Abstract
Objective: To analyze the quality of life (QoL) and frequency of depression in primary caregivers of patients with amyotrophic lateral sclerosis (ALS) in two neighboring European countries. Methods: a cross-sectional study performed in 164 dyads of ALS patients and caregivers followed at clinical ALS centers in Poland and Germany between 2015 and 2018. The quality of life (Anamnestic Comparative Self-Assessment - ACSA, Quality of Life in Life-Threatening Illness - Family Carer Version - QOLLTI-F) and depression (ALS-Depression-Inventory 12-Items - ADI-12) of the caregivers was assessed and correlated with caregivers- and patient-related factors. Patient’s clinical status was assessed by ALS Functional Rating Scale – revised and the Behavioral Score of the Edinburgh Cognitive and Behavioral ALS Screen. Results: the caregivers reported a positive QoL associated with functional and behavioral status of the patient, disease duration and caregivers’s depression The most impaired domains of the QoL differed depending on the country of provenance, cultural background and/or social support of the caregivers. Depression was present in 1/3 of the caregivers and was significantly more frequent in the Polish group. It positively correlated with female gender, disease duration, sleep disturbances and functional decline. Both QoL and mood were significantly lower in the caregivers more burdened with the functional care of the patients. Conclusions: the wellbeing of caregivers of ALS patients is affected by patient-related and culture-specific conditions. Understanding the needs and background of psychological adaptation of the caregivers from various countries may translate into better QoL and local patient care.
Introduction
Amyotrophic lateral sclerosis (ALS) relentlessly leads to impairment of manual activity and gait (Citation1), with bulbar symptoms altering communication and food intake (Citation2,Citation3). The communication may additionally be affected by deterioration of language skills due to cognitive impairment, observed in approximately 40% of patients (Citation4). Up to 15% of ALS patients develop frontotemporal dementia with compromised memory, awareness of the disease, compassion and inappropriate social behavior (Citation5). The above symptoms lead to a gradual dependence on caregivers (Citation6). The majority of primary caregivers are closely related to ALS patients or emotionally involved (Citation7). Initially, the care focuses on maintaining patient’s independence, facilitating motion and daily activities. Along the disease progression, the caregivers acquire more responsibilities, from feeding the patient, performing hygienic activities, to the patient’s displacement (Citation8). The caregivers are involved in providing multidisciplinary care - coordination of medical appointments, physio- and speech therapy, provision of pharmacological agents and fulfilling equipment needs (Citation9). High physical and emotional burden may lead to anxiety, depression and reduction of the QoL of the caregivers (Citation10). It is particularly pronounced in cases of rapid disease progression and/or cognitive impairment (Citation11–13). Longitudinal studies show that the cognitive dysfunction (i.e. disinhibition, impulsivity), rather than the disease progression per se negatively influences the caregivers’s QoL (Citation14). Besides, the presence of caregiver-reported behavioral symptoms predict clinical progression of ALS (Citation15).
Understanding the needs of the caregivers may improve their well-being and positively affect the quality of care (Citation15–17). Since we have previously found important inter-cultural differences in the end-of life decision process (Citation18) and the QoL and depression of ALS patients from different European countries (in press), our hypothesis was that the general burden of care in the patient’ caregivers may differ between societies. The aim of the study was to analyze the QoL and frequency of depression in primary caregivers of patients with ALS in Poland and Germany, two neighboring European countries, with different cultural background. The results in each country were to be correlated with caregivers- and patient-related factors.
