Objective To examine the longitudinal associations between caregiver strain and patients’ clinical and psychosocial characteristics as well as caregivers’ psychosocial characteristics.
Methods At 4-month intervals during the 12 months study period, longitudinal data on caregiver strain and patient and caregiver factors potentially associated with caregiver strain were collected from 126 couples, who participated in a randomised controlled trial on the effectiveness of case management in amyotrophic lateral sclerosis (ALS). Caregiver strain was assessed with the Caregiver Strain Index (CSI). Patient and caregiver factors included sociodemographic characteristics, distress, coping style and perceived quality of care, as well as the patient's functional status and emotional functioning. Multilevel regression analyses were performed.
Results Caregiver strain increased significantly during the study period (β=0.315 points/months, p<0.001) and was significantly associated with patient time-dependent factors functional status (β=−0.131 points/months, p<0.001) and emotional functioning (β=0.022 points/months, p=0.03), and caregiver time-dependent factors passive coping style (β=0.152 points/months, p=0.03), symptoms of anxiety (β=0.186 points/months, p<0.001) and perceived quality of care for the caregiver (β=−0.452 points/months, p<0.001).
Conclusions Our study has identified that apart from the patient's physical disability and emotional well-being, a passive coping style of the caregiver, increased symptoms of anxiety and feeling less supported by the ALS-team impact on caregiver strain. The multidisciplinary teams involved with the care of patients with ALS need to be aware of these factors and increase their attention for the caregiver. This will help guide the development of evidence-based supportive interventions that focus on caregiver's coping style and avoiding distress.
Trial registration number Netherlands Trial Register, number NTR1270.
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Owing to the progression of muscle weakness and the associated disease symptoms over the full course of the disease, patients with amyotrophic lateral sclerosis (ALS) become increasingly dependent on the support and care of their partner, family members and other relatives. Generally, the partner or one of the patients’ closest family members is the most important informal caregiver.1 During informal caregiving, a significant amount of time, attention and effort is devoted to the patient with ALS.1
As the disease progresses, strain on and psychological distress of informal caregivers of patients with ALS increase significantly,2–4 while caregivers’ quality of life worsens.5 Role strain due to many demands because of managing care, providing care, supporting the patient in decision-making, patient advocating and ordinary daily live responsibilities may have an impact on caregiver strain.6 ,7
Reducing the strain of informal caregivers should be a high priority in ALS care. Optimising the caregivers’ well-being is critical, not only for themselves but also for the patients.8 ,9 Knowledge about interventions which relieve caregiver strain is, however, still limited. ALS treatment guidelines and ALS literature lack evidence for interventions aimed at reducing caregivers’ adverse experiences and caregiver strain.10 ,11 In their literature review, Aoun et al12 highlighted the absence of interventions to improve care for family caregivers. From the results of cross-sectional surveys it appeared that caregivers reported shortcomings in ALS management as a reflection of caregiver strain.13 ,14
Insight into factors associated with caregiver strain may help to identify those at risk for high levels of strain and may guide the development of supportive interventions. Earlier cross-sectional studies identified various determinants of ALS caregiver strain,9 ,15–18 but fewer studies have reported longitudinal data.3 ,19 Some of the explored patient-related and caregiver-related variables might be modifiable, for example, patient's emotional lability and mental health and caregiver's distress (depression and anxiety).20 ,21 By acquiring more knowledge about specific patient and caregiver modifiable factors related to caregiver strain and the way it increases over time, we will be able to apply this to tailoring ALS care to the needs of the caregiver.
The aim of our cohort study was to identify patient and caregiver disease-related and psychosocial-related factors associated with caregiver strain over time in ALS.
Study design and population
This quantitative longitudinal cohort study was part of a cluster randomised controlled trial (RCT) that evaluated the effectiveness of case management in 132 patients with ALS and their most important informal caregiver (n=126).4 Patients were not eligible for trial entry if they had cognitive dysfunction. Patients and caregivers were excluded if they had insufficient mastery of the Dutch language.
