Cited by 130Amyotrophic Lateral Sclerosis ResearchMultiple Sclerosis Research StudiesLysosomal Storage Disorders Research

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Cerebrospinal fluid macrophage biomarkers in amyotrophic lateral sclerosis

Thompson, Alexander G., Gray, Elizabeth, Thézénas, Marie‐Laëtitia, Charles, Philip D., Evetts, Samuel, Hu, Michele T., Talbot, Kevin, Fischer, Roman, Kessler, Benedikt M., Turner, Martin R.·2018·Annals of Neurology

DOI 10.1002/ana.25143

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Abstract

Objective: The neurodegenerative disease, amyotrophic lateral sclerosis (ALS), is a heterogeneous clinical syndrome involving multiple molecular pathways. The development of biomarkers for use in therapeutic trials is a priority. We sought to use a high‐throughput proteomic method to identify novel biomarkers in individual cerebrospinal fluid (CSF) samples. Methods: Liquid chromatography/tandem mass spectrometry with label‐free quantification was used to identify CSF proteins using samples from a well‐characterized longitudinal cohort comprising patients with ALS (n = 43), the upper motor neuron variant, primary lateral sclerosis (PLS; n = 6), and cross‐sectional healthy (n = 20) and disease controls (Parkinsons' disease, n = 20; ALS mimic disorders, n = 12). Results: Three macrophage‐derived chitinases showed increased abundance in ALS: chitotriosidase (CHIT1), chitinase‐3‐like protein 1 (CHI3L1), and chitinase‐3‐like protein 2 (CHI3L2). Elevated CHI3L1 was common to ALS and PLS, whereas CHIT1 and CHI3L2 levels differed. Chitinase levels correlated with disease progression rate (CHIT1, r = 0.56, p < 0.001; CHI3L1, r = 0.31; p = 0.028; CHI3L2, r = 0.29, p = 0.044). CHIT1, CHI3L1, and CHI3L2 levels correlated with phosphorylated neurofilament heavy chain (pNFH; r = 0.62, p < 0.001; r = 0.49, p < 0.001; r = 0.41, p < 0.001). CHI3L1 levels, but not CHIT1 or CHI3L2, increased over time in those with low initial levels (gradient = 0.005 log abundance units/month, p = 0.001). High CHIT1 was associated with shortened survival (hazard ratio [HR] 2.84; p = 0.009). Inclusion of pNFH in survival models left only an association of pNFH and survival (HR 1.26; p = 0.019). Interpretation: Neuroinflammatory mechanisms have been consistently implicated through various experimental paradigms. These results support a key role for macrophage activity in ALS pathogenesis, offering novel target engagement and pharmacodynamic biomarkers for neuroinflammation‐focused ALS therapy. Ann Neurol 2018;83:258–268

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Background
Increased C-X-C Motif Chemokine Ligand 12 Levels in Cerebrospinal Fluid as a Candidate Biomarker in Sporadic Amyotrophic Lateral Sclerosis
Andrés‐Benito, P., Povedano, M., Domínguez, R., Marco, C., Colomina, M. J., López-Pérez, Ó., Santana, I. J., Baldeiras, I., Martínez‐Yélamos, S., Zerr, I., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228680 · Cited by 26
Primary Lateral Sclerosis: Clinical, radiological and molecular features
Bede, P., Pradat, P., Lope, J., Vourc’h, P., Blasco, H., & Corcia, P. (2021) · Revue Neurologique · doi:10.1016/j.neurol.2021.04.008 · Cited by 27
Saliva and Saliva Extracellular Vesicles for Biomarker Candidate Identification—Assay Development and Pilot Study in Amyotrophic Lateral Sclerosis
Sjöqvist, S., & Otake, K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065237 · Cited by 26
“We analyzed EVs and saliva by PEA using the panel “Olink Target 96 Cardiovascular III(v.6113)”. is panel as chosen because so e analytes have been reported to be related to ALS (e.g., Y L-40 [22], IT1 [23], P-1 [24]) and e have previously used this panel for CSFbased bio arker discovery for ALS [25].”