Materials and methods
The study was performed in 164 dyads of ALS patients and caregivers followed at the Department of Neurology, Medical University of Warsaw (n = 80) and University of Ulm (n = 84). The study subjects were consecutively recruited among ALS patients coming to out-patient visits or hospitalized to confirm the primary diagnosis. The interviews were performed between 2015 and 2018 with the use of standardized questionnaires and those designed within the JPND Needs in ALS project (www.NEEDSinALS.com). Inclusion criteria were: the diagnosis of clinically definite, probable or possible ALS according to the El Escorial criteria (Citation19), and the time from the diagnosis of over 3 months. Exclusion criteria included major cognitive impairment, additional neurological or psychiatric conditions, locked-in state and atypical motor neuron disease. Demographic characteristics of patients and caregivers are presented in and . The patients’ functional assessment was performed with Amyotrophic Lateral Sclerosis Functional Rating Scale-Revised (ALSFRS-R), which included 12 functional items concerning bulbar, limbs, trunk and respiratory functions (each item scored from 0 - unable to 4 - normal) (Citation20). Behavioral function was assessed using the caregiver survey component of the Edinburgh Cognitive and Behavioral ALS Screen (ECAS-BS); maximal 10 points for disinhibition, apathy, loss of empathy, perseverative and altered eating preferences (Citation21). The clinical assessment included the disease duration (time from symptoms onset to the survey) and the time from diagnosis in months. In both patients and caregivers, the QoL was assessed by Anamnestic Comparative Self-Assessment (ACSA) evaluating current global QoL compared with the worst and the best time in one’s life, judging from −5 to +5; values >0 indicate positive QoL, ranging from “1 = a bit good” to “5 = just as good as my best times” and <0 indicate negative QoL, ranging from −1 =a bit bad” to −5=“as bad as my worst times in my life”; 0 indicates neutral QoL compared to the best and worst times (Citation22). Caregivers’ QoL was additionally defined using Quality of Life in Life-Threatening Illness - Family Carer Version (QOLLTI-F) questionnaire, where the total score was the mean of the scores in 7 domains and their subscale scores (with 0 indicating the worst and 10 the best situation) (Citation23). The domains included: environment (place, privacy), patient state (anxiety about the patient’s condition), caregiver’s own state (control, time to care for self, thinking clear, physical wellbeing, emotional well-being), caregiver’s outlook (feelings about being a carer, spirituality comforting, meaning in life), relationships (with patients and others), quality of care (decision-making, quality of healthcare) and financial concerns. Caregiver’s depression was examined by the ALS-Depression-Inventory 12-Items (ADI-12; range 12–48 and >28 cutoff for clinically relevant depression) (Citation24), which is a short version of the Beck depression inventory II (Citation25). The amount of help provided by the caregivers was analyzed based on questions considering the percentage of time the caregivers devoted to help (<50% vs ≥50% of their entire time), and included: 1) functional care – supporting mobility, dressing and hygiene and preparing meals, and 2) emotional help - conversations and psychological support. The caregivers were also asked a binary question on the presence or absence of sleeping disturbances.
Table 1 Demographic characteristics of caregivers of patients with amyotrophic lateral sclerosis.
Table 2 Demographic characteristics of patients with amyotrophic lateral sclerosis.
The study was approved by the institutional Ethical Committees (KB/138/2013 and 19/12). Each participant signed a written informed consent prior to participation in the study.
Statistical analyses
Statistical analysis was performed using SPSS version 18. The demographic characteristics are reported as frequencies and percentages for categorical data, and means with a standard deviation for continuous variables. Comparison of mean values were evaluated with Student’s t-test; binary correlation was evaluated with Pearson’s correlation. In some measurements, due to the large difference in the numbers of both subgroups, only the Mann-Whitney test was used. The power analysis was previously described (Citation18).
Results
The majority of caregivers were females (67.7:33.3% F:M), mean age of 51.43 ± 13.49 years and mean level of education of 14.33 ± 2.61 years. Close to 66% (n = 108) of the examined caregivers were spouses/life-partners of the patients, while 22% (n = 36) were adult children. Over 81% (n = 133) of the interviewed caregivers lived in the same household with the patients. The majority (85.6%, n-140) spent more than 50% of their time on the emotional care and 18.1% (n = 30) on the functional care of ALS patients ().
Differences between countries
There was no difference in age and education between the Polish and German caregivers and patients ( and ). The gender distribution was also similar and accounted for 1:1.4 (female:male). In the German population it mirrored the patient’s distribution (female:male 1.58:1), whereas female caregivers were significantly over-represented in the Polish group (3:1). Among the Polish caregivers 75% (n = 60) devoted >50% of their time for emotional and 31.3% (n = 25) on the functional care, as compared to 96% (n = 80) and 5% (n = 4) of the German caregivers, respectively.
