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Abstract

Background: Recent attempts to standardise the definition of Mild Cognitive Impairment (MCI) in Parkinson’s disease (PD) by the Movement Disorder Society Task Force has led to a greater understanding of this entity but to date, there has been a paucity of research regarding the impact of PD-MCI on caregiver outcomes.

Objective: The aim of this study was to utilise the newly established PD-MCI diagnostic criteria to investigate caregiver outcomes in relation to four specific aspects: (1) caregiver burden, (2) quality of life (QoL), (3) caregiving experience, and (4) psychological distress.

Methods: This study included a total of 166 patient-caregiver dyads. Caregiver outcomes including quality of life, caregiver burden, mood disturbances, and caregiver experience were compared between caregivers of PD patients classified as having normal cognition (PD-NC) and PD-MCI.

Results: Despite the two groups being matched on demographic and clinical features, caregivers of PD-MCI patients reported a lower level of QoL with regard to physical health and more interruptions with usual activities. On the other hand, a higher impact on finances was reported in caregivers of PD-NC patients, relative to caregivers of PD-MCI patients.

Conclusions: This study has shown that even at earlier stages of cognitive impairment, PD-MCI caregivers already experience elevated levels of distress in the role of providing care to their care-recipients. These findings highlight the need to include management of caregiver distress and associated sequelae alongside the management of PD-MCI patients, early on in the disease course.

Keywords

Mild cognitive impairment Parkinson’s disease caregiver burden quality of life caregiver outcomes

INTRODUCTION

Mild Cognitive Impairment (MCI) is characterised as a transitional state between normal ageing and dementia that has been increasingly recognised across a number of patient populations [1, 2]. Broadly speaking, individuals with MCI present with cognitive deficits in the context of preserved capacity for daily functioning [1]. In Parkinson’s disease (PD), PD-MCI can be present even at the time of initial diagnosis, and represents a significant risk factor for the development of dementia (PDD) [3]. Recent attempts to standardise the definition of PD-MCI by the Movement Disorder Society (MDS) Task Force [4] has led to a greater understanding of this relationship but to date, there has been a paucity of research regarding the impact of PD-MCI on caregivers. This issue has clinical relevance as caregivers play a pivotal role in providing physical and emotional support to PD patients [5, 6]. Such responsibilities can often bring about emotional and social distress within caregivers [7, 8] in addition to considerable lifestyle or financial changes, and may prompt early institutionalization when these stressors become overwhelming [9, 10]. Therefore, as part of the treatment and management process, it is important to identify and target factors associated with caring for PD patients that specifically impact on caregivers’ wellbeing.

Notably, caregivers often have a unique perspective from which to detect subtle cognitive changes in their care-recipients [11, 12], which makes their report of such changes particularly useful in assisting early screening and intervention approaches for PD patients [11]. In particular, caregivers of PD-MCI patients may represent a cohort with increased risk of heightened distress, given their need to cope with cognitive impairments and potentially persistent cognitive decline in addition to the typical motor symptoms associated with PD.

Previous research has documented that caring for PD patients with dementia (PDD) is associated with an increased level of burden and stress [13, 14], which can be even greater than that observed in caregivers of Alzheimer’s disease patients [15]. However, it remains unclear whether PD-MCI has a similar impact on caregivers. Only one study has previously explored this issue where the investigators assessed caregiver burden using the Zarit Burden Interview (ZBI) in PD patients classified as having normal cognition (PD-NC), PD-MCI, and PDD [13]. In that study, the investigators reported a similar level of burden reported within caregivers of PD-NC and PD-MCI patients but significantly higher burden in caregivers of PDD patients. However, no additional measures were employed to gauge other caregiver outcomes. Therefore, the aim of the present study was to utilise the newly established diagnostic criteria for PD-MCI (Level 1 criteria) to investigate caregiver outcomes in relation to four specific aspects: (1) caregiver burden, (2) quality of life (QoL), (3) caregiving experience, and (4) psychological distress.

MATERIALS AND METHODS

Participants

This study included a total of 166 patient-caregiver dyads from the Parkinson’s Disease Research Clinic at the Brain and Mind Centre, University of Sydney. Caregivers included anyone living with a PD participant and providing informal care, whether they were a spouse, relative, or friend. All patients underwent neurological and neuropsychological assessment as previously reported elsewhere [16], while all caregivers were asked to complete self-reported measures including demographic questions (e.g. relationship with PD patient, employment status, and educational level) and psychometric questionnaires (see below). The research was approved by the Human Research Ethics Committee of the University of Sydney, and written informed consent was obtained from all PD participants and their caregivers.

