Clinical characterization of common pathogenic variants of SOD1-ALS in Germany.
SOD1
Amyotrophic lateral sclerosis
Clinical phenotype
Motor neuron disease
Tofersen
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
14 Aug 2024
14 Aug 2024
Historique:
received:
29
05
2024
accepted:
04
07
2024
revised:
01
07
2024
medline:
14
8
2024
pubmed:
14
8
2024
entrez:
14
8
2024
Statut:
aheadofprint
Résumé
Pathogenic variants in the Cu/Zn superoxide dismutase (SOD1) gene can be detected in approximately 2% of sporadic and 11% of familial amyotrophic lateral sclerosis (ALS) patients in Europe. We analyzed the clinical phenotypes of 83 SOD1-ALS patients focusing on patients carrying the most frequent (likely) pathogenic variants (R116G, D91A, L145F) in Germany. Moreover, we describe the effect of tofersen treatment on ten patients carrying these variants. R116G patients showed the most aggressive course of disease with a median survival of 22.0 months compared to 198.0 months in D91A and 87.0 months in L145F patients (HR 7.71, 95% CI 2.89-20.58 vs. D91A; p < 0.001 and HR 4.25, 95% CI 1.55-11.67 vs. L145F; p = 0.02). Moreover, R116G patients had the fastest median ALSFRS-R progression rate with 0.12 (IQR 0.07-0.20) points lost per month. Median diagnostic delay was 10.0 months (IQR 5.5-11.5) and therefore shorter compared to 57.5 months (IQR 14.0-83.0) in D91A (p < 0.001) and 21.5 months (IQR 5.8-38.8) in L145F (p = 0.21) carriers. As opposed to D91A carriers (50.0%), 96.2% of R116G (p < 0.001) and 100.0% of L145F (p = 0.04) patients reported a positive family history. During tofersen treatment, all patients showed a reduction of neurofilament light chain (NfL) serum levels, independent of the SOD1 variant. Patients with SOD1-ALS carrying R116G, D91A, or L145F variants show commonalities, but also differences in their clinical phenotype, including a faster progression rate with shorter survival in R116G, and a comparatively benign disease course in D91A carriers.
Identifiants
pubmed: 39141064
doi: 10.1007/s00415-024-12564-1
pii: 10.1007/s00415-024-12564-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O’Regan JP, Deng HX et al (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59–62. https://doi.org/10.1038/362059a0
doi: 10.1038/362059a0
pubmed: 8446170
Masrori P, Van Damme P (2020) Amyotrophic lateral sclerosis: a clinical review. Eur J Neurol 27:1918–1929. https://doi.org/10.1111/ene.14393
doi: 10.1111/ene.14393
pubmed: 32526057
Chiò A, Calvo A, Moglia C, Mazzini L, Mora G, PARALS Study Group (2011) Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J Neurol Neurosurg Psychiatry 82:740–746. https://doi.org/10.1136/jnnp.2010.235952
doi: 10.1136/jnnp.2010.235952
pubmed: 21402743
Rosenbohm A, Peter RS, Erhardt S, Lulé D, Rothenbacher D, Ludolph AC, Nagel G, ALS Registry Study Group (2017) Epidemiology of amyotrophic lateral sclerosis in Southern Germany. J Neurol 264:749–757. https://doi.org/10.1007/s00415-017-8413-3
doi: 10.1007/s00415-017-8413-3
pubmed: 28220290
DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, Kouri N, Wojtas A, Sengdy P, Hsiung GY, Karydas A, Seeley WW, Josephs KA, Coppola G, Geschwind DH, Wszolek ZK, Feldman H, Knopman DS, Petersen RC, Miller BL, Dickson DW, Boylan KB, Graff-Radford NR, Rademakers R (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72:245–256. https://doi.org/10.1016/j.neuron.2011.09.011