Regarding patient’s clinical measures, there was a statistically significant over-representation of patients with NIV (22.6% vs 2.5%; n = 19 vs n = 2) and PEG (8.3% vs 5%; n = 7 vs n = 4) among the German as compared to Polish patients. It was due to a difference in the geographic area covered by each center, with a much shorter commute in case of Germany, increasing access to patients with respiratory insufficiency. The disease duration and mean functional state did not significantly differ between the two populations (). Fifty patients (23 German, 27 Polish) were reported to present behavioral alterations, with a maximum of 4 and 5 out of 10 points, respectively. The difference was not significant (Chi2=5.674 p = 0.339, ETA = 0.194). None of the patients fulfilled criteria of FTD (Citation26).
Quality of life
Qollti-f
Caregivers of ALS patients from both populations showed a positive QoL, rating similarly most of the domains ( and ). The QoLLTI-F positively correlated with patients’ ALSFRS-R and negatively with behavioral impairment, caregivers’ depression, sleep disorders and devoting >50% of time to functional care (due to results in the Polish group) (). It did not correlate with the caregivers’ age, gender, education, relationship with patient, time devoted to emotional help, time from diagnosis, disease duration, use of NIV, IV or PEG. Mann Whitney’s U tests showed no difference between the QoL of caregivers of patients using and not using NIV, PEG or IV.
Table 3 Correlations between quality of life assessed in two scales: ASCA and QOLLTI-F, and psychological, socio-demographic factors and personal experience of the caregivers of patients with amyotrophic lateral sclerosis.
Table 4 Comparison of individual domains of the QOLLTI-F in the caregivers of patients with amyotrophic lateral sclerosis between Polish and German population.
Table 5 Correlations between individual QoL domains on the QOLLTI-F scale in the caregivers of patients with amyotrophic lateral sclerosis and ALSFRS-R, disease duration, time from diagnosis and ECAS-BS (in individual countries and in total) in patients.
QoL domains of environment, caregiver’s own state and patient state positively correlated with patients’ functional status. The domains of caregiver’s and patient’s state negatively correlated with the behavioral impairment. There was no correlation of any QoL domains with disease duration and time from diagnosis ().
Comparison of QOLLTI-F and QOLLTI-F’s domains between countries
A negative correlation between the QoL and spending >50% of time on the functional care was only found in the Polish group. It influenced the final result in the entire group ().
The quality of care was the best-rated domain in both populations. The worst was the caregiver’s outlook in Germany and the patient state in Poland (). Polish caregivers showed a significantly higher satisfaction with care and finding solace in spiritual factors (caregiver’s outlook). No differences were found in other domains.
Time from diagnosis negatively correlated with the environment in the German group and with financial problems in the Polish group. The behavioral impairment negatively correlated with QoL of caregivers related to relationships in Germany and related to caregiver’s own state in Poland.
Asca
The average QoL of the caregivers was positive (0.19 ± 2.68 in Poland and 0.66 ± 2.27 in Germany) and comparable between the countries (p = 0.22, t= −1.223). QoL negatively correlated with age (due to results of the German group), depression, sleep disturbances and presence of perseverations/stereotypes (ECAS-BS) (). There was no correlation with gender, level of education, relationship, percent of the time of emotional help, time from diagnosis, ECAS-BS and ALSFRS-R. The Mann Whitney’s U tests showed no difference between the QoL of caregivers of patients using and not using NIV. IV frequency was too low for analysis. There was a lower QoL among the caregivers of patients using vs non using PEG in both Poland and Germany (p = 0.038 vs. 0.024), although the groups were very small (n = 4 vs n = 7, respectively).
Table 6 Correlations between ADI-12 and psychological, socio-demographic factors and personal experience of the caregivers of patients with amyotrophic lateral sclerosis.
Differences between countries
In the German, but not the Polish group, the QoL negatively correlated with caregivers’ age. In the Polish group it negatively correlated with time spent on functional help and positively with disease duration.
