Progression to corticobasal syndrome: a longitudinal study of patients with nonfluent primary progressive aphasia and primary progressive apraxia of speech.

Corticobasal syndrome Nonfluent/agrammatic variant primary progressive aphasia Nonverbal oral apraxia Primary progressive apraxia of speech R01-DC10367 (PI Josephs) and R01-DC12519 (PI Whitwell) R01-DC14942 (PI Josephs)

Journal

Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161

Informations de publication

Date de publication:
07 Apr 2024
Historique:
received: 27 11 2023
accepted: 24 01 2024
revised: 23 01 2024
medline: 7 4 2024
pubmed: 7 4 2024
entrez: 7 4 2024
Statut: aheadofprint

Résumé

Nonfluent variant primary progressive aphasia (nfvPPA) and primary progressive apraxia of speech (PPAOS) can be precursors to corticobasal syndrome (CBS). Details on their progression remain unclear. We aimed to examine the clinical and neuroimaging evolution of nfvPPA and PPAOS into CBS. We conducted a retrospective longitudinal study in 140 nfvPPA or PPAOS patients and applied the consensus criteria for possible and probable CBS for every visit, evaluating limb rigidity, akinesia, limb dystonia, myoclonus, ideomotor apraxia, alien limb phenomenon, and nonverbal oral apraxia (NVOA). Given the association of NVOA with AOS, we also modified the CBS criteria by excluding NVOA and assigned every patient to either a progressors or non-progressors group. We evaluated the frequency of every CBS feature by year from disease onset, and assessed gray and white matter volume loss using SPM12. Asymmetric akinesia, NVOA, and limb apraxia were the most common CBS features that developed; while limb dystonia, myoclonus, and alien limb were rare. Eighty-two patients progressed to possible CBS; only four to probable CBS. nfvPPA and PPAOS had a similar proportion of progressors, although nfvPPA progressed to CBS earlier (p-value = 0.046), driven by an early appearance of limb apraxia (p-value = 0.0041). The non-progressors and progressors both showed premotor/motor cortex involvement at baseline, with spread into prefrontal cortex over time. An important proportion of patients with nfvPPA and PPAOS progress to possible CBS, while they rarely develop features of probable CBS even after long follow-up.

Sections du résumé

BACKGROUND AND OBJECTIVES OBJECTIVE
Nonfluent variant primary progressive aphasia (nfvPPA) and primary progressive apraxia of speech (PPAOS) can be precursors to corticobasal syndrome (CBS). Details on their progression remain unclear. We aimed to examine the clinical and neuroimaging evolution of nfvPPA and PPAOS into CBS.
METHODS METHODS
We conducted a retrospective longitudinal study in 140 nfvPPA or PPAOS patients and applied the consensus criteria for possible and probable CBS for every visit, evaluating limb rigidity, akinesia, limb dystonia, myoclonus, ideomotor apraxia, alien limb phenomenon, and nonverbal oral apraxia (NVOA). Given the association of NVOA with AOS, we also modified the CBS criteria by excluding NVOA and assigned every patient to either a progressors or non-progressors group. We evaluated the frequency of every CBS feature by year from disease onset, and assessed gray and white matter volume loss using SPM12.
RESULTS RESULTS
Asymmetric akinesia, NVOA, and limb apraxia were the most common CBS features that developed; while limb dystonia, myoclonus, and alien limb were rare. Eighty-two patients progressed to possible CBS; only four to probable CBS. nfvPPA and PPAOS had a similar proportion of progressors, although nfvPPA progressed to CBS earlier (p-value = 0.046), driven by an early appearance of limb apraxia (p-value = 0.0041). The non-progressors and progressors both showed premotor/motor cortex involvement at baseline, with spread into prefrontal cortex over time.
DISCUSSION CONCLUSIONS
An important proportion of patients with nfvPPA and PPAOS progress to possible CBS, while they rarely develop features of probable CBS even after long follow-up.