doi: 10.1016/j.neuron.2011.09.011
pubmed: 21944778
pmcid: 3202986
Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, Kalimo H, Paetau A, Abramzon Y, Remes AM, Kaganovich A, Scholz SW, Duckworth J, Ding J, Harmer DW, Hernandez DG, Johnson JO, Mok K, Ryten M, Trabzuni D, Guerreiro RJ, Orrell RW, Neal J, Murray A, Pearson J, Jansen IE, Sondervan D, Seelaar H, Blake D, Young K, Halliwell N, Callister JB, Toulson G, Richardson A, Gerhard A, Snowden J, Mann D, Neary D, Nalls MA, Peuralinna T, Jansson L, Isoviita VM, Kaivorinne AL, Hölttä-Vuori M, Ikonen E, Sulkava R, Benatar M, Wuu J, Chiò A, Restagno G, Borghero G, Sabatelli M, ITALSGEN Consortium, Heckerman D, Rogaeva E, Zinman L, Rothstein JD, Sendtner M, Drepper C, Eichler EE, Alkan C, Abdullaev Z, Pack SD, Dutra A, Pak E, Hardy J, Singleton A, Williams NM, Heutink P, Pickering-Brown S, Morris HR, Tienari PJ, Traynor BJ (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72:257–268. https://doi.org/10.1016/j.neuron.2011.09.010
doi: 10.1016/j.neuron.2011.09.010
pubmed: 21944779
pmcid: 3200438
Zou ZY, Zhou ZR, Che CH, Liu CY, He RL, Huang HP (2017) Genetic epidemiology of amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 88:540–549. https://doi.org/10.1136/jnnp-2016-315018
doi: 10.1136/jnnp-2016-315018
pubmed: 28057713
Ruf WP, Boros M, Freischmidt A, Brenner D, Grozdanov V, de Meirelles J, Meyer T, Grehl T, Petri S, Grosskreutz J, Weyen U, Guenther R, Regensburger M, Hagenacker T, Koch JC, Emmer A, Roediger A, Steinbach R, Wolf J, Weishaupt JH, Lingor P, Deschauer M, Cordts I, Klopstock T, Reilich P, Schoeberl F, Schrank B, Zeller D, Hermann A, Knehr A, Günther K, Dorst J, Schuster J, Siebert R, Ludolph AC, Müller K (2023) Spectrum and frequency of genetic variants in sporadic amyotrophic lateral sclerosis. Brain Commun 5:152. https://doi.org/10.1093/braincomms/fcad152
doi: 10.1093/braincomms/fcad152
Müller K, Brenner D, Weydt P, Meyer T, Grehl T, Petri S, Grosskreutz J, Schuster J, Volk AE, Borck G, Kubisch C, Klopstock T, Zeller D, Jablonka S, Sendtner M, Klebe S, Knehr A, Günther K, Weis J, Claeys KG, Schrank B, Sperfeld AD, Hübers A, Otto M, Dorst J, Meitinger T, Strom TM, Andersen PM, Ludolph AC, Weishaupt JH, German ALS, network MND-NET, (2018) Comprehensive analysis of the mutation spectrum in 301 German ALS families. J Neurol Neurosurg Psychiatry 89:817–827. https://doi.org/10.1136/jnnp-2017-317611
doi: 10.1136/jnnp-2017-317611
pubmed: 29650794
Huai J, Zhang Z (2019) Structural properties and interaction partners of familial ALS-associated SOD1 mutants. Front Neurol 10:527. https://doi.org/10.3389/fneur.2019.00527
doi: 10.3389/fneur.2019.00527
pubmed: 31164862
pmcid: 6536575
Cudkowicz ME, McKenna-Yasek D, Sapp PE, Chin W, Geller B, Hayden DL, Schoenfeld DA, Hosler BA, Horvitz HR, Brown RH (1997) Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann Neurol 41:210–221. https://doi.org/10.1002/ana.410410212
doi: 10.1002/ana.410410212
pubmed: 9029070