Depression
In total, 32.9% of the caregivers had a depressive disorder. ADI-12 positively correlated with female gender, disease duration, sleep disturbances and negatively with ALSFRS-R and apathy (ECAS-BS). The severity of depression didn’t correlate with time from the diagnosis, the severity of behavioral involvement, emotional help, relationship to the patient, caregivers’s age, education level (), nor the use of PEG (p = 0.06) and NIV (p = 0.61, Mann-Withney U test). A weak correlation was shown for IV (p = 0.05), but the groups were limited.
Differences between countries
Depression was significantly more frequent in Polish (41%) compared to German (25%) caregivers (). Its frequency was higher in Polish caregivers who spent >50% of time on functional care. A negative correlation between the ADI-12 score and ALSFRS-R was more pronounced in Poland, while the sleep disturbances were more frequent in Germany.
Discussion
The psychological burden of care for ALS patients may be particularly high due to relentless disease progression and unfavorable prognosis. The majority of Polish and German caregivers were spouses, adult children and other family members of ALS patients, similarly to previous publications (Citation6,Citation27). Although ALS is more common in men (Citation3,Citation28), the prevalence of Polish female caregivers exceeded twice the number of male patients. There were 60% of female caregivers in Germany and 75% in Poland, what is in line with previous epidemiological studies showing a higher female caregivers prevalence in traditional societies of Ireland (70.4%) (Citation29), Japan (76%) (Citation30) and Portugal (91%) (Citation31).
We have shown that caregivers from both countries report a similar, positive QoL. The QoL measured with QOLLTI-F in Poland (7.4) and Germany (7.0) was comparable to results of studies performed in other European countries, where they ranged between 7.3 and 5.8 (Citation10,Citation11,Citation32,Citation33). It needs to be emphasized that all the reported studies were carried among caregivers having access to specialized MND centers that offered a multidisciplinary care (Citation34,Citation35). The caregivers’ QoL positively correlated with patients’ functional state, while negatively with behavioral impairment, devoting more time to functional care and caregivers’ depression. With the above, it was largely dependent on a better functional and behavioral status of the patient, regardless of the country of provenience. The subjective assessment of patients’ neurobehavioral symptoms by the caregivers (ECAS-BS), mainly perseverations/stereotype behavior, correlated with a reduction in their QoL, similarly to the entire ECAS assessment described in earlier studies (Citation12,Citation36).
QOLLTI-F and ACSA evaluate different QoL parameters, focusing on patient/caregiver-related limitation, or current caregivers’ condition against overall life-experience, respectively (Citation23). Thus, QOLLTI-F showed lower QoL in patients with behavioral symptoms or worse functional status, while ASCA along disease duration and age. Both scales showed a negative correlation with depression.
Rating of the QoL domains differed between populations (Citation10,Citation11). In both our centers, the quality of care was rated best, possibly due to the multidisciplinary care. The worse-rated domain in Poland was the patient’s state and in Germany - the caregiver’s outlook. The results suggest a more patient-orientated attitude of the Polish and a self- or autonomy-orientated attitude of the German caregivers.
Spending >50% of time on daily functional care (31% in Poland, 5% in Germany) negatively correlated with the QoL. A significantly higher percentage of time spent on the functional care in the Polish caregivers reflected a difference of social support and health-care system (Citation37,Citation38). In both countries, medical care allowance, disability and social pensions are granted to most ALS patients. German patients get additional access to nursing care aids and home care services early in the disease course. In Poland these costs are not covered unless the caregiver is handicapped themselves.
Interestingly, Polish caregivers showed a greater satisfaction with care, recognizing current value of life and finding consolation in faith and spirituality. It resulted in assessment of the caregiver’s outlook domain as one of best as opposed to the worst in German caregivers. The results seem related to cultural background, with a more traditional approach to family in Poland, resulting in a personal support for parents or partners, regardless of the disease state (Citation39). Higher religiosity and spirituality may also be helpful in coping with ALS (Citation40,Citation41).
A similar, country-specific pattern was linked to ALS-related behavioral symptoms. In Poland they negatively correlated with caregiver’s own state, while in Germany - with caregiver’s relationship. This may again reflect the differences in the needs of the caregivers and the perception of a close person‘s illness by the environment in different countries.
