Prevalence and motor-functional correlates of frontotemporal-spectrum disorders in a large cohort of non-demented ALS patients.
Amyotrophic lateral sclerosis
Epidemiology
Frontotemporal degeneration
Neuropsychology
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
05 Sep 2024
05 Sep 2024
Historique:
received:
28
07
2024
accepted:
20
08
2024
revised:
20
08
2024
medline:
5
9
2024
pubmed:
5
9
2024
entrez:
5
9
2024
Statut:
aheadofprint
Résumé
This study aimed at (1) delivering generalizable estimates of the prevalence of frontotemporal-spectrum disorders (FTSDs) in non-demented ALS patients and (2) exploring their motor-functional correlates. N = 808 ALS patients without FTD were assessed for motor-functional outcomes-i.e., disease duration, severity (ALSFRS-R), progression rate (ΔFS), and stage (King's and Milano-Torino-MiToS-systems)-cognition-via the cognitive section of the Edinburgh Cognitive and Behavioural ALS Screen (ECAS)-and behaviour-via the ECAS-Carer Interview. Neuropsychological phenotypes were retrieved via Strong's revised criteria-i.e., ALS cognitively and behaviourally normal (ALScbn) or cognitively and/or behaviourally impaired (ALSci/bi/cbi). Defective ECAS-Total performances were detected in ~ 29% of patients, with the ECAS-Executive being failed by the highest number of patients (~ 30%), followed by the ECAS-Language, -Fluency, and -Memory (~ 15-17%) and -Visuospatial (~ %8). Apathy was the most frequent behavioural change (~ 28%), followed by loss of sympathy/empathy (~ 13%); remaining symptoms were reported in < 4% of patients. The distribution of Strong's classifications was as follows: ALScbn: 46.7%; ALSci/bi/cbi: 22.9%/20.0%/10.4%. Multinomial regressions on Strong's classifications revealed that lower ALSFRS-R scores were associated with a higher probability of ALSbi and ALScbi classifications (p ≤ .008). Higher King's and MiToS stages were associated with a higher probability of ALSbi classification (p ≤ .031). FTSDs affect ~ 50% of non-demented ALS patients, with cognitive deficits being as frequent as behavioural changes. A higher degree of motor-functional involvement is associated with worse behavioural outcomes-with this link being weaker for cognitive deficits.
Sections du résumé
BACKGROUND
BACKGROUND
This study aimed at (1) delivering generalizable estimates of the prevalence of frontotemporal-spectrum disorders (FTSDs) in non-demented ALS patients and (2) exploring their motor-functional correlates.
METHODS
METHODS
N = 808 ALS patients without FTD were assessed for motor-functional outcomes-i.e., disease duration, severity (ALSFRS-R), progression rate (ΔFS), and stage (King's and Milano-Torino-MiToS-systems)-cognition-via the cognitive section of the Edinburgh Cognitive and Behavioural ALS Screen (ECAS)-and behaviour-via the ECAS-Carer Interview. Neuropsychological phenotypes were retrieved via Strong's revised criteria-i.e., ALS cognitively and behaviourally normal (ALScbn) or cognitively and/or behaviourally impaired (ALSci/bi/cbi).
RESULTS
RESULTS
Defective ECAS-Total performances were detected in ~ 29% of patients, with the ECAS-Executive being failed by the highest number of patients (~ 30%), followed by the ECAS-Language, -Fluency, and -Memory (~ 15-17%) and -Visuospatial (~ %8). Apathy was the most frequent behavioural change (~ 28%), followed by loss of sympathy/empathy (~ 13%); remaining symptoms were reported in < 4% of patients. The distribution of Strong's classifications was as follows: ALScbn: 46.7%; ALSci/bi/cbi: 22.9%/20.0%/10.4%. Multinomial regressions on Strong's classifications revealed that lower ALSFRS-R scores were associated with a higher probability of ALSbi and ALScbi classifications (p ≤ .008). Higher King's and MiToS stages were associated with a higher probability of ALSbi classification (p ≤ .031).
CONCLUSIONS
CONCLUSIONS
FTSDs affect ~ 50% of non-demented ALS patients, with cognitive deficits being as frequent as behavioural changes. A higher degree of motor-functional involvement is associated with worse behavioural outcomes-with this link being weaker for cognitive deficits.
