. 2021 Jun 4;11(6):748.

doi: 10.3390/brainsci11060748.

Informal Caregiving in Amyotrophic Lateral Sclerosis (ALS): A High Caregiver Burden and Drastic Consequences on Caregivers' Lives

Pavel Schischlevskij¹, Isabell Cordts², René Günther^{3

4}, Benjamin Stolte⁵, Daniel Zeller⁶, Carsten Schröter⁷, Ute Weyen⁸, Martin Regensburger⁹, Joachim Wolf¹⁰, Ilka Schneider^{11

12}, Andreas Hermann^{13

14}, Moritz Metelmann¹⁵, Zacharias Kohl¹⁶, Ralf A Linker¹⁶, Jan Christoph Koch¹⁷, Claudia Stendel^{18

19}, Lars H Müschen¹, Alma Osmanovic¹, Camilla Binz¹, Thomas Klopstock^{18

19

20}, Johannes Dorst²¹, Albert C Ludolph^{21

22}, Matthias Boentert^{23

24}, Tim Hagenacker⁵, Marcus Deschauer², Paul Lingor², Susanne Petri¹, Olivia Schreiber-Katz¹

Affiliations

¹ Department of Neurology, Hannover Medical School, 30625 Hannover, Germany.
² Department of Neurology, Klinikum Rechts der Isar, Technical University of Munich, 81675 Munich, Germany.
³ Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden, 01307 Dresden, Germany.
⁴ German Center for Neurodegenerative Diseases (DZNE), 01307 Dresden, Germany.
⁵ Department of Neurology, University Medicine Essen, 45147 Essen, Germany.
⁶ Department of Neurology, University of Würzburg, 97080 Würzburg, Germany.
⁷ Hoher Meißner Clinic, Neurology, 37242 Bad Sooden-Allendorf, Germany.
⁸ Department of Neurology, Ruhr-University Bochum, BG-Kliniken Bergmannsheil, 44789 Bochum, Germany.
⁹ Department of Molecular Neurology, Friedrich-Alexander-University Erlangen-Nürnberg, 91054 Erlangen, Germany.
¹⁰ Department of Neurology, Diakonissen Hospital Mannheim, 68163 Mannheim, Germany.
¹¹ Department of Neurology, Martin-Luther University Halle/Saale, 06120 Halle, Germany.
¹² Department of Neurology, Klinikum Sankt Georg, 04129 Leipzig, Germany.
¹³ Translational Neurodegeneration Section "Albrecht-Kossel", Department of Neurology, University Medical Center Rostock, University of Rostock, 18147 Rostock, Germany.
¹⁴ German Center for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, 18147 Rostock, Germany.
¹⁵ Department of Neurology, University Hospital Leipzig, 04103 Leipzig, Germany.
¹⁶ Department of Neurology, University of Regensburg, 93053 Regensburg, Germany.
¹⁷ Department of Neurology, University Medicine Göttingen, 37075 Göttingen, Germany.
¹⁸ Department of Neurology, Friedrich-Baur Institute, University Hospital, Ludwig Maximilian University of Munich, 80336 Munich, Germany.
¹⁹ German Center for Neurodegenerative Diseases (DZNE), 80336 Munich, Germany.
²⁰ Munich Cluster for Systems Neurology (SyNergy), 80336 Munich, Germany.
²¹ Department of Neurology, University of Ulm, 89081 Ulm, Germany.
²² German Center for Neurodegenerative Diseases (DZNE), 89081 Ulm, Germany.
²³ Department of Neurology, Institute of Translational Neurology, University Hospital Münster, 48149 Münster, Germany.
²⁴ Department of Medicine, UKM Marienhospital, 48565 Steinfurt, Germany.

PMID: 34200087
PMCID: PMC8228206
DOI: 10.3390/brainsci11060748

Informal Caregiving in Amyotrophic Lateral Sclerosis (ALS): A High Caregiver Burden and Drastic Consequences on Caregivers' Lives

Pavel Schischlevskij et al. Brain Sci. 2021.