Standard protocol approvals, registrations and patient consents
The Medical Ethics Committee of the Academic Medical Centre in Amsterdam waived the need for ethical approval. The RCT was registered at the Netherlands Trial Register, number NTR1270. Informed consent for processing their research data was obtained from all participating patients and all caregivers.4
During the 12-month study period, we assessed baseline sociodemographic characteristics of the patients and their caregivers (eg, gender, age, education). Baseline information on ALS clinical characteristics (eg, site of onset, time since onset, forced vital capacity, percutaneous endoscopic gastrostomy use and non-invasive/invasive ventilation use) was provided by the treating rehabilitation medicine consultant from the multidisciplinary ALS care team of the patient-caregiver couple. Baseline and 4-month assessments of the measurements were carried out in the homes of the participants. Baseline assessments were performed by two experienced occupational therapists and 4-month assessments by two experienced research assistants.4
Caregiver strain was measured with the generic 13-item Caregiver Strain Index (CSI), widely used in healthcare research and clinical practice.22 Caregiver strain refers to the perception of stress and fatigue caused by the sustained effort required in caring for the patient.22 The CSI is a concise instrument with dichotomous yes/no answers to propositions, to assess participants’ negative caregiving experiences. The instrument measures both the objective impact of care (eg, ‘There have been changes in personal plans’) and subjective impact (eg, ‘Feeling completely overwhelmed’). The CSI showed no ceiling or floor effects and a high internal reliability.23
We monitored disease progression with the ALS Functional Rating Scale-Revised (ALSFRS-R). The ALSFRS-R is a 48-point validated disease-specific measure to assess function, and consists of four domains: fine motor function, gross motor function, bulbar function and respiratory function. A lower total score indicates greater disability.24
We assessed emotional aspects of the patient's health-related quality of life (QOL) with the Dutch version of the 40-item ALS Assessment Questionnaire (ALSAQ-40), domain emotional functioning. The ALSAQ-40 is a disease-specific health status measure, containing 40 items incorporated in five distinct areas of health: physical mobility (10 items), activities of daily living/independence (10 items), eating and drinking (3 items), communication (7 items) and emotional functioning (10 items). Each of the 5 scales is transformed into a scale of 0–100 (100 indicating poorest health).25
Perceived quality of care (QOC) of the total ALS care provided, was rated by patients and their caregivers on a 10-point numerical rating scale; 1 representing very poor QOC and 10 as excellent QOC. Caregivers were asked to give two ratings: one for the care provided to the patient, and one for the care provided to themselves.
As indicator for emotional distress, we used the Hospital Anxiety and Depression Scale (HADS).26 The HADS is a patient-reported outcome measure, developed as a screening instrument for use in hospital outpatient departments and has been validated for use with primary care patients and the general population. The HADS comprises 14 items divided equally between the two mood states (anxiety and depression). Participants were asked to rate items on anxiety and depressive symptoms during the previous week on a four-point scale (0–3), rendering a maximum score of 21 points for each subscale. A higher score indicates more distress.
Coping strategy was assessed with the Utrecht Coping List (UCL).27 The UCL consists of seven subscales, each representing a different coping strategy: active approach, palliative response, avoidance, seeking social support, passive reaction, expression of emotions and reassuring thoughts. We used the subscales active approach and passive reaction, as these represent the conceptualisation of adaptive and maladaptive coping styles.28 ,29 An active approach coping style is an active, offensive strategy to handle experienced problems and is considered as an adaptive coping style, whereas a passive reaction coping style is considered as a defensive, reactive coping strategy that is regarded as maladaptive.29 Both subscales consist of seven items scored on a four-point scale (1–4). We used the sum scores of these subscales in the analyses. Higher scores on the scale indicate that the particular coping strategy is used more often. The UCL showed moderate to good internal consistency (Cronbach's α 0.43–0.89) and test–retest reliability (r=0.37–0.85).27
Normality of the data was checked by plotting histograms and by means of a Kolmogorov-Smirnov test. We measured baseline correlations between patients’ and caregivers’ variables and the CSI total score using Pearson's correlation coefficients.