Identifiants
pubmed: 39235524
doi: 10.1007/s00415-024-12658-w
pii: 10.1007/s00415-024-12658-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abrahams S (2023) Neuropsychological impairment in amyotrophic lateral sclerosis–frontotemporal-spectrum disorder. Nat Rev Neurol 19:655–667
pubmed: 37828358
doi: 10.1038/s41582-023-00878-z
Strong MJ, Abrahams S, Goldstein LH et al (2017) Amyotrophic lateral sclerosis-frontotemporal-spectrum disorder (ALS-FTSD): Revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener 18:153–174
pubmed: 28054827
pmcid: 7409990
doi: 10.1080/21678421.2016.1267768
Raaphorst J, De Visser M, Linssen WH, De Haan RJ, Schmand B (2010) The cognitive profile of amyotrophic lateral sclerosis: a meta-analysis. Amyotroph Lateral Scler 11:27–37
pubmed: 19180349
doi: 10.3109/17482960802645008
Beeldman E, Raaphorst J, Twennaar MK, de Visser M, Schmand BA, de Haan RJ (2016) The cognitive profile of ALS: a systematic review and meta-analysis update. J Neurol Neurosurg Psychiatry 87:611–619
pubmed: 26283685
doi: 10.1136/jnnp-2015-310734
Finsel J, Uttner I, Vázquez Medrano CR, Ludolph AC, Lulé D (2023) Cognition in the course of ALS—a meta-analysis. Amyotroph Lateral Scler Frontotemporal Degener 24:2–13
pubmed: 35866707
doi: 10.1080/21678421.2022.2101379
Raaphorst J, Beeldman E, De Visser M, De Haan RJ, Schmand B (2012) A systematic review of behavioural changes in motor neuron disease. Amyotroph Lateral Scler 13:493–501
pubmed: 22424127
doi: 10.3109/17482968.2012.656652
Kutlubaev MA, Caga J, Xu Y, Areprintseva DK, Pervushina EV, Kiernan MC (2023) Apathy in amyotrophic lateral sclerosis: systematic review and meta-analysis of frequency, correlates, and outcomes. Amyotroph Lateral Scler Frontotemporal Degener 24:14–23
pubmed: 35352575
doi: 10.1080/21678421.2022.2053721
Gosselt IK, Nijboer TC, Van Es MA (2020) An overview of screening instruments for cognition and behaviour in patients with ALS: selecting the appropriate tool for clinical practice. Amyotroph Lateral Scler Frontotemporal Degener 21:324–336
pubmed: 32157912
doi: 10.1080/21678421.2020.1732424
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
pubmed: 23781974
doi: 10.3109/21678421.2013.805784
Chiò A, Moglia C, Canosa A, Manera U, Vasta R, Brunetti M et al (2019) Cognitive impairment across ALS clinical stages in a population-based cohort. Neurology 93(10):e984–e994
pubmed: 31409738
pmcid: 6745732
doi: 10.1212/WNL.0000000000008063
Al-Chalabi A, Hardiman O, Kiernan MC, Chiò A, Rix-Brooks B, van den Berg LH (2016) Amyotrophic lateral sclerosis: moving towards a new classification system. Lancet Neurol 15:1182–1194
pubmed: 27647646
doi: 10.1016/S1474-4422(16)30199-5
Rascovsky K, Hodges JR, Knopman D et al (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477
pubmed: 21810890
pmcid: 3170532
doi: 10.1093/brain/awr179
Gorno-Tempini ML, Hillis AE, Weintraub S et al (2011) Classification of primary progressive aphasia and its variants. Neurology 76:1006–1014
pubmed: 21325651
pmcid: 3059138
doi: 10.1212/WNL.0b013e31821103e6
Poletti B, Solca F, Carelli L et al (2016) The validation of the Italian Edinburgh cognitive and behavioural ALS screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener 17:489–498
pubmed: 27219526
doi: 10.1080/21678421.2016.1183679
Poletti B, Aiello EN, Solca F et al (2023) Diagnostic properties of the Italian ECAS-Carer Interview (ECAS-CI). Neurol Sci 44:941–946
pubmed: 36417015
doi: 10.1007/s10072-022-06505-x
Serian A, Finsel J, Ludolph AC, Uttner I, Lulé D (2024) Screening instruments of cognition: The relation of the mini-mental state examination to the Edinburgh cognitive and behavioural ALS screen in amyotrophic lateral sclerosis. PLoS ONE 19:e0304593
pubmed: 38900757
pmcid: 11189171
doi: 10.1371/journal.pone.0304593
Perneczky R, Wagenpfeil S, Komossa K, Grimmer T, Diehl J, Kurz A (2006) Mapping scores onto stages: mini-mental state examination and clinical dementia rating. Am J Geriatr Psychiatry 14:139–144
pubmed: 16473978
doi: 10.1097/01.JGP.0000192478.82189.a8
Poletti B, Aiello EN, La Tona A, et al. Single task-level, 2SD-based cutoffs for the Italian version of the Edinburgh Cognitive and Behavioral ALS screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener. 2023:1–4.