. 2021 Jun 4;11(6):748.

doi: 10.3390/brainsci11060748.

Authors

Affiliations

¹ Department of Neurology, Hannover Medical School, 30625 Hannover, Germany.
² Department of Neurology, Klinikum Rechts der Isar, Technical University of Munich, 81675 Munich, Germany.
³ Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden, 01307 Dresden, Germany.
⁴ German Center for Neurodegenerative Diseases (DZNE), 01307 Dresden, Germany.
⁵ Department of Neurology, University Medicine Essen, 45147 Essen, Germany.
⁶ Department of Neurology, University of Würzburg, 97080 Würzburg, Germany.
⁷ Hoher Meißner Clinic, Neurology, 37242 Bad Sooden-Allendorf, Germany.
⁸ Department of Neurology, Ruhr-University Bochum, BG-Kliniken Bergmannsheil, 44789 Bochum, Germany.
⁹ Department of Molecular Neurology, Friedrich-Alexander-University Erlangen-Nürnberg, 91054 Erlangen, Germany.
¹⁰ Department of Neurology, Diakonissen Hospital Mannheim, 68163 Mannheim, Germany.
¹¹ Department of Neurology, Martin-Luther University Halle/Saale, 06120 Halle, Germany.
¹² Department of Neurology, Klinikum Sankt Georg, 04129 Leipzig, Germany.
¹³ Translational Neurodegeneration Section "Albrecht-Kossel", Department of Neurology, University Medical Center Rostock, University of Rostock, 18147 Rostock, Germany.
¹⁴ German Center for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, 18147 Rostock, Germany.
¹⁵ Department of Neurology, University Hospital Leipzig, 04103 Leipzig, Germany.
¹⁶ Department of Neurology, University of Regensburg, 93053 Regensburg, Germany.
¹⁷ Department of Neurology, University Medicine Göttingen, 37075 Göttingen, Germany.
¹⁸ Department of Neurology, Friedrich-Baur Institute, University Hospital, Ludwig Maximilian University of Munich, 80336 Munich, Germany.
¹⁹ German Center for Neurodegenerative Diseases (DZNE), 80336 Munich, Germany.
²⁰ Munich Cluster for Systems Neurology (SyNergy), 80336 Munich, Germany.
²¹ Department of Neurology, University of Ulm, 89081 Ulm, Germany.
²² German Center for Neurodegenerative Diseases (DZNE), 89081 Ulm, Germany.
²³ Department of Neurology, Institute of Translational Neurology, University Hospital Münster, 48149 Münster, Germany.
²⁴ Department of Medicine, UKM Marienhospital, 48565 Steinfurt, Germany.

PMID: 34200087
PMCID: PMC8228206
DOI: 10.3390/brainsci11060748

Abstract

Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease that causes progressive autonomy loss and need for care. This does not only affect patients themselves, but also the patients' informal caregivers (CGs) in their health, personal and professional lives. The big efforts of this multi-center study were not only to evaluate the caregivers' burden and to identify its predictors, but it also should provide a specific understanding of the needs of ALS patients' CGs and fill the gap of knowledge on their personal and work lives. Using standardized questionnaires, primary data from patients and their main informal CGs (n = 249) were collected. Patients' functional status and disease severity were evaluated using the Barthel Index, the revised Amyotrophic Lateral Sclerosis Functional Rating Scale (ALSFRS-R) and the King's Stages for ALS. The caregivers' burden was recorded by the Zarit Burden Interview (ZBI). Comorbid anxiety and depression of caregivers were assessed by the Hospital Anxiety and Depression Scale. Additionally, the EuroQol Five Dimension Five Level Scale evaluated their health-related quality of life. The caregivers' burden was high (mean ZBI = 26/88, 0 = no burden, ≥24 = highly burdened) and correlated with patients' functional status (r_p = -0.555, p < 0.001, n = 242). It was influenced by the CGs' own mental health issues due to caregiving (+11.36, 95% CI [6.84; 15.87], p < 0.001), patients' wheelchair dependency (+9.30, 95% CI [5.94; 12.66], p < 0.001) and was interrelated with the CGs' depression (r_p = 0.627, p < 0.001, n = 234), anxiety (r_p = 0.550, p < 0.001, n = 234), and poorer physical condition (r_p = -0.362, p < 0.001, n = 237). Moreover, female CGs showed symptoms of anxiety more often, which also correlated with the patients' impairment in daily routine (r_s = -0.280, p < 0.001, n = 169). As increasing disease severity, along with decreasing autonomy, was the main predictor of caregiver burden and showed to create relevant (negative) implications on CGs' lives, patient care and supportive therapies should address this issue. Moreover, in order to preserve the mental and physical health of the CGs, new concepts of care have to focus on both, on not only patients but also their CGs and gender-associated specific issues. As caregiving in ALS also significantly influences the socioeconomic status by restrictions in CGs' work lives and income, and the main reported needs being lack of psychological support and a high bureaucracy, the situation of CGs needs more attention. Apart from their own multi-disciplinary medical and psychological care, more support in care and patient management issues is required.