MethodInfluential
Chitotriosidase as biomarker for early stage amyotrophic lateral sclerosis: a multicenter study
Steinacker, P., Feneberg, E., Halbgebauer, S., Witzel, S., Verde, F., Oeckl, P., Damme, P. V., Gaur, N., Gray, E., Großkreutz, J., et al. (2021) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.1080/21678421.2020.1861023 · Cited by 27
“For the differentiation of ALS and ALS mimics, we obtained weaker sensitivities and specificities compared to our previous study (8) and here also the largest differences between the centers involved here as well as between our and published data (6,11) were observed.”
ResultSelf-citation
Upper Motor Neuron Disorders: Primary Lateral Sclerosis, Upper Motor Neuron Dominant Amyotrophic Lateral Sclerosis, and Hereditary Spastic Paraplegia
Fullam, T., & Statland, J. M. (2021) · Brain Sciences · doi:10.3390/brainsci11050611 · Cited by 24
“CSF levels of chitinase proteins, a marker for microglial activation, have shown some promise in that they are elevated in patients with ALS as compared to PLS, however, the fact that they do not outperform NfL suggests their utility may be in monitoring therapies targeting microglial activation [74,75].”
Background
Cerebrospinal Fluid Chitinases as Biomarkers for Amyotrophic Lateral Sclerosis
Costa, J., Gromicho, M., Pronto‐Laborinho, A. C., Almeida, C., Gomes, R. A., Guerreiro, A. C. L., Oliva, A., Pinto, S., & de Carvalho, M. A. (2021) · Diagnostics · doi:10.3390/diagnostics11071210 · Cited by 22
“Concerning CHI3L1, there is discrepancy of results in the literature [29,30,38].”
BackgroundResultInfluential
Inflammatory checkpoints in amyotrophic lateral sclerosis: From biomarkers to therapeutic targets
Jiang, Z., Wang, Z., Wei, X., & Yu, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1059994 · Cited by 23
A Review of Biomarkers of Amyotrophic Lateral Sclerosis: A Pathophysiologic Approach
Alshehri, R. S., Abuzinadah, A. R., Alrawaili, M. S., Alotaibi, M. K., Alsufyani, H. A., Alshanketi, R. M., & Alshareef, A. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252010900 · Cited by 23
“CSF and plasma levels CHIT1 and YKL-40 have been measured in ALS using ELISA [200,201] and LC/MS [202] and appear to be longitudinally stable [201].”
BackgroundMethodInfluential
Increased chitotriosidase 1 concentration following nusinersen treatment in spinal muscular atrophy
Freigang, M., Steinacker, P., Wurster, C. D., Schreiber‐Katz, O., Osmanovic, A., Petri, S., Koch, J. C., Rostasy, K. M., Falkenburger, B. H., Ludolph, A. C., et al. (2021) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-021-01961-8 · Cited by 22
Genomic and transcriptomic advances in amyotrophic lateral sclerosis
Rizzuti, M., Sali, L., Melzi, V., Scarcella, S., Costamagna, G., Ottoboni, L., Quetti, L., Brambilla, L., Papadimitriou, D. A., Verde, F., et al. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102126 · Cited by 23
Neurofilament light chain as a biological marker for amyotrophic lateral sclerosis: a meta-analysis study
Sferruzza, G., Bosco, L., Falzone, Y., Russo, T., Domi, T., Quattrini, A., Filippi, M., & Riva, N. (2021) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.1080/21678421.2021.2007952 · Cited by 19
Characteristics of Sensory Neuron Dysfunction in Amyotrophic Lateral Sclerosis (ALS): Potential for ALS Therapy
Seki, S., Kitaoka, Y., Kawata, S., Nishiura, A., Uchihashi, T., Hiraoka, S.-I., Yokota, Y., Isomura, E. T., Kogo, M., & Tanaka, S. (2023) · Biomedicines · doi:10.3390/biomedicines11112967 · Cited by 18
Extracellular vesicles in TDP-43 proteinopathies: pathogenesis and biomarker potential
Dellar, E. R., Nikel, L., Fowler, S. L., Vahsen, B. F., Dafinca, R., Feneberg, E., Talbot, K., Turner, M. R., & Thompson, A. G. (2025) · Molecular Neurodegeneration · doi:10.1186/s13024-025-00859-4 · Cited by 17
“These are primarily proteins involved in inflammatory processes such as chitotriosidase-1 (CHIT1), chitinase-3-like protein-1 (CHI3L1 or YKL-40), chitinase-3-like protein-2 (CHI3L2 or YKL-39) and alpha 1-antichymo-trypsin (SERPINA3) [142, 177–180].”