Cedarbaum JM, Stambler N, Malta E et al (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. J Neurol Sci 169:13–21
pubmed: 10540002
doi: 10.1016/S0022-510X(99)00210-5
Kimura FC, Fujimura C, Ishida S, Nakajima H, Furutama D, Uehara H et al (2006) Progression rate of ALSFRS-R at time of diagnosis predicts survival time in ALS. Neurology 66:265–267
pubmed: 16434671
doi: 10.1212/01.wnl.0000194316.91908.8a
Roche JC, Rojas-Garcia R, Scott KM, Scotton W, Ellis CE, Burman R et al (2012) A proposed staging system for amyotrophic lateral sclerosis. Brain 135:847–852
pubmed: 22271664
pmcid: 3286327
doi: 10.1093/brain/awr351
Chiò A, Hammond ER, Mora G, Bonito V, Filippini G (2015) Development and evaluation of a clinical staging system for amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 86:38–44
pubmed: 24336810
doi: 10.1136/jnnp-2013-306589
Balendra R, Al Khleifat A, Fang T, Al-Chalabi A (2019) A standard operating procedure for King’s ALS clinical staging. Amyotroph Lateral Scler Frontotemporal Degener 20:159–164
pubmed: 30773950
pmcid: 6558284
doi: 10.1080/21678421.2018.1556696
Ghaderi S, Fatehi F, Kalra S, Batouli SA (2023) MRI biomarkers for memory-related impairment in amyotrophic lateral sclerosis: a systematic review. Amyotroph Lateral Scler Frontotemporal Degener 24:572–588
doi: 10.1080/21678421.2023.2236651
Crockford C, Newton J, Lonergan K, Chiwera T, Booth T, Chandran S et al (2018) ALS-specific cognitive and behaviour changes associated with advancing disease stage in ALS. Neurology 91:e1370–e1380
pubmed: 30209236
pmcid: 6177274
doi: 10.1212/WNL.0000000000006317
McHutchison CA, Wuu J, McMillan CT, Rademakers R, Statland J, Wu G et al (2024) Temporal course of cognitive and behavioural changes in motor neuron diseases. J Neurol Neurosurg Psychiatry 95(4):316–324
pubmed: 37827570
Elamin M, Bede P, Byrne S, Jordan N, Gallagher L, Wynne B et al (2013) Cognitive changes predict functional decline in ALS: a population-based longitudinal study. Neurology 80:1590–1597
pubmed: 23553481
doi: 10.1212/WNL.0b013e31828f18ac
Aiello EN, Pain D, Radici A, Aktipi KM, Sideri R, Appollonio I, Mora G (2022) Cognition and motor phenotypes in ALS: a retrospective study. Neurol Sci 43:5397–5402
pubmed: 35608739
pmcid: 9385798
doi: 10.1007/s10072-022-06157-x
Bersano E, Sarnelli MF, Solara V, Iazzolino B, Peotta L, De Marchi F et al (2020) Decline of cognitive and behavioral functions in amyotrophic lateral sclerosis: a longitudinal study. Amyotroph Lateral Scler Frontotemporal Degener 21:373–379
pubmed: 32484726
doi: 10.1080/21678421.2020.1771732
Canosa A, Moglia C, Manera U, Vasta R, Torrieri MC, Arena V et al (2021) Metabolic brain changes across different levels of cognitive impairment in ALS: a 18F-FDG-PET study. J Neurol, Neurosurg Psychiatry 92:357–363
doi: 10.1136/jnnp-2020-323876
Bock M, Duong YN, Kim A, Allen I, Murphy J, Lomen-Hoerth C (2017) Progression and effect of cognitive-behavioral changes in patients with amyotrophic lateral sclerosis. Neurol Clin Pract 7:488–498
pubmed: 29431172
pmcid: 5800712
doi: 10.1212/CPJ.0000000000000397
Ye S, Jin P, Chen L, Zhang N, Fan D (2021) Prognosis of amyotrophic lateral sclerosis with cognitive and behavioural changes based on a sixty-month longitudinal follow-up. PLoS ONE 16:e0253279
pubmed: 34379621
pmcid: 8357115
doi: 10.1371/journal.pone.0253279
Poletti B, Solca F, Carelli L, Faini A, Madotto F, Lafronza A et al (2018) Cognitive-behavioral longitudinal assessment in ALS: the Italian Edinburgh Cognitive and Behavioral ALS screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener 19:387–395
pubmed: 29804470
doi: 10.1080/21678421.2018.1473443
Aiello EN, Iazzolino B, Pain D, Peotta L, Palumbo F, Radici A et al (2022) The diagnostic value of the Italian version of the Edinburgh Cognitive and Behavioral ALS Screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener 23:527–531