Identifiants

DOI: 10.1007/s00415-024-12344-x PMID: 38583104
pubmed: 38583104
doi: 10.1007/s00415-024-12344-x
pii: 10.1007/s00415-024-12344-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIDCD NIH HHS
ID : R01-DC14942
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01-DC10367
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01-DC12519
Pays : United States

Informations de copyright

© 2024. Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Josephs KA et al (2014) The evolution of primary progressive apraxia of speech. Brain 137(Pt 10):2783–2795
pubmed: 25113789 pmcid: 4229741 doi: 10.1093/brain/awu223
Josephs KA, Duffy JR (2008) Apraxia of speech and nonfluent aphasia: a new clinical marker for corticobasal degeneration and progressive supranuclear palsy. Curr Opin Neurol 21(6):688–692
pubmed: 18989114 doi: 10.1097/WCO.0b013e3283168ddd
Utianski RL et al (2018) Clinical progression in four cases of primary progressive apraxia of speech. Am J Speech Lang Pathol 27(4):1303–1318
pubmed: 30458509 pmcid: 6436456 doi: 10.1044/2018_AJSLP-17-0227
Seckin ZI et al (2020) The evolution of parkinsonism in primary progressive apraxia of speech: a 6-year longitudinal study. Parkinsonism Relat Disord 81:34–40
pubmed: 33045651 pmcid: 7769910 doi: 10.1016/j.parkreldis.2020.09.039
Josephs KA et al (2013) Syndromes dominated by apraxia of speech show distinct characteristics from agrammatic PPA. Neurology 81(4):337–345
pubmed: 23803320 pmcid: 3772832 doi: 10.1212/WNL.0b013e31829c5ed5
Gorno-Tempini ML et al (2011) Classification of primary progressive aphasia and its variants. Neurology 76(11):1006–1014
pubmed: 21325651 pmcid: 3059138 doi: 10.1212/WNL.0b013e31821103e6
Rogalski EJ, Mesulam MM (2009) Clinical trajectories and biological features of primary progressive aphasia (PPA). Curr Alzheimer Res 6(4):331–336
pubmed: 19689231 pmcid: 2863134 doi: 10.2174/156720509788929264
Ulugut H et al (2022) The natural history of primary progressive aphasia: beyond aphasia. J Neurol 269(3):1375–1385
pubmed: 34216263 doi: 10.1007/s00415-021-10689-1
Josephs KA et al (2006) Clinicopathological and imaging correlates of progressive aphasia and apraxia of speech. Brain 129(Pt 6):1385–1398
pubmed: 16613895 doi: 10.1093/brain/awl078
Matias-Guiu JA et al (2015) Clinical course of primary progressive aphasia: clinical and FDG-PET patterns. J Neurol 262(3):570–577
pubmed: 25491078 doi: 10.1007/s00415-014-7608-0
Whitwell JL et al (2019) An Evaluation of the Progressive Supranuclear Palsy Speech/Language Variant. Mov Disord Clin Pract 6(6):452–461
pubmed: 31392246 pmcid: 6660227 doi: 10.1002/mdc3.12796
Blake, M.L., et al., Speech and language disorders associated with corticobasal degeneration. Journal of Medical Speech - Language Pathology, 2003. 11: p. 131+.
Armstrong MJ et al (2013) Criteria for the diagnosis of corticobasal degeneration. Neurology 80(5):496–503
pubmed: 23359374 pmcid: 3590050 doi: 10.1212/WNL.0b013e31827f0fd1
Josephs KA et al (2021) A molecular pathology, neurobiology, biochemical, genetic and neuroimaging study of progressive apraxia of speech. Nat Commun 12(1):3452
pubmed: 34103532 pmcid: 8187627 doi: 10.1038/s41467-021-23687-8
Santos-Santos MA et al (2016) Features of patients with Nonfluent/Agrammatic primary progressive aphasia with underlying progressive supranuclear palsy pathology or corticobasal degeneration. JAMA Neurol 73(6):733–742
pubmed: 27111692 pmcid: 4924620 doi: 10.1001/jamaneurol.2016.0412
Duffy JR, Strand EA, Josephs KA (2014) Motor Speech Disorders Associated with Primary Progressive Aphasia. Aphasiology 28(8–9):1004–1017
pubmed: 25309017 doi: 10.1080/02687038.2013.869307