Self-citation
Protein biomarkers for the diagnosis and prognosis of Amyotrophic Lateral Sclerosis
Donini, L., Tanel, R., Zuccarino, R., & Basso, M. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.09.002 · Cited by 20
Neurodegenerative biomarkers outperform neuroinflammatory biomarkers in amyotrophic lateral sclerosis
Kläppe, U., Sennfält, S., Lovik, A., Finn, A., Bofaisal, U., Zetterberg, H., Blennow, K., Piehl, F., Kmezic, I., Press, R., et al. (2023) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.1080/21678421.2023.2263874 · Cited by 20
“CHIT1 could also discriminate ALS patients from mimics, but performed less well than NFs and worse than previously reported, even when excluding CHIT1 concentrations 200 ng/L (9, 43 – 45).”
Result
Exploiting the role of CSF NfL, CHIT1, and miR-181b as potential diagnostic and prognostic biomarkers for ALS
Gagliardi, D., Rizzuti, M., Masrori, P., Saccomanno, D., Bo, R. D., Sali, L., Meneri, M., Scarcella, S., Milone, I., Hersmus, N., et al. (2024) · Journal of Neurology · doi:10.1007/s00415-024-12699-1 · Cited by 18
Proteomic Approaches to Decipher Mechanisms Underlying Pathogenesis in Multiple Sclerosis Patients
Singh, V. P., Tripathi, A. K., & Dutta, R. (2019) · PROTEOMICS · doi:10.1002/pmic.201800335 · Cited by 17
Pathophysiological Underpinnings of Extra-Motor Neurodegeneration in Amyotrophic Lateral Sclerosis: New Insights From Biomarker Studies
Reyes‐Leiva, D., Dols‐Icardo, O., Sirisi, S., Cortés‐Vicente, E., Turón‐Sans, J., de Luna, N., Blesa, R., Belbin, O., Montal, V., Alcolea, D. A., et al. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.750543 · Cited by 18
“Recent proteomic studies confirmed that three macrophage-derived chitinases (YKL-40, chitotriosidase, and chitinase like-3 protein 2) were increased in ALS and predicted a faster disease course but only YKL-40 levels increased over time in those with low initial levels (187).”
Background
Serum NfL and CHI3L1 for ALS and parkinsonian disorders in the process of diagnosis
Haji, S., Sako, W., Murakami, N., Osaki, Y., & Izumi, Y. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-022-02470-z · Cited by 17
“2018), and ALS (Illán-Gala et al. 2018; Thompson et al. 2018; Gille et al. 2019; Gray et al. 2020; Vu et al. 2020); however, the blood CHI3L1 concentration was not significantly different between any groups in this study-even with ECL, which is a highly sensitive method.”