Cudkowicz ME, McKenna-Yasek D, Chen C, Hedley-Whyte ET, Brown RH Jr (1998) Limited corticospinal tract involvement in amyotrophic lateral sclerosis subjects with the A4V mutation in the copper/zinc superoxide dismutase gene. Ann Neurol 43:703–710. https://doi.org/10.1002/ana.410430604
doi: 10.1002/ana.410430604
pubmed: 9629839
Bali T, Self W, Liu J, Siddique T, Wang LH, Bird TD, Ratti E, Atassi N, Boylan KB, Glass JD, Maragakis NJ, Caress JB, McCluskey LF, Appel SH, Wymer JP, Gibson S, Zinman L, Mozaffar T, Callaghan B, McVey AL, Jockel-Balsarotti J, Allred P, Fisher ER, Lopate G, Pestronk A, Cudkowicz ME, Miller TM (2017) Defining SOD1 ALS natural history to guide therapeutic clinical trial design. J Neurol Neurosurg Psychiatry 88:99–105. https://doi.org/10.1136/jnnp-2016-313521
doi: 10.1136/jnnp-2016-313521
pubmed: 27261500
Tang L, Dorst J, Chen L, Liu X, Ma Y, Günther K, Michels S, Müller K, Freischmidt A, Weishaupt JH, Fan D, Ludolph AC (2021) A natural history comparison of SOD1-mutant patients with amyotrophic lateral sclerosis between Chinese and German populations. Transl Neurodegener 10:42. https://doi.org/10.1186/s40035-021-00266-x
doi: 10.1186/s40035-021-00266-x
pubmed: 34711284
pmcid: 8555265
Rabe M, Felbecker A, Waibel S, Steinbach P, Winter P, Müller U, Ludolph AC (2010) The epidemiology of CuZn-SOD mutations in Germany: a study of 217 families. J Neurol 257:1298–1302. https://doi.org/10.1007/s00415-010-5512-9
doi: 10.1007/s00415-010-5512-9
pubmed: 20309572
Tafuri F, Ronchi D, Magri F, Comi GP, Corti S (2015) SOD1 misplacing and mitochondrial dysfunction in amyotrophic lateral sclerosis pathogenesis. Front Cell Neurosci 9:336. https://doi.org/10.3389/fncel.2015.00336
doi: 10.3389/fncel.2015.00336
pubmed: 26379505
pmcid: 4548205
Bunton-Stasyshyn RK, Saccon RA, Fratta P, Fisher EM (2015) SOD1 function and its implications for amyotrophic lateral sclerosis pathology: new and renascent themes. Neuroscientist 21:519–529. https://doi.org/10.1177/1073858414561795
doi: 10.1177/1073858414561795
pubmed: 25492944
Petrov D, Mansfield C, Moussy A, Hermine O (2017) ALS clinical trials review: 20 years of failure. Are we any closer to registering a new treatment? Front Aging Neurosci 9:68. https://doi.org/10.3389/fnagi.2017.00068
doi: 10.3389/fnagi.2017.00068
pubmed: 28382000
pmcid: 5360725
Writing Group; Edaravone (MCI-186) ALS 19 Study Group (2017) Safety and efficacy of edaravone in well defined patients with amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled trial. Lancet Neurol 16:505–512. https://doi.org/10.1016/S1474-4422(17)30115-1
doi: 10.1016/S1474-4422(17)30115-1
Paganoni S, Macklin EA, Hendrix S, Berry JD, Elliott MA, Maiser S, Karam C, Caress JB, Owegi MA, Quick A, Wymer J, Goutman SA, Heitzman D, Heiman-Patterson T, Jackson CE, Quinn C, Rothstein JD, Kasarskis EJ, Katz J, Jenkins L, Ladha S, Miller TM, Scelsa SN, Vu TH, Fournier CN, Glass JD, Johnson KM, Swenson A, Goyal NA, Pattee GL, Andres PL, Babu S, Chase M, Dagostino D, Dickson SP, Ellison N, Hall M, Hendrix K, Kittle G, McGovern M, Ostrow J, Pothier L, Randall R, Shefner JM, Sherman AV, Tustison E, Vigneswaran P, Walker J, Yu H, Chan J, Wittes J, Cohen J, Klee J, Leslie K, Tanzi RE, Gilbert W, Yeramian PD, Schoenfeld D, Cudkowicz ME (2020) Trial of sodium phenylbutyrate-taurursodiol for amyotrophic lateral sclerosis. N Engl J Med 383:919–930. https://doi.org/10.1056/NEJMoa1916945