The longitudinal course of caregiver strain and its association with patients’ and caregivers’ variables were analysed with random coefficient analysis. This analysis technique does not require complete follow-up data from all participants. Consequently, data of all participants, including those with incomplete sets, were analysed. First, we investigated time-independent and time-dependent factors for their bivariate association with caregiver strain.
Second, we built a multivariate model in which we included patients’ variables significantly associated with caregiver strain, and another model in which we included caregivers’ variables. Each model included time (as a continuous variable in months) and time squared to capture linear and non-linear course. Furthermore, within each model we explored whether the ALSFRS-R sum score was statistically significant in terms of the association with caregiver strain over time. In order to account for individual trajectories of caregiver strain, we used a random intercept (and slope). A random slope was only included if this improved the model fit (based on the likelihood ratio test). We employed a backward selection on the variables (based on the Wald test) to exclude all variables with a p value greater than 0.1.
Third, the remaining patient and caregiver variables together with time (linear and quadratic) were combined in a final association model. Variables with a p value greater than 0.05 were eliminated, resulting in the best model for patients’ and caregivers’ determinants associated with caregiver strain.
For the descriptive statistics we used SPSS V.22.0 software and for the random coefficient analyses MLwiN (MLwiN V.2.32, Centre for Multilevel Modelling, University of Bristol, UK).
Table 1 presents baseline descriptive statistics of the sociodemographic and clinical characteristics of the 126 informal caregivers and patients with ALS who participated in our study. One hundred and seven caregivers were spouses of the patients with ALS, 10 caregivers were sons or daughters and 66% of the caregivers were female. The flow chart of participants (figure 1) shows the number of assessments and the reason why data were missing at each time point.
Scores of participants’ time-dependent variables at the four assessments are presented in table 2. Analyses of the time-independent and time-dependent factors associated (univariate and bivariate, respectively), with caregiver strain resulted in five caregiver variables: age at inclusion; HADS anxiety and depression; QOC care for the caregiver; UCL passive reaction, and seven patient variables: age at inclusion; ALSAQ-40 domain emotional functioning; ALSFRS-R sum score; QOC care for the patient; HADS depression; UCL active approach and passive reaction. Table 3 presents the longitudinal association with CSI total score for each independent variable separately.
Multilevel analyses showed that caregiver strain increased significantly during the study period. Time and time squared were significant, although the size of the β for the quadratic time trend was very small compared to that for the linear term (β −0.008 (SE 0.002) versus 0.299 (SE 0.053)) indicating only a slight deviation from a linear trend. Increase in caregiver strain was associated with the patients’ time-dependent variables ‘disease severity’ and ‘ emotional functioning’, and with the caregivers’ time-dependent variables ‘anxiety’, ‘perceived quality of care for themselves’ and ‘passive coping style’ (table 4).
Our longitudinal study has shown that apart from factors relating to the patient's physical disability and emotional functioning, caregiver's coping behaviour, anxiety and perceived quality of care for the caregiver have an impact on caregiver strain in ALS.
The positive association we found between caregiver burden and the patient's physical limitations is in agreement with previous ALS studies,2 ,9 ,16 as well as with studies in other progressive neurological disorders.30 Some studies could not, however, corroborate the impact of physical limitations on caregiver strain.15 ,17 ,19 This inconsistency might be explained by methodological differences (univariate vs multivariate associations).
We found that caregivers of patients with better emotional functioning perceived less strain. As far as we could ascertain, our study is the first to reveal evidence for this association. We believe that this finding is of importance for improving multidisciplinary ALS care with respect to QOL of the patient and caregiver strain.11 Therefore, interventions targeting patient's emotional problems aimed at optimising QOL is a real challenge for the multidisciplinary care team and community care professionals, the development of support programmes should be prioritised.