Keywords: amyotrophic lateral sclerosis (ALS); anxiety; caregiver burden; decreasing autonomy; depression; functional status; health-related quality of life; informal caregiving; psychological support; socioeconomic status.

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Conflict of interest statement

P.S. reports no conflicts of interest. I.C. reports no conflicts of interest. R.G. reports no conflicts of interest. B.S. received speaker honoraria from Biogen without relation to ALS. D.Z. received compensation for participation on an advisory board of Biogen, as well as for consultancy work from Novartis. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. C.S. (Carsten Schröter) reports no conflicts of interest. U.W. received compensation for activities with Merz and Desitin. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. M.R. reports no conflicts of interest. J.W. reports no conflicts of interest. I.S. received personal/speaker fees from Sanofi Genzyme, Biogen and from the German Neuromuscular Society “Deutsche Gesellschaft fuer Muskelkranke“ (DGM e.V.) without relation to ALS. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. A.H. reported conflict of interest due to consultant work for Biogen, Desitin, and Roche. Additionally, A.H. received research funding from BMBF, GBA-Innovations Fund, Helmholtz Gesellschaft, NOMIS-Foundation, and “Hermann und Lilly-Schilling Stiftung für medizinische Forschung” im Stifterverband. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. M.M. reports no conflicts of interest. Z.K. reports no conflicts of interest. R.A.L. received compensation for activities with Biogen, Celgene, Merck, Novartis, and Roche, as well as research support from DFG, Else-Kröner-Fresenius Stiftung, Biogen and Novartis. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. J.C.K. received personal fees from Biogen, Roche, Avexis, Abbvie and Ipsen and funding by the “Deutsche Gesellschaft fuer Muskelkranke “(DGM e.V.) outside of the submitted work. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. C.S. (Claudia Stendel) reports no conflicts of interest. L.H.M. reports no conflicts of interest. A.O. received honoraria as a speaker/consultant from the German Neuromuscular Society “Deutsche Gesellschaft fuer Muskelkranke “(DGM e.V.), Biogen and Impulze. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. C.B. reports no conflicts of interest. T.K. reports no conflicts of interest. J.D. reports no conflicts of interest. A.C.L. reports no conflicts of interest. M.B. received honoraria from UCB Pharma, Sanofi Genzyme, Desitin, Löwenstein Medical, Sanofi- Genzyme, and Biogen, as well as financial research support from Sanofi-Genzyme and Löwenstein Medical. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. T.H. received honoraria from Biogen, Roche, Novartis and Alexion without relation to ALS and received research funding from Biogen, AveXis and Roche without relation to ALS. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. M.D. received honoraria from Biogen and Roche without relation to ALS and received funding for the BMBF-funded Rock ALS study and for the registered study SMArtCARE from the University of Freiburg (without relation to ALS). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. P.L. has no conflicts of interest in the context of this work. S.P. received honoraria as speaker/consultant from Biogen GmbH, Roche, Novartis, Teva, Cytokinetics Inc., and Desitin; and grants from DGM e.V, Federal Ministry of Education and Research, German Israeli Foundation for Scientific Research and Development, EU Joint Program for Neurodegenerative Disease Research. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. O.S.-K. has received honoraria as a speaker/consultant and/or funding for travel expenses from the German Neuromuscular Society “Deutsche Gesellschaft fuer Muskelkranke (DGM e.V.), Novartis, Biogen GmbH, Biermann Verlag GmbH, MK+S—Medizin, Kommunikation & Service GmbH, and the Jain Foundation. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

