian therapy regularly for 6 months; and 6) patients who were accompanied by their usual caregivers for more than three consecutive consultations.

Demographic and clinical information obtained from patients and their caregivers included age, gender, marital status, years of education, presence of chronic illness, working status, monthly family income, caregiver relationship to the patient, living arrangements, duration of caregiving (months), daily hours of caregiving, duration of disease (years), severity of PD, and drug therapy. The presence or absence of motor fluctuations, dyskinesia, hallucinations, delusions, sialorrhea, urinary and bowel incontinence, and sleep disturbances was recorded.

The present study was approved by the University Institutional Review Board. Patients and their caregivers provided written informed consent.

The same neurologist interviewed all patients and their caregivers and completed questionnaires using face-to-face survey interviews. All questionnaires for patients and caregivers were developed through qualitative research and a validation study in accordance with Turkish cultural characteristics.

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Instruments

Each patient was assessed with the Unified Parkinson's Disease Rating Scale (UPDRS), the Schwab-England Activities of Daily Living (SE-ADL), the Hoehn & Yahr (HY) scale, and MMSE scales. The HY and SE-ADL scales assess patients’ disease severity and disability. Motor and non-motor symptoms, both disease and drug complications were evaluated with the UPDRS. Sleep disturbances in patients with PD were assessed with the Parkinson’s Disease Sleep (PDS) and Epworth Sleepiness (ES) scales.

The Hospital Anxiety and Depression Scales (HADS) and the Beck Depression Inventory (BDI) were used to assess anxiety and depressive symptoms in PD patients and their caregivers. The HADS consists of 14 items (7 for assessment of anxiety and 7 for assessment of depressive symptoms). The scores on each scale were summed, and, the higher the score, the higher the degree of anxiety or depression. A HADS–Anxiety scale score of ≥10 indicates risk of anxiety, and a HADS–Depression score of ≥7 indicates risk for depression.7 The BDI is a widely-used, 21-item inventory covering somatic, affective, and behavioral symptoms of depression. Scores can range from 0 to 63, with higher scores representing a stronger tendency toward depressive feelings. A score of ≥17 indicates risk for depression.8

The Zarit Burden Inventory (ZBI) measures the care-burden on caregivers. It is a 22-item questionnaire, with a total score range of 0 to 88. No cut-off scores have been established, but higher scores indicate greater levels of caregiver burden.3

The QoL of patients and their caregivers was evaluated using the Turkish version of the World Health Organization Quality of Life Assessment-Bref (WHOQOL-BREF). The WHOQOL-BREF questionnaire consists of 27 items. Two questions assess global QoL, and the remaining items assess specific aspects of QoL that include the physical health, psychological health, social relationships, and environmental domains.9 The scores of the domains were transformed into a linear 0–100-point scale. Higher scores indicated better QoL in each domain.

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Statistical Analyses

We used multiple linear-regression analyses to identify variables related to caregiver burden, psychological status of the caregivers, and caregiver scores in each WHOQOL-BREF domain. We used the Mann-Whitney U test or Kruskal-Wallis test to compare the distribution of scores for independent samples, and the Pearson’s correlation coefficient (r) to test the association between caregiver burden or WHOQOL-BREF and the other measures. Variables were included in the above models following a stepwise procedure, with statistical significance defined as p<0.05. All analyses were carried out using SPSS software (Version 15.0 for Windows; SPSS, Inc.; Chicago, IL, USA).

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Demographic, Clinical, and Psychological Status of Patients and Caregivers

Of the 50 patients, 34 (68%) were men, and the mean age was 67.6 (standard deviation [SD]: 9.3 years (range: 46–89). Forty-six patients (92%) had the tremors/rigid form of PD, and eight patients (16%) had a family history of PD. The distribution of patients according to HY stage: 13 patients at Stage 2, 16 at Stage 3, 14 at Stage 4, and 7 patients at Stage 5 of the disease. The mean duration of PD was 9.7 (3.4) years (range: 4–17). The average SE-ADL score was 50%. Of all patients, 27 (54%) had lucid dreams; 8 (16%) had mild or moderate hallucinations; 42 (84%) had sialorrhea; 19 (38%) had dyskinesia; 41 (82%) had motor fluctuations; 25 (50%) had motor blocks; 8 (16%) had objective orthostatic hypotension; and 5 patients had urinary or bowel incontinence. All patients were receiving antiparkinsonian drugs; 5 patients (10%) used an antidepressant; 8 (16%) used an antipsychotic agent; and 10 patients (20%) used more than one type of psychotropic drug.