doi: 10.1056/NEJMoa1916945
pubmed: 32877582
pmcid: 9134321
Miller TM, Cudkowicz ME, Genge A, Shaw PJ, Sobue G, Bucelli RC, Chiò A, Van Damme P, Ludolph AC, Glass JD, Andrews JA, Babu S, Benatar M, McDermott CJ, Cochrane T, Chary S, Chew S, Zhu H, Wu F, Nestorov I, Graham D, Sun P, McNeill M, Fanning L, Ferguson TA, Fradette S, VALOR and OLE Working Group (2022) Trial of antisense oligonucleotide tofersen for SOD1 ALS. N Engl J Med 387:1099–1110. https://doi.org/10.1056/NEJMoa2204705
doi: 10.1056/NEJMoa2204705
pubmed: 36129998
Wiesenfarth M, Dorst J, Brenner D, Elmas Z, Parlak Ö, Uzelac Z, Kandler K, Mayer K, Weiland U, Herrmann C, Schuster J, Freischmidt A, Müller K, Siebert R, Bachhuber F, Simak T, Günther K, Fröhlich E, Knehr A, Regensburger M, German A, Petri S, Grosskreutz J, Klopstock T, Reilich P, Schöberl F, Hagenacker T, Weyen U, Günther R, Vidovic M, Jentsch M, Haarmeier T, Weydt P, Valkadinov I, Hesebeck-Brinckmann J, Conrad J, Weishaupt JH, Schumann P, Körtvélyessy P, Meyer T, Ruf WP, Witzel S, Senel M, Tumani H, Ludolph AC (2024) Effects of tofersen treatment in patients with SOD1-ALS in a “real-world” setting—a 12-month multicenter cohort study from the German early access program. EClinicalMedicine 69:102495. https://doi.org/10.1016/j.eclinm.2024.102495
doi: 10.1016/j.eclinm.2024.102495
pubmed: 38384337
pmcid: 10878861
Meyer T, Schumann P, Weydt P, Petri S, Koc Y, Spittel S, Bernsen S, Günther R, Weishaupt JH, Dreger M, Kolzarek F, Kettemann D, Norden J, Boentert M, Vidovic M, Meisel C, Münch C, Maier A, Körtvélyessy P (2023) Neurofilament light-chain response during therapy with antisense oligonucleotide tofersen in SOD1-related ALS: treatment experience in clinical practice. Muscle Nerve 67:515–521. https://doi.org/10.1002/mus.27818
doi: 10.1002/mus.27818
pubmed: 36928619
Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron Diseases (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293–299. https://doi.org/10.1080/146608200300079536
doi: 10.1080/146608200300079536
pubmed: 11464847
Richards S, Aziz N, Bale S, Bick D, Das S, Gastier-Foster J, Grody WW, Hegde M, Lyon E, Spector E, Voelkerding K, Rehm HL, Laboratory Quality Assurance Committee ACMG (2015) Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med 17:405–424. https://doi.org/10.1038/gim.2015.30
doi: 10.1038/gim.2015.30
pubmed: 25741868
pmcid: 4544753
Ruffo P, Perrone B, Conforti FL (2022) SOD-1 variants in amyotrophic lateral sclerosis: systematic re-evaluation according to ACMG-AMP guidelines. Genes (Basel) 13:537. https://doi.org/10.3390/genes13030537
doi: 10.3390/genes13030537
pubmed: 35328090
Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, Nakanishi A (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 169:13–21. https://doi.org/10.1016/s0022-510x(99)00210-5
doi: 10.1016/s0022-510x(99)00210-5
pubmed: 10540002
Tang L, Ma Y, Liu XL, Chen L, Fan DS (2019) Better survival in female SOD1-mutant patients with ALS: a study of SOD1-related natural history. Transl Neurodegener 8:2. https://doi.org/10.1186/s40035-018-0142-8
doi: 10.1186/s40035-018-0142-8
pubmed: 30637102
pmcid: 6325854
