Repeated cognitive assessments show stable function over time in patients with ALS.
Amyotrophic lateral sclerosis
Cognitive impairment
ECAS
Longitudinal
Survival
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
09 Jun 2024
09 Jun 2024
Historique:
received:
08
03
2024
accepted:
26
05
2024
revised:
24
05
2024
medline:
10
6
2024
pubmed:
10
6
2024
entrez:
9
6
2024
Statut:
aheadofprint
Résumé
Amyotrophic lateral sclerosis (ALS) is a multisystem disorder with not only motor symptoms but also extra-motor features including cognitive impairment. The most common cognitive profile observed in patients with ALS includes deficits in executive function, language, and social cognition. However, longitudinal studies on cognitive changes over time in ALS are sparse. We aimed to investigate the presence and nature of cognitive impairment at the time of ALS diagnosis and its association with survival as well as explore longitudinal cognitive change. Patients (n = 216) were recruited at the Karolinska University Hospital in Stockholm, Sweden. Follow-up visits (n = 307 in total) were performed every 6 months. Cognitive impairment was assessed using the Edinburgh Cognitive and Behavioural ALS Screen (ECAS) and/or Montreal Cognitive Assessment (MoCA). Cognitive impairment was observed in 38% of the patients at the time of ALS diagnosis, and the majority of these patients had deficits in executive function and/or language. Patients with cognitive impairment at the time of diagnosis had a more rapid decline in ALSFRS-R at 12- and 18-months follow-up, and a shorter survival. Cognitive function was stable during the first 2 years after diagnosis, and did not follow the trajectories of decline in motor functions. Cognitive impairment in ALS was associated with a faster decline of motor functions, and shorter survival. However, cognitive function did not deteriorate over time. Cognitive assessment is essential for the patients and caregivers to understand the phenotypic expression of ALS.
Sections du résumé
BACKGROUND
BACKGROUND
Amyotrophic lateral sclerosis (ALS) is a multisystem disorder with not only motor symptoms but also extra-motor features including cognitive impairment. The most common cognitive profile observed in patients with ALS includes deficits in executive function, language, and social cognition. However, longitudinal studies on cognitive changes over time in ALS are sparse. We aimed to investigate the presence and nature of cognitive impairment at the time of ALS diagnosis and its association with survival as well as explore longitudinal cognitive change.
METHOD
METHODS
Patients (n = 216) were recruited at the Karolinska University Hospital in Stockholm, Sweden. Follow-up visits (n = 307 in total) were performed every 6 months. Cognitive impairment was assessed using the Edinburgh Cognitive and Behavioural ALS Screen (ECAS) and/or Montreal Cognitive Assessment (MoCA).
RESULTS
RESULTS
Cognitive impairment was observed in 38% of the patients at the time of ALS diagnosis, and the majority of these patients had deficits in executive function and/or language. Patients with cognitive impairment at the time of diagnosis had a more rapid decline in ALSFRS-R at 12- and 18-months follow-up, and a shorter survival. Cognitive function was stable during the first 2 years after diagnosis, and did not follow the trajectories of decline in motor functions.
CONCLUSION
CONCLUSIONS
Cognitive impairment in ALS was associated with a faster decline of motor functions, and shorter survival. However, cognitive function did not deteriorate over time. Cognitive assessment is essential for the patients and caregivers to understand the phenotypic expression of ALS.
Identifiants
pubmed: 38853167
doi: 10.1007/s00415-024-12479-x
pii: 10.1007/s00415-024-12479-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Svenska Läkaresällskapet
ID : SLS-986189
Organisme : Vetenskapsrådet
ID : 2023-02428
Informations de copyright
© 2024. The Author(s).