Boxer AL et al (2006) Patterns of brain atrophy that differentiate corticobasal degeneration syndrome from progressive supranuclear palsy. Arch Neurol 63(1):81–86
pubmed: 16401739 doi: 10.1001/archneur.63.1.81
Josephs KA et al (2008) Voxel-based morphometry in autopsy proven PSP and CBD. Neurobiol Aging 29(2):280–289
pubmed: 17097770 doi: 10.1016/j.neurobiolaging.2006.09.019
Josephs KA et al (2012) Characterizing a neurodegenerative syndrome: primary progressive apraxia of speech. Brain 135(Pt 5):1522–1536
pubmed: 22382356 pmcid: 3338923 doi: 10.1093/brain/aws032
Höglinger GU et al (2017) Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria. Mov Disord 32(6):853–864
pubmed: 28467028 pmcid: 5516529 doi: 10.1002/mds.26987
Freitas S et al (2013) Montreal cognitive assessment: validation study for mild cognitive impairment and Alzheimer disease. Alzheimer Dis Assoc Disord 27(1):37–43
pubmed: 22193353 doi: 10.1097/WAD.0b013e3182420bfe
Kertesz A et al (2000) The Frontal Behavioral Inventory in the differential diagnosis of frontotemporal dementia. J Int Neuropsychol Soc 6(4):460–468
pubmed: 10902415 doi: 10.1017/S1355617700644041
Cummings JL et al (1994) The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 44(12):2308–2314
pubmed: 7991117 doi: 10.1212/WNL.44.12.2308
Goetz CG et al (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23(15):2129–2170
pubmed: 19025984 doi: 10.1002/mds.22340
Kertesz, A., The Western aphasia battery. 1982, New York : Grune & Stratton, 1982.
Golbe LI, Ohman-Strickland PA (2007) A clinical rating scale for progressive supranuclear palsy. Brain 130(Pt 6):1552–1565
pubmed: 17405767 doi: 10.1093/brain/awm032
Whitwell JL et al (2011) Clinical correlates of white matter tract degeneration in progressive supranuclear palsy. Arch Neurol 68(6):753–760
pubmed: 21670399 pmcid: 3401587 doi: 10.1001/archneurol.2011.107
Crook R, Hardy J, Duff K (1994) Single-day apolipoprotein E genotyping. J Neurosci Methods 53(2):125–127
pubmed: 7823614 doi: 10.1016/0165-0270(94)90168-6
De Renzi E, Vignolo LA (1962) The token test: A sensitive test to detect receptive disturbances in aphasics. Brain 85:665–678
pubmed: 14026018 doi: 10.1093/brain/85.4.665
Lansing AE et al (1999) An empirically derived short form of the Boston naming test. Arch Clin Neuropsychol 14(6):481–487
pubmed: 14590575 doi: 10.1093/arclin/14.6.481
Yorkston K, M., Speech deterioration in amyotrophic lateral sclerosis : implications for the timing of intervention. Jounal of Medical Speech-Language Pathology, 1993. 1: p. 35–46.
Strand EA et al (2014) The Apraxia of Speech Rating Scale: a tool for diagnosis and description of apraxia of speech. J Commun Disord 51:43–50
pubmed: 25092638 pmcid: 4254321 doi: 10.1016/j.jcomdis.2014.06.008
Botha H et al (2014) Nonverbal oral apraxia in primary progressive aphasia and apraxia of speech. Neurology 82(19):1729–1735
pubmed: 24727315 pmcid: 4032207 doi: 10.1212/WNL.0000000000000412
Utianski RL et al (2018) Prosodic and phonetic subtypes of primary progressive apraxia of speech. Brain Lang 184:54–65
pubmed: 29980072 pmcid: 6171111 doi: 10.1016/j.bandl.2018.06.004
Grossman M et al (2023) Frontotemporal lobar degeneration. Nat Rev Dis Primers 9(1):40
pubmed: 37563165 doi: 10.1038/s41572-023-00447-0
Fadiga, L., L. Craighero, and R. Catherine, Broca’s Region: A Speech Area? Broca's Region, 2006.
Josephs KA et al (2012) Neuroanatomical correlates of the progressive supranuclear palsy corticobasal syndrome hybrid. Eur J Neurol 19(11):1440–1446
pubmed: 22519566 doi: 10.1111/j.1468-1331.2012.03726.x
Dodich A et al (2019) The clinico-metabolic correlates of language impairment in corticobasal syndrome and progressive supranuclear palsy. Neuroimage Clin 24:102009
pubmed: 31795064 pmcid: 6978212 doi: 10.1016/j.nicl.2019.102009