This study showed that caregivers who used more passive coping strategies experienced higher levels of strain, a finding in line with results of Weisser et al's31 longitudinal study, in which caregivers described becoming (pro)active in dealing with the situation as ‘helpful’. We suggest that interventions aimed at providing insight into how caregivers cope with the negative changes in their situation and at finding effective (active) coping strategies may lead to manageable strain.
The current study supports previous findings that lower QOC for the caregiver is associated with higher strain, which indicates the importance of high-quality ALS care for the caregiver during the disease stages. All participating patients and caregivers received support from a multidisciplinary ALS care team in accordance with the gold standard treatment for patients with ALS. Within our cohort, both patients and caregivers rated the overall quality of ALS care as moderate to good. Nevertheless, caregivers experienced lower QOC for themselves compared to QOC for the patients. Bakker et al32 in their qualitative study reported that some patients and caregivers perceived the QOC of their ALS team to be suboptimal. Other studies showed that family members of patients with ALS search for practical and emotional support from their healthcare professionals.13 ,14 ,33 Caregivers who experienced the specialist ALS clinic as being supportive, mentioned that this helped them to cope with the situation.34 For ALS care professionals, a shortcoming in multidisciplinary ALS care is the availability of specific evidence-based interventions to guide the family caregivers.11 Caregiver strain should be recognised by the care professionals and tailor-made interventions to prevent or reduce strain, fitting the needs of the caregivers, should be developed, validated and implemented.
Reduced caregiver distress contributes to managing the caregiver's situation and thus decreasing strain.33 In line with these caregiver experiences, our study showed that higher levels of caregiver anxiety were associated with higher levels of caregiver strain. Previous cross-sectional studies also reported a positive relation of caregiver anxiety with caregiver strain.15 ,16 The caregivers’ anxiety scores in these studies were comparable to our results, although all studies used different (types of) anxiety questionnaires. During the patient's disease trajectory, particular attention to the caregiver's symptoms of distress is needed to offer timely interventions to alleviate caregiver strain. Previous intervention studies within dementia and cancer showed improvements in distressing caregiver symptoms like mood and coping associated with strain.35
The strengths of our study include the large sample of patients and their caregivers, the data collection over a 1 year follow-up period and the random coefficients model for data analysis.
The results of our study must be viewed in the context of the Dutch ALS care setting—all patients and caregivers were supported by a multidisciplinary ALS care team and by their primary healthcare professionals. In the Netherlands clinical practice guidelines do not provide specific supportive interventions for caregivers in ALS but emotional and psychological support is available within the Dutch ALS care setting. We did not monitor the content and frequency of psychological or emotional support participants received within the multidisciplinary or primary care setting, but emotional functioning of the patient participants was rated as almost uncomplicated and did not worsen over time. In addition, the relatively low to moderate levels of caregiver strain and patients’ and caregivers’ anxiety and depression suggest that in general the Dutch multidisciplinary ALS care is for patients as well as caregivers of a high standard.
Neither this nor previous longitudinal studies concerning caregiver strain investigated an inception cohort, with the disadvantage of limitations in the comparability of the results due to the different time points in the disease trajectory of the patients. Our study was representative with respect to patients’ baseline characteristics (age, bulbar onset, time to diagnosis, gender) for the total ALS population in the Netherlands.36 Furthermore, the sociodemographic characteristics of the caregivers studied were comparable to those of previous prospective ALS studies.2 ,19 The proportion of non-Caucasian participants might not be representative for the total ALS population. The strain experienced by non-Caucasian caregivers of patients with ALS has not been the subject of previous studies. The results within this subgroup might differ as differences in cultural, spiritual and religious beliefs could affect coping styles, experienced distress and care needs.37
This study was conducted alongside the RCT on case management for patients with ALS and their most important caregivers.4 Patients with neurobehavioural symptoms were excluded from participation in the case management study. We did not assess our patients’ neurobehavioural symptoms during the study period and hence did not investigate the association with caregiver burden. Previous ALS studies showed an association of caregiver strain with neurobehavioural changes in the patient.15 ,21 Caregiver intervention, aimed at improving the way neurobehavioural changes are dealt with might reduce caregiver strain, but requires further study.38 Studies reviewing interventions in caregivers of patients with dementia that require an active participation of caregivers, such as psychoeducation, counselling, cognitive behavioural therapy and mutual support groups, showed a reduction in caregiver stress or burden and caregivers highly appreciated supporting interventions.39
Our study focused on aspects of caregiver strain and ignored the positive aspects of caregiving.32 Taking care of a loved-one can apparently give the caregiver the feeling of doing a good job which in turn contributes positively to coping with the demands of caregiving.40 It is important to consider both positive and the negative aspects when offering caregiver support. The currently available ALS-specific and generic caregiver strain measurement instruments should be validated for the ALS caregiver population, to quantify this phenomenon and to use this new knowledge in ALS caregiver studies.