**Figure 1**
Evaluation of caregivers‘ general burden: Mean scores are presented with standard errors (error bars). Statistically significant findings: (a) ZBI-BI groups (ANOVA: p < 0.001; KWT: p < 0.001; r_s = −0.542, p < 0.001, *n =* 242), ZBI-BI (r_p = −0.555, p < 0.001, *n =* 242); (b) ZBI-King’s Stages (ANOVA: p < 0.001; KWT: p < 0.001; r_s = 0.300, p < 0.001, *n =* 237), ZBI-ALSFRS-R (r_p = −0.460, p < 0.001, *n =* 237); (c) DOC-BI groups (p < 0.001; KWT: p < 0.001; r_s = −0.636, p < 0.001, *n =* 249), DOC-BI (r_p = −0.617, p < 0.001, *n =* 249); (d) DOC-King’s Stages (p < 0.001; KWT: p < 0.001; r_s = 0.294, p < 0.001, *n =* 244) DOC-ALSFRS-R (r_p = −0.452, p < 0.001, *n =* 244). * = post-hoc: p ≤ 0.05 between subgroups. Abbreviations: ZBI = Zarit Burden Interview; BI = Barthel Index; DOC = duration of caregiving, ALSFRS-R = Revised Amyotrophic Lateral Sclerosis Functional Rating Scale.

**Figure 2**
General impairment of caregivers according to BI groups (a) and gender (b): The caregivers were able to indicate their perceived general impairment in different dimensions of their everyday life on a four-point Likert scale from “not impaired at all” to “extremely impaired”. Six adjacent columns are assigned to one distinct BI group (a) or gender (b). One column corresponds to one domain. The extent of the colored sections represents the percentage of answers provided by the CGs on the abovementioned scale. The proportion of “very/extremely” impaired CGs increased with the loss of autonomy of the patient (BI group 4 (= BI score 100 points = full independence) to BI group 1 (= BI score 0–20 points = full dependence)), and the number of “not very/not at all” restricted CGs correspondingly decreased (a), while no significant differences were observed according to the CGs’ gender (b). Abbreviations: BI = Barthel Index; CGs = caregivers.

**Figure 3**
Caregivers’ health-related quality of life and anxiety/depression: Mean scores are presented with standard errors. Statistically significant findings: (a) EQ-VAS/EQ-5D-5L index value-BI groups (ANOVA: p < 0.001; KWT: p < 0.001; r_s = 0.317, p < 0.001, *n =* 243/ANOVA: p = 0.005; KWT: p = 0.001; r_s = 0.252, p < 0.001, *n =* 244); EQ-VAS/EQ-5D-5L index value-BI (r_p = 0.320, p < 0.001, *n =* 243/r_p = 0.258, p < 0.001, *n =* 244); (b) EQ-VAS/EQ-5D-5L index value-King’s Stages (no significant findings); EQ-VAS/EQ-5D-5L index value-ALSFRS-R (r_p = 0.278, p < 0.001, *n =* 238/r_p = 0.214, p = 0.001, *n =* 239); (c) HADS-D/HADS-A-BI groups (ANOVA: p < 0.001; KWT: p < 0.001; r_s = −0.376, p < 0.001, *n =* 240/ANOVA: p = 0.036; KWT: p = 0.03; r_s = −0.187, p = 0.004, *n =* 240); HADS-D/HADS-A-BI (r_p = −0.400, p < 0.001, *n =* 240/r_p = −0.200, p < 0.002, *n =* 240); (d) HADS-D/HADS-A-King’s Stages (ANOVA: p = 0.002; KWT: p = 0.001; r_s = 0.217, p = 0.001, *n =* 236/no significant findings); HADS-D/HADS-A-ALSFRS-R (r_p = −0.321, p < 0.001, *n =* 236/r_p = −0.193, p = 0.003, *n =* 236). * = post-hoc: p ≤ 0.05 between subgroups. Abbreviations: BI = Barthel Index; EQ-VAS = EuroQol visual analog scale; EQ-5D-5L index value x 100 = EuroQol Five Dimension Five Level Scale index value multiplied by 100; HADS-D = Hospital Anxiety and Depression Scale-depression subscale; HADS-A = Hospital Anxiety and Depression Scale-anxiety subscale.