Clinical assessment of PD patients

The diagnosis of idiopathic PD was based on the United Kingdom Parkinson’s Disease Society (UKPDS) Brain Bank criteria [17], and was confirmed by a neurologist (SJGL). The neurological evaluation rated participants according to Hoehn & Yahr (H & Y) stage, and assessed them on the revised MDS Task Force Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) [18]. Details of age at disease onset, symptoms at onset, disease duration, and medications were also recorded.

Neuropsychological assessment

All patients underwent a neuropsychological battery comprising the following tests: the revised National Adult Reading Test (NART; an estimate of premorbid intellectual functioning), Mini-Mental State Examination (a measure of global cognitive function), Trail Making Test A (total time; attention/visuomotor processing speed), Trail Making Test B (total time; executive functioning), digit span subtest from the Wechsler Adult Intelligence Scale-III (total score; working memory), Logical Memory I (total score; memory), Logical Memory II (delayed recall total; memory), Controlled Oral Word Association Test phonemic fluency (letters: FAS; executive functioning), and Controlled Oral Word Association Test semantic fluency (animals: total score; language) [16].

Diagnosis of PD-MCI

Raw scores for each cognitive measure were transformed to z-scores based on appropriate age- and/or education-matched normative data. In order to determine the presence and magnitude of cognitive impairment for each individual, NART scores were also transformed to z-scores to allow for a direct comparison with individual test scores [16]. As stipulated in the MDS guidelines [4], PD-MCI was diagnosed when (1) impairment was observed on two or more neuropsychological tests, defined by at least 1.5 standard deviation (SD) below premorbid level of cognitive functioning, and (2) subjective cognitive problems were reported by patients or family members as defined by a score of 1 or more on item 1 (cognitive impairment) of the MDS-UPDRS part I [16]. The utilization of a cut-off score of 1.5SD below premorbid level of cognitive functioning rather than 1.5SD below normative data was based on previous suggestion that a comparison between current cognitive functioning and normative data (without allowing for premorbid intellect) may lead to poor sensitivity and specificity in those with high and low premorbid intellect respectively (e.g. falsely inflating MCI rates among lower functioning individuals) [16]. Sub-classification of PD-MCI (e.g. into amnestic or non-amnestic domains) was not performed as this may only be completed when utilizing a Level 2 criteria neuropsychological battery.

Patient self-report measures

Questionnaires were utilised to investigate whether PD-NC and PD-MCI patients were matched on their level of psychological symptoms, as previous studies have suggested the presence of non-motor symptoms in PD is associated with greater caregiver burden [14]. The Hospital Anxiety and Depression Scale (HADS) is an established questionnaire comprising fourteen items that measure anxiety and depression symptoms [19]. Scores are scaled between 0 and 21 for each domain, with higher scores indicating higher levels of psychological distress. The Epworth Sleepiness Scale (ESS) [20] was used to measure daytime sleepiness. Scores are scaled between 0 and 24, with higher scores indicating higher levels of daytime sleepiness. To identify patients with possible rapid eye movement (REM) sleep behaviour disorder (RBD), the REM Sleep Behaviour Disorder Screening Questionnaire (REMSBD) was used. Scores range between 0 and 13, with a cut-score of ≥5 indicating the likely presence of RBD [21]. Severity of psychotic and compulsive symptoms was derived from the Scales for Outcomes in Parkinson’s disease-Psychiatric Complications (SCOPA-PC) [22], which comprise seven items. Scores range from 0 to 21, with higher scores indicating greater symptom severity.

Caregiver self-report measures

The World Health Organisation Quality of Life Scale BREF version (WHOQoL-BREF) [23] was used to measure caregivers’ QoL. The questionnaire consists of 26 items covering QoL within the following four domains: (1) physical health, (2) psychological health, (3) social relationships, and (4) environment. Scaled scores on the WHOQoL-BREF range from 0 to 100, with higher scores indicating better QoL. Data from a caregiver’s questionnaire was considered missing when >20% of data were absent. As stipulated in the WHOQoL-BREF test manual, a domain score was not calculated when >2 items were missing from that domain (with the exception of the social relationship domain, where it was only calculated when ≤1 item was missing).

Caregiver burden was derived from the ZBI questionnaire [24], which consists of 12 items. Scores range from 0 to 48, with a higher score indicating higher levels of burden. In addition, the Caregiver Reaction Assessment Scale (CRA) [25] was used to evaluate caregivers’ reactions to the experience of caring for a PD patient. The questionnaire consists of 24 items covering the following five dimensions: (1) caregiver’s esteem, which measures how the individual’s self-esteem is affected by caregiving, (2) impact on finances, which assesses strain of the financial situation on the caregiver and the family, (3) lack of family support, which measures whether the caregiver perceives support from family members to be adequate, (4) impact on schedule, which measures the extent to which caregiving interrupts usual activities, and (5) impact on health, which measures if the caregiver is physically capable of and has the energy to provide care. Psychological distress in caregivers was also measured using the HADS [19].