Wiesenfarth M, Günther K, Müller K, Witzel S, Weiland U, Mayer K, Herrmann C, Brenner D, Schuster J, Freischmidt A, Lulé D, Meyer T, Regensburger M, Grehl T, Emmer A, Petri S, Großkreutz J, Rödiger A, Steinbach R, Klopstock T, Reilich P, Schöberl F, Wolf J, Hagenacker T, Weyen U, Zeller D, Ludolph AC, Dorst J (2023) Clinical and genetic features of amyotrophic lateral sclerosis patients with C9orf72 mutations. Brain Commun 5:87. https://doi.org/10.1093/braincomms/fcad087
doi: 10.1093/braincomms/fcad087
Niemann S, Joos H, Meyer T, Vielhaber S, Reuner U, Gleichmann M, Dengler R, Müller U (2004) Familial ALS in Germany: origin of the R115G SOD1 mutation by a founder effect. J Neurol Neurosurg Psychiatry 75:1186–1188. https://doi.org/10.1136/jnnp.2003.028324
doi: 10.1136/jnnp.2003.028324
pubmed: 15258228
pmcid: 1739190
Rosen DR, Bowling AC, Patterson D, Usdin TB, Sapp P, Mezey E, McKenna-Yasek D, O’Regan J, Rahmani Z, Ferrante RJ et al (1994) A frequent ala 4 to val superoxide dismutase-1 mutation is associated with a rapidly progressive familial amyotrophic lateral sclerosis. Hum Mol Genet 3:981–987. https://doi.org/10.1093/hmg/3.6.981
doi: 10.1093/hmg/3.6.981
pubmed: 7951249
Gagliardi D, Ripellino P, Meneri M, Del Bo R, Antognozzi S, Comi GP, Gobbi C, Ratti A, Ticozzi N, Silani V, Ronchi D, Corti S (2023) Clinical and molecular features of patients with amyotrophic lateral sclerosis and SOD1 mutations: a monocentric study. Front Neurol 14:1169689. https://doi.org/10.3389/fneur.2023.1169689
doi: 10.3389/fneur.2023.1169689
pubmed: 37265463
pmcid: 10230028
Spargo TP, Opie-Martin S, Hunt GP, Kalia M, Al Khleifat A, Topp SD, Shaw CE, Al-Chalabi A, Iacoangeli A, Project Mine ALS Sequencing Consortium (2023) SOD1-ALS-Browser: a web-utility for investigating the clinical phenotype in SOD1 amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 3:1–10. https://doi.org/10.1080/21678421.2023.2236650
doi: 10.1080/21678421.2023.2236650
Opie-Martin S, Iacoangeli A, Topp SD, Abel O, Mayl K, Mehta PR, Shatunov A, Fogh I, Bowles H, Limbachiya N, Spargo TP, Al-Khleifat A, Williams KL, Jockel-Balsarotti J, Bali T, Self W, Henden L, Nicholson GA, Ticozzi N, McKenna-Yasek D, Tang L, Shaw PJ, Chio A, Ludolph A, Weishaupt JH, Landers JE, Glass JD, Mora JS, Robberecht W, Damme PV, McLaughlin R, Hardiman O, van den Berg L, Veldink JH, Corcia P, Stevic Z, Siddique N, Silani V, Blair IP, Fan DS, Esselin F, de la Cruz E, Camu W, Basak NA, Siddique T, Miller T, Brown RH, Al-Chalabi A, Shaw CE (2022) The SOD1-mediated ALS phenotype shows a decoupling between age of symptom onset and disease duration. Nat Commun 13:6901. https://doi.org/10.1038/s41467-022-34620-y
doi: 10.1038/s41467-022-34620-y
pubmed: 36371497
pmcid: 9653399
Al-Chalabi A, Andersen PM, Chioza B, Shaw C, Sham PC, Robberecht W, Matthijs G, Camu W, Marklund SL, Forsgren L, Rouleau G, Laing NG, Hurse PV, Siddique T, Leigh PN, Powell JF (1998) Recessive amyotrophic lateral sclerosis families with the D90A SOD1 mutation share a common founder: evidence for a linked protective factor. Hum Mol Genet 7:2045–2050. https://doi.org/10.1093/hmg/7.13.2045
doi: 10.1093/hmg/7.13.2045
pubmed: 9817920