The mean age of the caregivers was 56.6 (13.2) years (range: 20–85). Most caregivers were women (N=39; 78%). Three groups of caregivers were identified according to their relationship with the patient: spouses (N=37; 74%), children (N=11; 22% [daughter: N=8; son: N=3), and siblings (N=2; 4%). The mean duration of marriage was 38.2 (12.0) years. All caregivers were family members. Patients were most frequently cared for by a spouse or daughter at the patient’s home. The average caregiving duration was 26 months, and the average amount of time spent in daily caregiving was 10 hours. Psychotropic drugs were prescribed for 10% of the caregivers.

The HADS score revealed that 9 of the PD patients (18%) had anxiety symptoms, and 29 (58%) had depression symptoms. The ES scale revealed that 9 patients (18%) had pathological sleepiness. According to the PDS scale, 40 patients reported that they were satisfied with their sleep.

The caregiver scores on the HADS–Anxiety scale revealed that 18 (36%) had anxiety symptoms, and, according to the HADS–Depression and BDI scales, 22 (44%) and 14 (28%) of caregivers, respectively, had depression symptoms. No caregiver experienced pathological sleepiness.

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Variables Affecting Caregivers’ Psychological State

No significant correlation was found between the patient and caregiver demographic characteristics and clinical data and the caregiver HADS and BDI scores. However, a significant difference was found between the HADS scores of PD patients and the HADS and BDI scores of the caregivers (p <0.05).

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Variables Affecting Caregiver Burden

According to the ZBI scale, caregivers reported feeling a mild burden (score 27.6 [15.1]). Variables that significantly affected caregiver burden were stage of the disease (HY scale; r=0.42; p=0.02), the SE-ADL score (r = −0.46; p=0.001); UPDRS I, II, III, IV-A, B, C and Total patient score (r=0.32, p=0.02; r=0.40, p=0.004; r=0.28, p=0.04; r=0.41, p=0.003; r=0.33, p=0.01; r=0.42, p=0.002; r=0.37, p=0.007, respectively); dyskinesia, motor fluctuations, sudden motor blocks, and daily “off” time (r=0.28, p=0.04; r=0.04, p=0.01; r=0.28, p=0.04; r=0.29, p=0.04, respectively), daily caregiving hours (r=0.47, p<0.001), patient HADS–Anxiety and Depression scores (r=0.47, p <0.001; r=0.43, p=0.002, respectively), patient daytime sleepiness level (r=0.28, p=0.04), caregiver HADS–Anxiety and Depression scores (r=0.53, p=0.001; r=0.44, p=0.001, respectively), and caregiver BDI scores (r=0.48, p=0.001).

No significant relationship was found between patient and caregiver demographics and clinical features and other measures of caregiver burden.

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Variables Affecting Caregiver QoL

No significant relationship was found between patient and caregiver demographic characteristics and caregiver WHOQOL-BREF domain scores (p >0.05). A significant negative correlation was found between the presence of sialorrhea in patients and the caregivers’ Environmental Domain score and between the presence of dyskinesia and the caregivers’ Psychological Health domain score. Furthermore, a significant negative correlation was found between patient HADS–Anxiety scores and caregiver scores on the Physical Health and Environmental domains of the WHOQOL-BREF. The caregiver HADS and BDI scores showed a significant negative correlation with each of the caregiver WHOQOL-BREF domain scores. Thus, caregiver burden was negatively correlated with every WHOQOL-BREF domain except Social Relationships (Table 1).

 
Anchor for Jump
TABLE 1.Correlations Among WHOQOL-BREF Domains of the Caregivers and Other Variables in Patients and Caregivers, r (p)
Table Footer Note

WHOQOL–BREF: World Health Organization Quality of Life Assessment–Bref; HADS: Hospital Anxiety and Depression Scale; BDI: Beck Depression Inventory; ZBI: Zarit Burden Inventory.