Statistical analyses

All continuous data was assessed for normality. Significant outliers, as defined by z-scores of > ±3, were excluded from analyses. Comparison of demographic and clinical variables between the two groups based on the presence or absence of PD-MCI in their corresponding patient dyad (i.e. PD-NC versus PD-MCI) was assessed using either an analysis of variance (ANOVA) or the Mann-Whitney U test (depending on whether the variable met parametric assumptions). For the categorical measures of gender and caregiver education, the Chi-square (χ²) test was used. A step-wise backward binary logistic regression analysis with PD-NC or PD-MCI caregiver entered as the dependent variable was performed to investigate whether caregiver type could be distinguished by the following variables: WHOQoL-BREF: physical, psychological, social relationships, and environmental domain, CRA: esteem, lack of family support, impact on finances, impact on schedule, and impact on health domain, as well as HADS: anxiety and depression domains. All analyses employed an alpha level of p < 0.05 and were two-tailed.

RESULTS

Demographic and clinical characteristics

Table 1 presents the descriptive statistics for caregiver demographics. There were no significant differences between caregivers of PD-MCI and PD-NC patient in demographic features. Forty-seven individuals (28%) with PD were classified as PD-MCI. There were no significant differences between PD-MCI and PD-NC patients in demographic and clinical features (see Table 2).

Caregiver measures

Variables that distinguished caregivers of PD-MCI and PD-NC patients involved: (1) WHOQoL-BREF: physiological domain, (2) CRA: impact on finances domain, and (3) CRA: impact on schedule domain (see Table 3). In particular, caregivers of PD-MCI patients reported a lower level of QoL with regard to physical health, and more interruptions with usual activities than caregivers of PD-NC patients. A higher impact on finances was reported in caregivers of PD-NC patients, relative to caregivers of PD-MCI patients. There were no significant differences between caregivers in the two groups in the following measures: WHOQoL-BREF: psychological, social relationships, and environmental domain, CRA: esteem, lack of family support, and impact on health domain, as well as HADS: anxiety and depression domains.

DISCUSSION

To date, only one study has examined the issue of caregiver burden specifically in PD-MCI patients [13]; however, that study did not examine other caregiver outcomes in this regard. The present study has therefore extended our understanding of caregiver outcomes in relation to burden, QoL, caregiving experience, and psychological distress in people living with and caring for patients classified as PD-MCI according to the recently proposed MDS Task Force PD-MCI criteria. Results from the current study showed that despite the two groups being matched on demographic and clinical features, caregivers of PD-MCI patients reported a lower level of QoL with regard to physical health and more interruptions with usual activities.

We anticipate that the degree of impact on QoL and caregiving experience reported by caregivers of PD-MCI patients in the present study is perhaps likely to be milder than that which might be reported by caregivers of PDD patients [13], given the known, considerable functional impairment (and subsequently reduced independence) in patients with established dementia. Nevertheless, the current findings, demonstrating that caregivers of PD-MCI are already experiencing a lower level of QoL with regard to physical health and more interruptions with usual activities at earlier stages of cognitive impairment, are striking. Given that PD-MCI is associated with a heightened risk of developing PDD, it is plausible that many of these PD-MCI caregivers will eventually become PDD caregivers. In the face of increasing cognitive limitations, PD-MCI patients may require additional assistance with daily living, which may provoke distress and burden in their caregivers [26]. Therefore, interventions to reduce the degree of impact on caregiver outcomes at the very earliest stages of the patient presenting with a possible dementing condition may help to preserve caregivers’ wellbeing for longer periods, and may have the wider societal benefit of reducing or delaying rates of institutionalization [26].

In this vein, a number of studies have been carried out to investigate the efficacy of intervention programs for PD caregivers (for a review, see Martinez-Martin et al. [27]). In general, results from these studies are encouraging, with reported improvements in caregiver strain [28], caregiver burden [28, 29], and mood [30] amongst others. These results further merit the application of intervention programs for PD-MCI caregivers. Importantly, given that the functional changes in patients with PD-MCI pose a unique set of challenges to caregivers, such intervention programs should be tailored to match caregivers’ needs. As shown in the present study, a lower level of QoL with regard to physical health and more interruptions with usual activities were reported in caregivers of PD-MCI than those of PD-NC patients. These results have implications for the areas of assistance that PD-MCI caregivers might require. Perhaps future interventions developed for this purpose could target specific aspects of impact, such as caregivers’ health concerns relating to PD-MCI caregiving, in order to maximize their wellbeing. Further research exploring areas that require enhanced assistance and support in PD-MCI caregivers would be an important future direction for the development of caregiver intervention programs.