BackgroundMethod
Network analysis of the cerebrospinal fluid proteome reveals shared and unique differences between sporadic and familial forms of amyotrophic lateral sclerosis
Trautwig, A. N., Fox, E. J., Dammer, E. B., Shantaraman, A., Ping, L., Duong, D. M., Watson, C. M., Wu, F., Asress, S., Guo, Q. J., et al. (2025) · Molecular Neurodegeneration · doi:10.1186/s13024-025-00838-9 · Cited by 23
“The characterization of asymptomatic carriers as well as the unprecedented number of SOD1-mutation carriers ( n = 35, 22 SOD1 ALS, 13 asymptomatic carriers) differentiate this study from previous CSF biomarker studies [37, 41–43].”
Influential
Multi-Study Proteomic and Bioinformatic Identification of Molecular Overlap between Amyotrophic Lateral Sclerosis (ALS) and Spinal Muscular Atrophy (SMA)
Šoltić, D., Bowerman, M., Stock, J. P. P., Shorrock, H. K., Gillingwater, T. H., & Fuller, H. R. (2018) · Brain Sciences · doi:10.3390/brainsci8120212 · Cited by 17
Untangling neuroinflammation in amyotrophic lateral sclerosis
Thompson, A. G., & Turner, M. R. (2019) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2019-321242 · Cited by 16
Self-citation
A novel SETX gene mutation associated with Juvenile amyotrophic lateral sclerosis
Ma, L., Shi, Y., Chen, Z., Li, S., & Zhang, J. (2018) · Brain and Behavior · doi:10.1002/brb3.1066 · Cited by 15
Data‐independent acquisition proteomics of cerebrospinal fluid implicates endoplasmic reticulum and inflammatory mechanisms in amyotrophic lateral sclerosis
Dellar, E. R., Vendrell, I., Talbot, K., Kessler, B. M., Fischer, R., Turner, M. R., & Thompson, A. G. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.16030 · Cited by 13
“…a powerful tool for biomarker discovery in ALS, identifying an increase in a set of glial proteins—the chitinase proteins chitotriosidase-1 (CHIT1), chitinase- 3-like protein-1 (CHI3L1 or YKL-40) and chitinase- 3-like protein-2 (CHI3L2 or YKL-39) (Thompson et al., 2018 ; Varghese et al., 2013 ).”
MethodInfluentialSelf-citation
Progress and New Frontiers in Biomarkers for Amyotrophic Lateral Sclerosis
Turner, M. R. (2018) · Biomarkers in Medicine · doi:10.2217/bmm-2018-0149 · Cited by 14
Self-citation
Urinary biomarkers for amyotrophic lateral sclerosis: candidates, opportunities and considerations
Rogers, M., Schultz, D. W., Karnaros, V., & Shepheard, S. R. (2023) · Brain Communications · doi:10.1093/braincomms/fcad287 · Cited by 13
“63,64 A longitudinal mass spectrometry analysis indicated that CHIT1, CHI3L1 and CHI3L2 correlate with disease progression and with pNfH levels.”
Background
Hereditary Motor Neuropathies and Amyotrophic Lateral Sclerosis: a Molecular and Clinical Update
García-Santibáñez, R., Burford, M. J., & Bucelli, R. C. (2018) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-018-0901-z · Cited by 14
Mass spectrometry based protein biomarkers and drug target discovery and clinical diagnosis in Age-Related progressing neurodegenerative diseases
Agrawal, I., Tripathi, P., & Biswas, S. (2022) · Drug Metabolism Reviews · doi:10.1080/03602532.2022.2029475 · Cited by 12
Fluid Biomarkers of Frontotemporal Lobar Degeneration
van der Ende, E. L., & Swieten, J. C. V. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-51140-1_9 · Cited by 11
Targeted Proteomics upon Treatment with Tofersen Identifies Novel Response Markers for Superoxide Dismutase 1‐Linked Amyotrophic Lateral Sclerosis
Steffke, C., Baskar, K., Bachhuber, F., Wiesenfarth, M., Dorst, J., Schuster, J., Schöberl, F., Reilich, P., Regensburger, M., German, A., et al. (2025) · Annals of Neurology · doi:10.1002/ana.70025 · Cited by 14
Circulating proteomic biomarkers for diagnosing sporadic amyotrophic lateral sclerosis: a cross-sectional study
He, L., Zhou, Q., Xiu, C., Shao, Y., Shen, D., Meng, H., Le, W., & Chen, S. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.389357 · Cited by 10
“Several studies have used high-throughput proteomics methods to explore novel biomarkers (De Benedetti et al., 2017; Thompson et al., 2018).”