In the present study, we investigated the impact of clinical PD symptoms on the level of anxiety and depression in caregivers, their QoL, and caregiver burden. Caregiver burden and QoL should be considered when arranging patient treatment, and measures should be taken to lessen the burden, particularly for caregivers of patients in the later stages of PD.2

In our study, 78% of the caregivers were women, and 22% were men. This finding is consistent with previous studies showing that the majority of caregivers are women.1013 Caregiving is perceived to be a job for wives and daughters for a variety of socioeconomic reasons, but primarily because it is considered the man’s place to work outside the home.

All of the caregivers in our study were spouses, children, or siblings, attesting to the impact of PD on the family of patients. We did not intend to study only caregivers who were family members, but we found that the caregivers of patients who were eligible for our study were all family members, indicating that, in Turkish society, caregiving is primarily imposed on family members. Our results are consistent with those of a previous study showing that patients are cared for by wives or daughters in the patients’ home.14 An association between caregiver burden and the caregiver’s relationship to the patient has been reported;15 however, we did not find a significant difference in caregiver burden between spouses and children.

Our findings were consistent with those of Martinez-Martin et al.,12 who reported that the daily hours of caregiving increased as the severity of the disease increased (p=0.03) and daily functioning decreased (p=0.01). We found a significant relationship between severity of disease, as measured by the HY scale and the SE-ADL percentage, and daily hours of caregiving.

Depression symptoms have been reported in 40%–50% of caregivers, and 30% have been found to experience anxiety.1114 Using psychological tests, we found depression symptoms in 28% of the caregivers, according to the BDI, and in 44% of the caregivers according to the HADS–Depression scale. The percentage of caregivers with depression symptoms, as measured by the HADS–Depression scale, was similar to that reported in previous studies; however, the percentage of caregivers suffering depression according to the BDI score was lower than that previously reported. We used a score of 17 as the cut-off point on the BDI scale; however, previous studies used a cut-off point of 10. Thus, either the HADS–Depression or BDI should be used to detect symptoms of depression in caregivers. We found that the BDI was more appropriate for caregivers because the HADS–Depression scale includes a broader range of depression symptoms. Female caregivers have been reported to have more depressive symptoms than male caregivers;11,16 however, we did not find a significant relationship between caregiver gender and other sociodemographic features.

We found that patient anxiety and depression was the most significant patient characteristic contributing to caregiver anxiety and depression. This finding was consistent with that of Miller.17 Furthermore, symptoms of anxiety and depression in patients can cause a subtle increase in caregiver burden and decrease QoL. These results are consistent with those of previous studies.2,1820

According to the ZBI scores, caregivers reported feeling a mild burden. A significant relationship was found between the ZBI score and phase of disease, specifying the clinical status of patients, stage of the disease, the SE-ADL percentage, UPDRS scores, anxiety and depression scores, and motor and non-motor symptoms. This finding is consistent with reports in the literature.2,1114,17,18 Thus, the burden score increases as the severity of the disease increases and as the patient SE-ADL percentage decreases. We did not examine the impact of cognitive symptoms on caregivers in the present study. Although a previous study reported a significant relationship between caregiver burden and patient QoL,11 we found no evidence of such a relationship.

No significant difference was found between men and women in the “burden” levels of daily hours of caregiving and total caregiving time.11,16 We found that daily hours of caregiving was significantly related to caregiving burden (p <0.001), but observed no significant relationship between burden and age, gender, or education of the caregiver. These results are consistent with the literature.1013

Caregiver burden has been reported to cause anxiety and depression in the caregivers.12,18,19 In the present study, we found a relationship between the level of caregiver anxiety and depression and the burden they felt. It is likely that caregiver depression and anxiety increase the caregiver burden and that increased burden may, in turn, increase depression and anxiety.