In addition to intervention programs for PD-MCI caregivers, having access to PD nurse specialists (i.e. specialist practitioners with essential skills in the assessment and management of PD symptoms) in the community is likely to help alleviate caregiver burden via providing information, education, and ongoing support to individuals caring for PD patients [31, 32]. Through additional information provided to caregivers, PD nurse specialists can potentially help delay the institutionalization of patients with PD.

Similar to results from Leroi et al. (2012) [13], the present study found the level of caregiver burden to be similar amongst those caring for patients with PD-MCI and PD-NC. Considering that PD-MCI patients have relatively preserved capacity for daily functioning, it is possible that the amount of assistance they require from their caregivers may not be significant enough to translate to upheavals in perceived caregiver burden. Future studies with longitudinal follow-up of PD-MCI patients and their caregivers may allow a better understanding of the trajectory of caregiver burden over time. In addition, the present study found that caregivers of PD-NC patients reported more financial strain in relation to the caregiving experience than those of PD-MCI patients. It remains to be investigated what factors contributed to this finding. Such difference could be attributed to caregiver factors such as financial stability and awareness of available resources to lessen their financial burden. This warrants the exploration of the association between caregiver factors (e.g. socio-demographic factors, access to resources and services) and different aspects of caregiver outcomes.

LIMITATIONS

One of the limitations of this study relates to the disparity in sample size in the two groups (PD-MCI: 47 versus PD-NC: 119). Indeed, the smaller sample size in the PD-MCI caregiver group could have potentially undermined statistically significant differences in caregiver outcomes between the two groups. Nevertheless, such disparity is more likely to be reflective of the rate of MCI in the PD population [16]. Future studies with larger sample sizes are needed to increase statistical power and to better understand caregiver outcomes in caregivers of PD-MCI patients.

This study employed Level 1 diagnostic criteria for PD-MCI, and therefore MCI subtyping (e.g. amnestic versus non-amnestic) was beyond the current scope of research conducted here. An exploration of caregiver distress amongst MCI subtypes may have clinical relevance for management planning in PD-MCI as PD patients with amnestic versus non-amnestic MCI subtypes may experience different functional sequelae. However, the administration of a more comprehensive battery of neuropsychological tests may not always be practical or available due to the longer administration time required to characterise cognitive impairment in more detail, and the associated increased possibility of fatigue (particularly in this population) [16]. Another limitation of this study relates to the reliance on self-report questionnaires to investigate caregiver distress. It is possible that more detailed insights can be gained via structured clinical interviews. However, it is important not to overload caregivers given the clear time constraints imposed on them, and questionnaires were therefore selected as the mode of investigation in this exploratory study. On a related note, future studies could also employ a caregiver-specific QoL measure to investigate more subtle issues experienced by caregivers.

CONCLUSION

In conclusion, while the negative impact of PDD on caregiver outcomes has been established in previous studies, its impact on PD-MCI caregivers has to-date, remained unclear. The present study has shown that even at this earlier stage of cognitive impairment, PD-MCI caregivers are already experiencing an elevated level of distress in the role of providing care to their care-recipients. These findings highlight the need to include management of caregiver distress and its associated psychological aspects alongside the direct management of PD-MCI patients.

CONFLICT OF INTEREST

The authors have no conflict of interest to report.

FINANCIAL DISCLOSURES OF ALL AUTHORS

JYY Szeto has no financial disclosures.

Dr L Mowszowski is supported by a National Health and Medical Research Council (NHMRC) – Australian Research Council Dementia Research Development Fellowship (IDs 1109618).

M Gilat is supported by an International Postgraduate Research Scholarship at the University of Sydney.

CC Walton is supported by an Australian Postgraduate Award at the University of Sydney.

Prof SL Naismith is supported by a NHMRC Career Development Fellowship (ID 1008117).

Prof SJG Lewis is supported by a NHMRC Practitioner Fellowship (ID 1003007).

Footnotes

ACKNOWLEDGMENTS

We thank the patients of the Parkinson’s Disease Research Clinic for being so generous with their time and efforts.

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Mild Cognitive Impairment in Parkinson’s Disease: Impact on Caregiver Outcomes

Abstract

Keywords

INTRODUCTION

MATERIALS AND METHODS

Participants

Clinical assessment of PD patients

Neuropsychological assessment

Diagnosis of PD-MCI

Patient self-report measures

Caregiver self-report measures

Statistical analyses

RESULTS

Demographic and clinical characteristics

Caregiver measures

DISCUSSION

LIMITATIONS

CONCLUSION

CONFLICT OF INTEREST

FINANCIAL DISCLOSURES OF ALL AUTHORS

Footnotes

ACKNOWLEDGMENTS

References