pubmed: 35311435
doi: 10.1080/21678421.2022.2051552
Aiello EN, Solca F, Torre S, Carelli L, Monti A, Ferrucci R et al (2023) Reliable change indices for the Italian Edinburgh cognitive and behavioral ALS screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener 24:339–342
pubmed: 36286187
doi: 10.1080/21678421.2022.2134801
McMillan CT, Wuu J, Rascovsky K, Cosentino S, Grossman M, Elman L et al (2022) Defining cognitive impairment in amyotrophic lateral sclerosis: an evaluation of empirical approaches. Amyotroph Lateral Scler Frontotemporal Degener 23:517–526
pubmed: 35253557
pmcid: 9448823
doi: 10.1080/21678421.2022.2039713
Carelli L, Solca F, Faini A, Madotto F, Lafronza A, Monti A et al (2018) The complex interplay between depression/anxiety and executive functioning: insights from the ECAS in a large ALS population. Front Psychol 9:450
pubmed: 29674987
pmcid: 5895754
doi: 10.3389/fpsyg.2018.00450
Siciliano M, Trojano L, Trojsi F, Monsurro MR, Tedeschi G, Santangelo G (2019) Assessing anxiety and its correlates in amyotrophic lateral sclerosis: The state-trait anxiety inventory. Muscle Nerve 60:47–55
pubmed: 30897219
doi: 10.1002/mus.26475
Mioshi E, Lillo P, Kiernan M, Hodges J (2012) Activities of daily living in motor neuron disease: role of behavioural and motor changes. J Clin Neurosci 19:552–556
pubmed: 22249015
doi: 10.1016/j.jocn.2011.07.042
Aiello EN, Solca F, Torre S, Gentile F, Scheveger F, Olivero M et al (2024) Frontotemporal-spectrum disorders and functional independence in non-demented ALS patients. Neurol Sci 45:1087–1095
pubmed: 37773576
doi: 10.1007/s10072-023-07074-3
Shah JS, Pedraza O, Festic E, Oskarsson B (2021) The relationship between ventilatory function and cognitive and behavioral impairment in ALS. Amyotroph Lateral Scler Frontotemporal Degener 22:62–67
pubmed: 34348534
doi: 10.1080/21678421.2021.1924206
Maranzano A, Verde F, Colombo E, Poletti B, Doretti A, Bonetti R et al (2023) Regional spreading pattern is associated with clinical phenotype in amyotrophic lateral sclerosis. Brain 146:4105–4116
pubmed: 37075222
pmcid: 10545526
doi: 10.1093/brain/awad129
Maranzano A, Poletti B, Solca F, Torre S, Colombo E, Faré M et al (2022) Upper motor neuron dysfunction is associated with the presence of behavioural impairment in patients with amyotrophic lateral sclerosis. Eur J Neurol 29:1402–1409
pubmed: 34989063
doi: 10.1111/ene.15243
Aiello EN, Solca F, Torre S, Patisso V, De Lorenzo A, Treddenti M, et al. Bulbar involvement and cognitive features in amyotrophic lateral sclerosis: a retrospective study on 347 patients. Front Aging Neurosci. 2023;15.
Yang T, Hou Y, Li C, Cao B, Cheng Y, Wei Q, Zhang L et al (2021) Risk factors for cognitive impairment in amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 92:688–693
pubmed: 33563800
doi: 10.1136/jnnp-2020-325701
Moglia C, Calvo A, Canosa A, Manera U, Vasta R, Di Pede F et al (2024) Cognitive and behavioral features of patients with Amyotrophic lateral sclerosis who are carriers of the TARDBP pathogenic variant. Neurology 102:e208082
pubmed: 38261982
pmcid: 10962913
doi: 10.1212/WNL.0000000000208082
Dalla Bella E, Bersano E, Bruzzone MG, Gellera C, Pensato V, Lauria G et al (2022) Behavioral and cognitive phenotypes of patients with amyotrophic lateral sclerosis carrying SOD1 variants. Neurology 99:e2052–e2062
pubmed: 35985819
pmcid: 9651465
doi: 10.1212/WNL.0000000000201044
Calvo A, Moglia C, Canosa A, Manera U, Vasta R, Grassano M et al (2024) High Frequency of Cognitive and Behavioral Impairment in Amyotrophic Lateral Sclerosis Patients with SOD1 Pathogenic Variants. Ann Neurol 96:150–158
pubmed: 38568044
doi: 10.1002/ana.26928