Background
Chitotriosidase 1 in the cerebrospinal fluid as a putative biomarker for HTLV-1-associated myelopathy/tropical spastic paraparesis (HAM/TSP) progression
Gomes, Y. C. P., Freitas, N. L., Souza, F. S., Sandim, V., Pereira, D. D. A., Nogueira, F. C. S., Echevarria‐Lima, J., Leite, A. C. C. B., Lima, M. A., Silva, M. T. T., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.949516 · Cited by 9
Advancing mechanistic understanding and biomarker development in amyotrophic lateral sclerosis
Thompson, A. G., Oeckl, P., Feneberg, E., Bowser, R. P., Otto, M., Fischer, R., Kessler, B. M., & Turner, M. R. (2021) · Expert Review of Proteomics · doi:10.1080/14789450.2021.2004890 · Cited by 9
“Proteomic biofluid studies in ALS have generally detected changes presumed to reflect downstream consequences of neurodegeneration, such as the leakage of neurofilament proteins from damaged neurons, activation of glial cells, the effects of synaptic loss, or altered extracellular matrix regulation [28,108,124].”
BackgroundResultSelf-citation
Monocyte-Derived Macrophages Contribute to Chitinase Dysregulation in Amyotrophic Lateral Sclerosis: A Pilot Study
Gaur, N., Huß, E., Prell, T., Steinbach, R., Guerra, J., Srivastava, A., Witte, O. W., & Großkreutz, J. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.629332 · Cited by 9
Proteomic profiling of cerebrospinal fluid reveals TKT as a potential biomarker for medulloblastoma
Kim, J. W., Choi, S. A., Dan, K., Koh, E. J., Ha, S., Phi, J. H., Kim, K. H., Han, D., & Kim, S. (2024) · Scientific Reports · doi:10.1038/s41598-024-71738-z · Cited by 8
Elevated Cerebrospinal Fluid Ubiquitin Carboxyl‐Terminal Hydrolase Isozyme L1 in Asymptomatic C9orf72 Hexanucleotide Repeat Expansion Carriers
Dellar, E. R., Vendrell, I., Amein, B., Lester, D., Edmond, E., Yoganathan, K. T., Dharmadasa, T., Sogorb‐Esteve, A., Fischer, R., Talbot, K., et al. (2024) · Annals of Neurology · doi:10.1002/ana.27133 · Cited by 7
Self-citation
Neurochemical biomarkers of amyotrophic lateral sclerosis: recent developments
Verde, F. (2025) · Current Opinion in Neurology · doi:10.1097/wco.0000000000001411 · Cited by 7
Study on Tissue Homogenization Buffer Composition for Brain Mass Spectrometry-Based Proteomics
Karpiński, A., Torres-Elguera, J. C., Sanner, A., Konopka, W., Kaczmarek, L., Winter, D., Konopka, A., & Bulska, E. (2022) · Biomedicines · doi:10.3390/biomedicines10102466 · Cited by 7
“This knowledge can support the development of targeted therapies [8] or diagnostic tests based on identified biomarkers [3,9].”