Références
Bersano E, Sarnelli MF, Solara V, Iazzolino B, Peotta L, De Marchi F, Facchin A, Moglia C, Canosa A, Calvo A, Chiò A, Mazzini L (2020) Decline of cognitive and behavioral functions in amyotrophic lateral sclerosis: a longitudinal study. Amyotroph Lateral Scler Frontotemporal Degener 21:373–379. https://doi.org/10.1080/21678421.2020.1771732
doi: 10.1080/21678421.2020.1771732
pubmed: 32484726
Strong MJ, Abrahams S, Goldstein LH, Woolley S, Mclaughlin P, Snowden J, Mioshi E, Roberts-South A, Benatar M, HortobáGyi T, Rosenfeld J, Silani V, Ince PG, Turner MR (2017) Amyotrophic lateral sclerosis - frontotemporal spectrum disorder (ALS-FTSD): Revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener 18:153–174. https://doi.org/10.1080/21678421.2016.1267768
doi: 10.1080/21678421.2016.1267768
pubmed: 28054827
pmcid: 7409990
Chiò A, Moglia C, Canosa A, Manera U, Vasta R, Brunetti M, Barberis M, Corrado L, D’Alfonso S, Bersano E, Sarnelli MF, Solara V, Zucchetti JP, Peotta L, Iazzolino B, Mazzini L, Mora G, Calvo A (2019) Cognitive impairment across ALS clinical stages in a population-based cohort. Neurology 93:E984–E994. https://doi.org/10.1212/WNL.0000000000008063
doi: 10.1212/WNL.0000000000008063
pubmed: 31409738
pmcid: 6745732
DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NCA, Flynn H, Adamson J, Kouri N, Wojtas A, Sengdy P, Hsiung GYR, 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
Pender N, Pinto-Grau M, Hardiman O (2020) Cognitive and behavioural impairment in amyotrophic lateral sclerosis. Curr Opin Neurol 33:649–654. https://doi.org/10.1097/WCO.0000000000000862
doi: 10.1097/WCO.0000000000000862
pubmed: 32833751
Hardiman O, Al-Chalabi A, Chio A, Corr EM, Logroscino G, Robberecht W, Shaw PJ, Simmons Z, Van Den Berg LH (2017) Amyotrophic lateral sclerosis. Nat Rev Dis Primers 3:17071. https://doi.org/10.1038/NRDP.2017.71
doi: 10.1038/NRDP.2017.71
pubmed: 28980624
Montuschi A, Iazzolino B, Calvo A, Moglia C, Lopiano L, Restagno G, Brunetti M, Ossola I, Lo Presti A, Cammarosano S, Canosa A, Chiò A (2015) Cognitive correlates in amyotrophic lateral sclerosis: a population-based study in Italy. J Neurol Neurosurg Psychiatry 86:168–173. https://doi.org/10.1136/JNNP-2013-307223
doi: 10.1136/JNNP-2013-307223
pubmed: 24769471
Foucher J, Winroth I, Lovik A, Sennfält S, Pereira JB, Fang F, Lule D, Andersen PM, Ingre C (2023) Validity and reliability measures of the Swedish Karolinska version of the Edinburgh Cognitive and Behavioral ALS Screen (SK-ECAS). Amyotroph Lateral Scler Frontotemporal Degener 24:713–718. https://doi.org/10.1080/21678421.2023.2239857
doi: 10.1080/21678421.2023.2239857
Niven E, Newton J, Foley J, Colville S, Swingler R, Chandran S, Bak TH, Abrahams S (2015) Validation of the Edinburgh Cognitive and Behavioural Amyotrophic Lateral Sclerosis Screen (ECAS): A cognitive tool for motor disorders. ALS 16:172–179. https://doi.org/10.3109/21678421.2015.1030430
doi: 10.3109/21678421.2015.1030430
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699. https://doi.org/10.1111/J.1532-5415.2005.53221.X
doi: 10.1111/J.1532-5415.2005.53221.X
pubmed: 15817019
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. 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
2023 Gene Panel Karolinska University Hospital. Karolinska University Hospital website. https://www.karolinska.se/48eb7b/globalassets/global/2-funktioner/funktion-kul/gmck/gmck-rd/genetik/neurodegenerativasjukdomar-v3.0-88-gener.pdf . Accessed 31 May 2024
Rascovsky K, Grossman M (2013) Clinical diagnostic criteria and classification controversies in frontotemporal lobar degeneration. Int Rev Psychiatry. https://doi.org/10.3109/09540261.2013.763341
doi: 10.3109/09540261.2013.763341
pubmed: 23611345
pmcid: 3906583
G James M Gareth D Witten T Hastie R Tibshirani 2022 An introduction to statistical learning : with applications in R. 607
Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein L, Murphy J, Shoesmith C, Rosenfeld J, Leigh PN, Bruijn L, Ince P, Figlewicz D (2009) Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 10:131–146. https://doi.org/10.1080/17482960802654364
doi: 10.1080/17482960802654364
pubmed: 19462523