Conclusions and clinical implications
Our findings demonstrate that apart from the patient's physical disability and perceived emotional functioning, caregiver's coping behaviour, psychological distress and perceived quality of care for the caregiver is related to their perceived strain. In addition to attention and support for the caregiver, care professionals should be aware of the modifiable factors that are potentially amenable to interventions to help caregivers actively cope with their changing role and their impending overload, thus contributing to a higher QOC. The strong association between strain on and perceived QOC for the caregiver indicates the importance of the quality of ALS care during the disease stages. Psychoeducational interventions are required to provide caregivers with insight into their (potential) mental imbalance related to strain and anxiety, and stress-management strategies should be implemented to help them deal with their tasks and responsibilities. Also in the interest of the caregiver, future studies might focus on tailor-made support with respect to the emotional well-being of the patient with ALS.
The authors thank the participating patients and their caregivers; the recruiting rehabilitation medicine consultants; the participating rehabilitation medicine consultants, Gerda Valk, research nurse (University Medical Centre Utrecht) and Kim Bibbe, psychology student (University Medical Centre Utrecht), who conducted the outcome assessments; and Tim Zandbelt (University Medical Centre Utrecht) and Hermieneke Vergunst (University Medical Centre Utrecht), who conducted data entry.
Contributors HC made substantial contributions to the design of the study, the interpretation of data and drafted the article. AB performed the data analyses and made substantial contributions to the interpretation of data and to the revision of the article. All other authors (SdM, JHV, FN and LHvdB) made substantial contributions to the study design and interpretation of data and revised the article critically for important intellectual content. LvdB, as guarantor takes full responsibility for the data, the analyses and interpretation and the conduct of the research. He and the first author (HC) have full access to all of the data. The procedures we followed were in accordance with the ethical standards of the Medical Ethics Committee of the tertiary academic diagnostic centres in the Netherlands. All patients and their caregivers took part on a voluntary basis.
Funding The research leading to these results has received funding from the Netherlands organisation for Health Research and Development (ZonMw), support grant No 1150.0008, and the Netherlands ALS Foundation.
Competing interests HC, JHV, FN, LHvdB and AB received support from the Netherlands Organization for Health Research and Development (ZonMw), support grant No 1150.0008. FN serves on the editorial board of the Journal of Rehabilitation Medicine and the scientific advisory board of the Anna Fund. LHvdB received travel grants and consultancy fees from Baxter; serves on scientific advisory boards for Prinses Beatrix Spierfonds, Thierry Latran Foundation and Biogen Idec; serves on the editorial board of Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration and the Journal of Neurology, Neurosurgery & Psychiatry; and received research support from the Prinses Beatrix Spierfonds, Netherlands ALS Foundation, VSB Fonds, Adessium Foundation, the European Community's Seventh Framework Programme (FP7/2007–2013) under grant agreement no. 259867 and the Netherlands Organization for Health Research and Development (ZonMw). The authors alone are responsible for the content and writing of the paper.
Provenance and peer review Not commissioned; externally peer reviewed.
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