We found no significant relationship between caregiver QoL and WHOQOL-BREF domain scores and patient sociodemographic variables. Moreover, no relationship was found between the QoL of patients and their caregivers, suggesting that caregiver QoL may not depend on the QoL of the people they are caring for. Anxiety and depression symptoms of the caregivers have a direct influence on their QoL. A significant relationship was found between the presence of dyskinesia and sialorrhea in patients and caregiver QoL, particularly between dyskinesia and the Physical and Psychological Health domains (p=0.02 and p=0.03, respectively) and sialorrhea and the environmental domain (p=0.03). Of the psychological symptoms, patient anxiety had the most significant effect on caregiver QoL in the Physical Health and Environmental domains (p=0.01 and p=0.002, respectively). Our data indicated that the presence of dyskinesia, sialorrhea, and anxiety in the patients had a substantial effect on caregiver QoL scores, and the degree of caregiver burden influenced caregiver QoL. Furthermore, our findings suggest that the patient characteristics that influence caregiver burden (i.e., severity of the disease, disability of the patients, and UPDRS scores) have an indirect effect on caregiver QoL; in particular, the presence of dyskinesia had a significant effect on both caregiver QoL and burden. These results are consistent with those reported in the literature.12,14,21,22

Limitations of the present study include a relatively small sample size and use of only scales for assessing patient and caregiver psychological status. A psychological-status examination may provide a more accurate measure. Furthermore, in contrast to the findings of Hirayama et al.,23 we believe that the WHOQOL-BREF scale may be more useful for assessing QoL in caregivers than in patients with PD because the patients did not understand the questions clearly. Each question was repeated three times in order to get the most accurate response.

In conclusion, patient anxiety was the most significant patient factor affecting caregiver psychological status. Patient disease severity, UPDRS scores, disability, anxiety and depression symptoms, and excessive daytime sleepiness significantly affected caregiver burden, and the presence of dyskinesia, sialorrhea, and anxiety symptoms in patients with PD significantly affected caregiver QoL. Moreover, anxiety and depression symptoms in the caregivers, caregiver burden, and QoL have significant mutual effects. Thus, Turkish family members caring for patients with PD, particularly patients in late stages, with psychiatric symptoms, experience a decrease in psychological well-being, QoL, and increased caregiver burden. These results can be useful for developing treatment approaches that increase caregiver QoL and relieve the caregiver burden during the course of PD.

Fahn  S;  Jankovic  J (ed):  Principles and Practice of Movement Disorders .  Philadelphia, PA,  Churchill Livingstone, 2010
 
Carter  JH;  Stewart  BJ;  Archbold  PG;  Parkinson’s Study Group,  et al:  Living with a person who has Parkinson’s disease: the spouse’s perspective by stage of disease.  Mov Disord 1998; 13:20–28
[CrossRef] | [PubMed]
 
Zarit  SH;  Reever  KE;  Bach-Peterson  J:  Relatives of the impaired elderly: correlates of feelings of burden.  Gerontologist 1980; 20:649–655
[CrossRef] | [PubMed]
 
Edwards  NE;  Scheetz  PS:  Predictors of burden for caregivers of patients with Parkinson’s disease.  J Neurosci Nurs 2002; 34:184–190
[CrossRef] | [PubMed]
 
Fitzpatrick  R;  Fletcher  A;  Gore  S  et al:  Quality of life measures in health care. I: applications and issues in assessment.  BMJ 1992; 305:1074–1077
[CrossRef] | [PubMed]
 
Carter  JH;  Stewart  BJ;  Lyons  KS  et al:  Do motor and nonmotor symptoms in PD patients predict caregiver strain and depression? Mov Disord 2008; 23:1211–1216
[CrossRef] | [PubMed]
 
Zigmond  AS;  Snaith  RP:  The Hospital Anxiety and Depression Scale.  Acta Psychiatr Scand 1983; 67:361–370
[CrossRef] | [PubMed]
 
Beck  AT;  Steer  RA:  Internal consistencies of the original and revised Beck Depression Inventory.  J Clin Psychol 1984; 40:1365–1367
[CrossRef] | [PubMed]
 
The WHOQOL Group:  Development of the World Health Organization WHOQOL-BREF Quality of Life assessment.  Psychol Med 1998; 28:551–558
[CrossRef] | [PubMed]
 
Hooker  K;  Manoogian-O’Dell  M;  Monahan  DJ  et al:  Does type of disease matter? gender differences among Alzheimer’s and Parkinson’s disease spouse caregivers.  Gerontologist 2000; 40:568–573
[CrossRef] | [PubMed]
 
Schrag  A;  Hovris  A;  Morley  D  et al:  Caregiver burden in Parkinson’s disease is closely associated with psychiatric symptoms, falls, and disability.  Parkinson Relat Disord 2006; 12:35–41
[CrossRef]
 