Chapman L, Cooper-Knock J, Shaw PJ (2023) Physical activity as an exogenous risk factor for amyotrophic lateral sclerosis: a review of the evidence. Brain 146:1745–1757. https://doi.org/10.1093/brain/awac470
doi: 10.1093/brain/awac470
pubmed: 36918362
pmcid: 10151186
Lian L, Liu M, Cui L, Guan Y, Liu T, Cui B, Zhang K, Tai H, Shen D (2019) Environmental risk factors and amyotrophic lateral sclerosis (ALS): a case–control study of ALS in China. J Clin Neurosci 66:12–18. https://doi.org/10.1016/j.jocn.2019.05.036
doi: 10.1016/j.jocn.2019.05.036
pubmed: 31155341
Filippini T, Tesauro M, Fiore M, Malagoli C, Consonni M, Violi F, Iacuzio L, Arcolin E, Oliveri Conti G, Cristaldi A, Zuccarello P, Zucchi E, Mazzini L, Pisano F, Gagliardi I, Patti F, Mandrioli J, Ferrante M, Vinceti M (2020) Environmental and occupational risk factors of amyotrophic lateral sclerosis: a population-based case–control study. Int J Environ Res Public Health 17:2882. https://doi.org/10.3390/ijerph17082882
doi: 10.3390/ijerph17082882
pubmed: 32331298
pmcid: 7216189
Vasta R, Callegaro S, Sgambetterra S, Cabras S, Di Pede F, De Mattei F, Matteoni E, Grassano M, Bombaci A, De Marco G, Fuda G, Marchese G, Palumbo F, Canosa A, Mazzini L, De Marchi F, Moglia C, Manera U, Chiò A, Calvo A (2023) Presymptomatic geographical distribution of ALS patients suggests the involvement of environmental factors in the disease pathogenesis. J Neurol 270:5475–5482. https://doi.org/10.1007/s00415-023-11888-8
doi: 10.1007/s00415-023-11888-8
pubmed: 37491680
pmcid: 10576667
Yazar V, Kühlwein JK, Knehr A, Grozdanov V, Ekici AB, Ludolph AC, Danzer KM (2023) Impaired ATF3 signaling involves SNAP25 in SOD1 mutant ALS patients. Sci Rep 13:12019. https://doi.org/10.1038/s41598-023-38684-8
doi: 10.1038/s41598-023-38684-8
pubmed: 37491426
pmcid: 10368635
Bennett SA, Tanaz R, Cobos SN, Torrente MP (2019) Epigenetics in amyotrophic lateral sclerosis: a role for histone post-translational modifications in neurodegenerative disease. Transl Res 204:19–30. https://doi.org/10.1016/j.trsl.2018.10.002
doi: 10.1016/j.trsl.2018.10.002
pubmed: 30391475
Marjanović IV, Selak-Djokić B, Perić S, Janković M, Arsenijević V, Basta I, Lavrnić D, Stefanova E, Stević Z (2017) Comparison of the clinical and cognitive features of genetically positive ALS patients from the largest tertiary center in Serbia. J Neurol 264:1091–1098. https://doi.org/10.1007/s00415-017-8495-y
doi: 10.1007/s00415-017-8495-y
pubmed: 28444446
Andersen PM, Forsgren L, Binzer M, Nilsson P, Ala-Hurula V, Keränen ML, Bergmark L, Saarinen A, Haltia T, Tarvainen I, Kinnunen E, Udd B, Marklund SL (1996) Autosomal recessive adult-onset amyotrophic lateral sclerosis associated with homozygosity for Asp90Ala CuZn-superoxide dismutase mutation. A clinical and genealogical study of 36 patients. Brain 119:1153–1172. https://doi.org/10.1093/brain/119.4.1153
doi: 10.1093/brain/119.4.1153
pubmed: 8813280
Bernard E, Pegat A, Svahn J, Bouhour F, Leblanc P, Millecamps S, Thobois S, Guissart C, Lumbroso S, Mouzat K (2020) Clinical and molecular landscape of ALS patients with SOD1 mutations: novel pathogenic variants and novel phenotypes. A single ALS center study. Int J Mol Sci 21:6807. https://doi.org/10.3390/ijms21186807
doi: 10.3390/ijms21186807
pubmed: 32948071
pmcid: 7554847