**Figure 4**
Caregivers’ health impairment: The caregivers were able to state if they felt health-impaired themselves due to caregiving (yes) or not (no) (a) and could differ between physical (blue) and mental (yellow) symptoms (b). Three adjacent columns in (a) are assigned to each BI group (groups 1–4). The extent of the colored sections represents the percentage of caregivers. We observed a statistically significant increase in the incidence of physical and mental health impairment according to the BI group (BI group 4 (=BI score 100 points = full independence) to BI group 1 (=BI score 0–20 points = full dependence)) and thus decreasing autonomy of the patients. Abbreviations: BI = Barthel Index.

**Figure 5**
Impairment in caregivers’ work lives according to BI groups: The caregivers were able to state their work life impairment with “yes/no” in the following domains: abandoned work due to caregiving; general work life impairment; reduction of working hours; drop in salary; career restriction. Five adjacent columns are assigned to each BI group. One column corresponds to one domain. The extent of the colored sections represents the percentage of caregivers. There was a statistically significant correlation of the investigated domains to the BI groups. Abbreviations: BI = Barthel Index.

**Figure 6**
Correlation of parameters: Statistically significant correlations: ZBI-DOC (r_p = 0.379, p < 0.001, *n =* 242); ZBI-HADS-D (r_p = 0.627, p < 0.001, *n =* 234); ZBI-HADS-A (r_p = 0.550, p < 0.001, *n =* 234); ZBI-EQ-VAS/EQ-5D-5L index value (r_p = −0.362, p < 0.001, *n =* 237/r_p = −0.315, p < 0.001, *n =* 238); HADS-D-HADS-A (r_p = 0.745, p < 0.001, *n =* 240), HADS-D-DOC (r_p = 0.332, p < 0.001, *n =* 240); HADS-D-EQ-VAS/EQ−5D-5L index value (r_p = −0.488, p < 0.001, *n =* 238/r_p = −0.399, p < 0.001, *n =* 238); HADS-A-DOC (r_p = 0.230, p < 0.001, *n =* 240), HADS-A-EQ-VAS/EQ-5D-5L index value (r_p= −0.386, p < 0.001, *n =* 238/r_p = −0.272, p < 0.001, *n =* 238); DOC-EQ-VAS/EQ-5D-5L index value (r_p= −0.371, p < 0.001, *n =* 243/r_p = −0.375, p < 0.001, *n =* 244). Abbreviations: ZBI = Zarit Burden Interview; EQ-VAS = EuroQol visual analog scale; EQ-5D-5L index value = EuroQol Five Dimension Five Level Scale index value; HADS-D = Hospital Anxiety and Depression Scale-depression subscale; HADS-A = Hospital Anxiety and Depression Scale-anxiety subscale; DOC = duration of caregiving.

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Informal Caregiving in Amyotrophic Lateral Sclerosis (ALS): A High Caregiver Burden and Drastic Consequences on Caregivers' Lives

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Informal Caregiving in Amyotrophic Lateral Sclerosis (ALS): A High Caregiver Burden and Drastic Consequences on Caregivers' Lives

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