Martínez-Martín  P;  Forjaz  MJ;  Frades-Payo  B  et al:  Caregiver burden in Parkinson’s disease.  Mov Disord 2007; 22:924–931, quiz 1060
[CrossRef] | [PubMed]
 
Lökk  J:  Caregiver strain in Parkinson’s disease and the impact of disease duration.  European Journal of Physical Rehabilitative Medicine 2008; 44:39–45
 
Aarsland  D;  Larsen  JP;  Karlsen  K  et al:  Mental symptoms in Parkinson’s disease are important contributors to caregiver distress.  Int J Geriatr Psychiatry 1999; 14:866–874
[CrossRef] | [PubMed]
 
Whetten-Goldstein  K;  Sloan  F;  Kulas  E  et al:  The burden of Parkinson’s disease on society, family, and the individual.  J Am Geriatr Soc 1997; 45:844–849
[PubMed]
 
Pruchno  RA;  Resch  NL:  Husbands and wives as caregivers: antecedents of depression and burden.  Gerontologist 1989; 29:159–165
[CrossRef] | [PubMed]
 
Miller  E;  Berrios  GE;  Politynska  BE:  Caring for someone with Parkinson’s disease: factors that contribute to distress.  Int J Geriatr Psychiatry 1996; 11:263–268
[CrossRef]
 
Caap-Ahlgren  M;  Dehlin  O:  Factors of importance to the caregiver burden experienced by family caregivers of Parkinson’s disease patients.  Aging Clin Exp Res 2002; 14:371–377
[PubMed]
 
Thommessen  B;  Aarsland  D;  Braekhus  A  et al:  The psychosocial burden on spouses of the elderly with stroke, dementia, and Parkinson’s disease.  Int J Geriatr Psychiatry 2002; 17:78–84
[CrossRef] | [PubMed]
 
Martínez-Martín  P;  Guerrero-Díaz  MT;  Frades-Payo  B:  [Neuropsychological disorders in Parkinson’s disease: evaluating them and their impact on the caregiver].  Rev Neurol 2004; 39:639–645
[PubMed]
 
Karlsen  KH;  Larsen  JP;  Tandberg  E  et al:  Influence of clinical and demographic variables on quality of life in patients with Parkinson’s disease.  J Neurol Neurosurg Psychiatry 1999; 66:431–435
[CrossRef] | [PubMed]
 
Schrag  A;  Jahanshahi  M;  Quinn  NP:  What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 2000; 69:308–312
[CrossRef] | [PubMed]
 
Hirayama  MS;  Gobbi  S;  Gobbi  LT  et al:  Quality of life (QoL) in relation to disease severity in Brazilian Parkinson’s patients as measured using the WHOQOL-BREF.  Arch Gerontol Geriatr 2008; 46:147–160
[CrossRef] | [PubMed]
 
References Container
Anchor for Jump
TABLE 1.Correlations Among WHOQOL-BREF Domains of the Caregivers and Other Variables in Patients and Caregivers, r (p)
Table Footer Note

WHOQOL–BREF: World Health Organization Quality of Life Assessment–Bref; HADS: Hospital Anxiety and Depression Scale; BDI: Beck Depression Inventory; ZBI: Zarit Burden Inventory.

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References

Fahn  S;  Jankovic  J (ed):  Principles and Practice of Movement Disorders .  Philadelphia, PA,  Churchill Livingstone, 2010
 
Carter  JH;  Stewart  BJ;  Archbold  PG;  Parkinson’s Study Group,  et al:  Living with a person who has Parkinson’s disease: the spouse’s perspective by stage of disease.  Mov Disord 1998; 13:20–28
[CrossRef] | [PubMed]
 
Zarit  SH;  Reever  KE;  Bach-Peterson  J:  Relatives of the impaired elderly: correlates of feelings of burden.  Gerontologist 1980; 20:649–655
[CrossRef] | [PubMed]
 
Edwards  NE;  Scheetz  PS:  Predictors of burden for caregivers of patients with Parkinson’s disease.  J Neurosci Nurs 2002; 34:184–190
[CrossRef] | [PubMed]
 
Fitzpatrick  R;  Fletcher  A;  Gore  S  et al:  Quality of life measures in health care. I: applications and issues in assessment.  BMJ 1992; 305:1074–1077
[CrossRef] | [PubMed]
 