Background
Increased cerebrospinal fluid YKL-40 levels are associated with disease severity of neuromyelitis optica spectrum disorders
Qi, Y., Chou, L.-S., Zhang, L., Liu, M., Yi, M., Zhang, Q., Wang, J., Li, T., Zhang, D., & Yang, L. (2020) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2020.102395 · Cited by 7
Network Analysis of the CSF Proteome Characterizes Convergent Pathways of Cellular Dysfunction in ALS
Thompson, A. G., Gray, E., Charles, P. D., Hu, M. T. M., Talbot, K., Fischer, R., Kessler, B. M., & Turner, M. R. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.642324 · Cited by 7
Self-citation
Neuroinflammation and glycosylation-related cerebrospinal fluid proteins for predicting functional decline in amyotrophic lateral sclerosis: a proteomic study
Nakamura, K., Fujita, K., Suzuki, M., Kunugi, A., Hirozane, Y., Kunikata, T., Takahashi, B., Narazaki, G., Kondo, H., Haji, S., et al. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1418320 · Cited by 5
Estimating acceleration time point of respiratory decline in ALS patients: A novel metric
Sato, K., Iwata, A., Kurihara, M., Nagashima, Y., Mano, T., & Toda, T. (2019) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2019.05.031 · Cited by 5
A prognostic biomarker in amyotrophic lateral sclerosis
Mitsumoto, H., & Saito, T. (2018) · Rinsho Shinkeigaku · doi:10.5692/clinicalneurol.cn-001220 · Cited by 5
Pathogenesis of Alzheimer’s disease: Involvement of the Choroid PlexusPreprint
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Peptide variability and signatures associated with disease progression in CSF collected longitudinally from ALS patients
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Targeting Macrophage for the Treatment of Amyotrophic Lateral Sclerosis
Li, L., Liu, J., & She, H. (2019) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527318666190409103831 · Cited by 3
Proteomic-based evidence for adult neurogenesis in birds and mammals as indicated from cerebrospinal fluid
Voukali, E., & Vinkler, M. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.329002 · Cited by 3
“…lipofuscinosis, amyotrophic lateral sclerosis, Alzheimer’s disease, Parkinson’s disease, or unipolar major depressive disorder (Sleat et al., 2017; Bereman et al., 2018; Sathe et al., 2018; Thompson et al., 2018; Dayon et al., 2019; Johnson et al., 2020; Rotunno et al., 2020; Wang et al., 2020).”
Novel therapeutic approaches for motor neuron disease
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Clinical Trials in ALS – Current Challenges and Strategies for Future Directions
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Authors: Thompson, A. G., Gray, E., Thézénas, M., Charles, P. D., Evetts, S., Hu, M. T., Talbot, K., Fischer, R., Kessler, B. M., & Turner, M. R.
Affiliations: University of Oxford (GB)
Nuffield Department of Clinical Neurosciences University of Oxford United Kingdom
Corresponding author: Kessler, Benedikt M.
Turner, Martin R.
ORCID: Thompson, Alexander G.
Gray, Elizabeth
Charles, Philip D.
Talbot, Kevin
Kessler, Benedikt M.
Turner, Martin R.
Venue: Annals of Neurology
Publisher: Wiley
Published: 2018-02
Volume: 83
Issue: 2
Pages: 258-268
ISSN: 0364-5134 (ISSN-L)
1531-8249
DOI: 10.1002/ana.25143
OpenAlex: W2794716002
Cited by: 130
References: 27
Citations by year: 2026: 3 · 2025: 13 · 2024: 7 · 2023: 13 · 2022: 20 · 2021: 22 · 2020: 20 · 2019: 16 · 2018: 16
FWCI: 12.47
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 8 d)
Locations: Annals of Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: Medical Research Council (MR/K01014X/1)
Topics: Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Health Sciences › Medicine › Genetics (clinical) › Lysosomal Storage Disorders Research
Keywords: amyotrophic lateral sclerosis, cerebrospinal fluid biomarkers, chitotriosidase, YKL-40, primary lateral sclerosis, disease progression, survival prediction, neuroinflammation, proteomics
MeSH terms: Amyotrophic Lateral Sclerosis, Chitinases, Cross-Sectional Studies, Female, Humans, Macrophages, Male, Middle Aged, Cohort Studies, Biomarkers, Disease Progression, Proteomics

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Cerebrospinal fluid macrophage biomarkers in amyotrophic lateral sclerosis

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