Abrahams S, Newton J, Niven E, Foley J, Bak TH (2014) Screening for cognition and behaviour changes in ALS. Amyotroph Lateral Scler Frontotemporal Degener 15:9–14. https://doi.org/10.3109/21678421.2013.805784
doi: 10.3109/21678421.2013.805784
pubmed: 23781974
Beeldman E, Govaarts R, De Visser M, Klein Twennaar M, Van Der Kooi AJ, Van Den Berg LH, Veldink JH, Pijnenburg YAL, De Haan RJ, Schmand BA, Raaphorst J (2020) Progression of cognitive and behavioural impairment in early amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 91:779–780. https://doi.org/10.1136/jnnp-2020-322992
doi: 10.1136/jnnp-2020-322992
pubmed: 32404381
Elamin M, Bede P, Byrne S, Jordan N, Gallagher L, Wynne B, O’Brien C, Phukan J, Lynch C, Pender N, Hardiman O (2013) Cognitive changes predict functional decline in ALS: a population-based longitudinal study. Neurology 80:1590–1597. https://doi.org/10.1212/WNL.0B013E31828F18AC
doi: 10.1212/WNL.0B013E31828F18AC
pubmed: 23553481
Consonni M, Dalla Bella E, Bersano E, Lauria G (2021) Cognitive and behavioural impairment in amyotrophic lateral sclerosis: a landmark of the disease? A mini review of longitudinal studies. Neurosci Lett 754:135898. https://doi.org/10.1016/j.neulet.2021.135898
doi: 10.1016/j.neulet.2021.135898
pubmed: 33862143
Abrahams S, Leigh PN, Goldstein LH (2005) Cognitive change in ALS: a prospective study. Neurology 64:1222–1226. https://doi.org/10.1212/01.WNL.0000156519.41681.27
doi: 10.1212/01.WNL.0000156519.41681.27
pubmed: 15824350
Kasper E, Zydatiss K, Schuster C, Machts J, Bittner D, Kaufmann J, Benecke R, Vielhaber S, Teipel S, Prudlo J (2016) No change in executive performance in ALS patients: a longitudinal neuropsychological study. Neurodegener Dis 16:184–191. https://doi.org/10.1159/000440957
doi: 10.1159/000440957
pubmed: 26613522
Roberts-South A, Findlater K, Strong M, Orange JB (2012) Longitudinal changes in discourse production in amyotrophic lateral sclerosis. Semin Speech Lang 33:79–94. https://doi.org/10.1055/S-0031-1301165
doi: 10.1055/S-0031-1301165
pubmed: 22362326
Strong MJ, Grace GM, Orange JB, Leeper HA, Menon RS, Aere C (1999) A prospective study of cognitive impairment in ALS. Neurology 53:1665–1670. https://doi.org/10.1212/WNL.53.8.1665
doi: 10.1212/WNL.53.8.1665
pubmed: 10563610
Burkhardt C, Neuwirth C, Weber M (2017) Longitudinal assessment of the Edinburgh Cognitive and Behavioural Amyotrophic Lateral Sclerosis Screen (ECAS): lack of practice effect in ALS patients? Amyotroph Lateral Scler Frontotemporal Degener 18:202–209. https://doi.org/10.1080/21678421.2017.1283418
doi: 10.1080/21678421.2017.1283418
pubmed: 28165766
Jutten RJ, Grandoit E, Foldi NS, Sikkes SAM, Jones RN, Choi SE, Lamar ML, Louden DKN, Rich J, Tommet D, Crane PK, Rabin LA (2020) Lower practice effects as a marker of cognitive performance and dementia risk: a literature review. Alzheimer’s and Dementia: Diagnosis, Assessment and Disease Monitoring. https://doi.org/10.1002/dad2.12055
doi: 10.1002/dad2.12055
pubmed: 32671181
pmcid: 7346865
Öijerstedt L, Andersson C, Jelic V, van Swieten JC, Jiskoot LC, Seelaar H, Borroni B, Sanchez-Valle R, Moreno F, Laforce R, Synofzik M, Galimberti D, Rowe JB, Masellis M, Tartaglia MC, Finger E, Vandenberghe R, de Mendonca A, Tagliavini F, Santana I, Ducharme S, Butler CR, Gerhard A, Levin J, Danek A, Otto M, Frisoni G, Ghidoni R, Sorbi S, Rohrer JD, Graff C (2022) Practice effects in genetic frontotemporal dementia and at-risk individuals: a GENFI study. J Neurol Neurosurg Psychiatry 93:336–339. https://doi.org/10.1136/jnnp-2021-327005
doi: 10.1136/jnnp-2021-327005
pubmed: 34408008
Tjokrowijoto P, Phillips M, Ceslis A, Henderson RD, McCombe PA, Robinson GA (2023) Sensitivity and specificity of the ECAS in identifying executive function and social cognition deficits in MND. Amyotroph Lateral Scler Frontotemporal Degener 24:466–474. https://doi.org/10.1080/21678421.2023.2188053
doi: 10.1080/21678421.2023.2188053
pubmed: 36967700
Caga J, Hsieh S, Lillo P, Dudley K, Mioshi E (2019) The impact of cognitive and behavioral symptoms on ALS patients and their caregivers. Front Neurol 10:19. https://doi.org/10.3389/FNEUR.2019.00192
doi: 10.3389/FNEUR.2019.00192