Carter  JH;  Stewart  BJ;  Lyons  KS  et al:  Do motor and nonmotor symptoms in PD patients predict caregiver strain and depression? Mov Disord 2008; 23:1211–1216
[CrossRef] | [PubMed]
 
Zigmond  AS;  Snaith  RP:  The Hospital Anxiety and Depression Scale.  Acta Psychiatr Scand 1983; 67:361–370
[CrossRef] | [PubMed]
 
Beck  AT;  Steer  RA:  Internal consistencies of the original and revised Beck Depression Inventory.  J Clin Psychol 1984; 40:1365–1367
[CrossRef] | [PubMed]
 
The WHOQOL Group:  Development of the World Health Organization WHOQOL-BREF Quality of Life assessment.  Psychol Med 1998; 28:551–558
[CrossRef] | [PubMed]
 
Hooker  K;  Manoogian-O’Dell  M;  Monahan  DJ  et al:  Does type of disease matter? gender differences among Alzheimer’s and Parkinson’s disease spouse caregivers.  Gerontologist 2000; 40:568–573
[CrossRef] | [PubMed]
 
Schrag  A;  Hovris  A;  Morley  D  et al:  Caregiver burden in Parkinson’s disease is closely associated with psychiatric symptoms, falls, and disability.  Parkinson Relat Disord 2006; 12:35–41
[CrossRef]
 
Martínez-Martín  P;  Forjaz  MJ;  Frades-Payo  B  et al:  Caregiver burden in Parkinson’s disease.  Mov Disord 2007; 22:924–931, quiz 1060
[CrossRef] | [PubMed]
 
Lökk  J:  Caregiver strain in Parkinson’s disease and the impact of disease duration.  European Journal of Physical Rehabilitative Medicine 2008; 44:39–45
 
Aarsland  D;  Larsen  JP;  Karlsen  K  et al:  Mental symptoms in Parkinson’s disease are important contributors to caregiver distress.  Int J Geriatr Psychiatry 1999; 14:866–874
[CrossRef] | [PubMed]
 
Whetten-Goldstein  K;  Sloan  F;  Kulas  E  et al:  The burden of Parkinson’s disease on society, family, and the individual.  J Am Geriatr Soc 1997; 45:844–849
[PubMed]
 
Pruchno  RA;  Resch  NL:  Husbands and wives as caregivers: antecedents of depression and burden.  Gerontologist 1989; 29:159–165
[CrossRef] | [PubMed]
 
Miller  E;  Berrios  GE;  Politynska  BE:  Caring for someone with Parkinson’s disease: factors that contribute to distress.  Int J Geriatr Psychiatry 1996; 11:263–268
[CrossRef]
 
Caap-Ahlgren  M;  Dehlin  O:  Factors of importance to the caregiver burden experienced by family caregivers of Parkinson’s disease patients.  Aging Clin Exp Res 2002; 14:371–377
[PubMed]
 
Thommessen  B;  Aarsland  D;  Braekhus  A  et al:  The psychosocial burden on spouses of the elderly with stroke, dementia, and Parkinson’s disease.  Int J Geriatr Psychiatry 2002; 17:78–84
[CrossRef] | [PubMed]
 
Martínez-Martín  P;  Guerrero-Díaz  MT;  Frades-Payo  B:  [Neuropsychological disorders in Parkinson’s disease: evaluating them and their impact on the caregiver].  Rev Neurol 2004; 39:639–645
[PubMed]
 
Karlsen  KH;  Larsen  JP;  Tandberg  E  et al:  Influence of clinical and demographic variables on quality of life in patients with Parkinson’s disease.  J Neurol Neurosurg Psychiatry 1999; 66:431–435
[CrossRef] | [PubMed]
 
Schrag  A;  Jahanshahi  M;  Quinn  NP:  What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 2000; 69:308–312
[CrossRef] | [PubMed]
 
Hirayama  MS;  Gobbi  S;  Gobbi  LT  et al:  Quality of life (QoL) in relation to disease severity in Brazilian Parkinson’s patients as measured using the WHOQOL-BREF.  Arch Gerontol Geriatr 2008; 46:147–160
[CrossRef] | [PubMed]
 
References Container
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