As previously reported, the disease duration per se did not influence the overall QoL (Citation42), while it affected individual domains. As devoting more time for care reduces the family income, financial problems prevailed in Polish caregivers of patients with longer disease duration. In Germany, the disease duration adversely affected the domain of environment including lack of privacy and constant living with the ill. Caregivers were previously reported to suffer from a lack of free time and possibility to fulfill their own needs (Citation11). It might be one of reasons for increasing usage of nursing home services in Europe, including Germany (Citation43).
The difference in MND center-service areas was probably the reason for the significant over-representation of patients using NIV in the German population, what might have affected the care burden. Interestingly enough, in neither country we found a difference in QoL between caregivers of patients using and not using NIV. Similarly, in previous German and British studies, the introduction of NIV did not influence the caregivers’ QoL (Citation44,Citation45). Only PEG had an effect on caregivers’ QoL, although the group was limited (n = 11) for reliable conclusions.
As many as 41% of Polish and 25% of German caregivers, had symptoms of depression. In comparable samples in Australia (n = 140), Korea (n = 139), China (n = 93) and in Italy (n = 70) it was detected in approximately 31%, 38%, 25% and 11%, respectively (Citation14,Citation36,Citation46,Citation47). Similarly to previous studies, the depression was more common in women (Citation36,Citation48,Citation49) and did not depend on age (Citation10,Citation12,Citation50). Its higher prevalence in Polish caregivers was in line with population-based (Citation51,Citation52) and own studies, where the depression frequency among Polish ALS patients and healthy controls was higher compared to German and Swedish patients (Citation18). It points to country-specific rather than disease-related phenomenon. Although previous publication in the field reported conflicting results, we found a negative correlation between the functional status of the patients from either population and severity of depression in caregivers. Some studies show that caregivers’ levels of depression are closely related to the degree of the patient’s incapacitation (Citation11,Citation53–55), while others show lack of correlation (Citation47,Citation50,Citation56) or no increase of depression severity along the disease course (Citation50,Citation57). The variability may also reflect the differences in social aspects of care, which were not directly studied.
In neither Poland or Germany, was the behavioral impairment in patients with ALS related to caregivers’ depression. Instead, similarly to the results of the QoL, we found a strong correlation between the time spent on functional care and depression in the Polish population. Beside increased severity of depression during prolonged care (Citation10,Citation57), we also found its increased frequency in the entire group with the duration of the disease.
Limitations of the study
1) A high level of specialized and multidisciplinary care might have influenced the patients’ and caregivers overall well-being. 2) The questionnaire did not directly address financial and employment status of patient and caregivers. 3) The groups differed by the frequency of patients using NIV. 4) The data was gathered prior to the COVID19 pandemic and did not reflect the unstable health care situation. It may reflect the caregivers’ wellbeing not affected by transient external factors.
Conclusions
ALS is a family disease affecting the entire patient’s environment. The wellbeing of caregivers is most affected by patient-related and country-specific conditions. Although generally positive, the QoL is the most impaired in patient and caregiver-related areas depending on the country of provenience, cultural background and social support. A significant group of caregivers develops symptoms of depression depending on the patient’s functional state and disease duration. The depression significantly prevails in the Polish group, indicating a country- and culture- rather than a disease-specific background. Both QoL and mood are significantly lower in the caregivers more burdened with the functional care. Since improving the caregivers’ QoL has a positive effect on the patient’s wellbeing (Citation10,Citation31), the emphasis should be placed on influencing modifiable factors that affect the QoL and mood in the caregivers. Thus the most important clinical implication of the study include a need for a stronger social- and health-system support to family members of ALS patients who carry the main burden of personal care. In Poland the focus should be on direct daily care and in Germany on caregivers’ personal space and time, with special care to female and elderly caregivers who may be more vulnerable to depression and decreased QoL. Further and thorough understanding of the needs and background of psychological adaptation of the caregivers may translate into a better patient care in future.
Acknowledgements
The authors thank the patients and caregivers from Germany and Poland for participating in this study.
Declaration of interest
No potential conflict of interest was reported by the author(s).
Additional information
Funding
References
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