Adeli A et al (2013) Ideomotor apraxia in agrammatic and logopenic variants of primary progressive aphasia. J Neurol 260(6):1594–1600
pubmed: 23358624 pmcid: 3676701 doi: 10.1007/s00415-013-6839-9
Graff-Radford J et al (2012) Parkinsonian motor features distinguish the agrammatic from logopenic variant of primary progressive aphasia. Parkinsonism Relat Disord 18(7):890–892
pubmed: 22575236 pmcid: 3424382 doi: 10.1016/j.parkreldis.2012.04.011
Tetzloff KA et al (2018) Clinical and imaging progression over 10 years in a patient with primary progressive apraxia of speech and autopsy-confirmed corticobasal degeneration. Neurocase 24(2):111–120
pubmed: 29799310 pmcid: 6095655 doi: 10.1080/13554794.2018.1477963
Kwon M et al (2022) Pure prosodic type of primary progressive apraxia of speech mimicking nonfluent aphasia and later progressing to corticobasal syndrome. Alzheimer Dis Assoc Disord 36(4):365–367
pubmed: 35288519 doi: 10.1097/WAD.0000000000000498
Scepkowski LA, Cronin-Golomb A (2003) The alien hand: cases, categorizations, and anatomical correlates. Behav Cogn Neurosci Rev 2(4):261–277
pubmed: 15006289 doi: 10.1177/1534582303260119
Albrecht F et al (2019) Unraveling corticobasal syndrome and alien limb syndrome with structural brain imaging. Cortex 117:33–40
pubmed: 30927559 doi: 10.1016/j.cortex.2019.02.015
Wolpe N et al (2014) The medial frontal-prefrontal network for altered awareness and control of action in corticobasal syndrome. Brain 137(1):208–220
pubmed: 24293266 doi: 10.1093/brain/awt302
Di Stasio F et al (2019) Corticobasal syndrome: neuroimaging and neurophysiological advances. Eur J Neurol 26(5):701-e52
pubmed: 30720235 doi: 10.1111/ene.13928
Hassan A, Josephs KA (2016) Alien Hand Syndrome. Curr Neurol Neurosci Rep 16(8):73
pubmed: 27315251 doi: 10.1007/s11910-016-0676-z
Graff-Radford J et al (2013) The alien limb phenomenon. J Neurol 260(7):1880–8
pubmed: 23572346 pmcid: 3914666 doi: 10.1007/s00415-013-6898-y
Tetreault AM et al (2020) Network Localization of Alien Limb in Patients with Corticobasal Syndrome. Ann Neurol 88(6):1118–1131
pubmed: 32935385 doi: 10.1002/ana.25901
Liuzzi D et al (2016) The anatomical basis of upper limb dystonia: lesson from secondary cases. Neurol Sci 37(9):1393–8
pubmed: 27173653 doi: 10.1007/s10072-016-2598-6
Thompson, P.D., et al., The myoclonus in corticobasal degeneration. Evidence for two forms of cortical reflex myoclonus. Brain, 1994. 117 ( Pt 5): p. 1197–207.

Auteurs

Danna P Garcia-Guaqueta (DP)

Department of Neurology, Behavioral Neurology & Movement Disorders, Mayo Clinic, College of Medicine and Science, Rochester, MN, 55905, USA.

Hugo Botha (H)

Department of Neurology, Behavioral Neurology & Movement Disorders, Mayo Clinic, College of Medicine and Science, Rochester, MN, 55905, USA.

Rene L Utianski (RL)

Department of Neurology, Behavioral Neurology & Movement Disorders, Mayo Clinic, College of Medicine and Science, Rochester, MN, 55905, USA.

Joseph R Duffy (JR)

Department of Neurology, Behavioral Neurology & Movement Disorders, Mayo Clinic, College of Medicine and Science, Rochester, MN, 55905, USA.

Heather M Clark (HM)

Department of Neurology, Behavioral Neurology & Movement Disorders, Mayo Clinic, College of Medicine and Science, Rochester, MN, 55905, USA.

Austin W Goodrich (AW)

Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, 55905, USA.

Nha Trang Thu Pham (NTT)

Department of Radiology, Mayo Clinic, Rochester, MN, 55905, USA.

Mary M Machulda (MM)

Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, 55905, USA.

Matt Baker (M)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA.

Rosa Rademakers (R)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA.
VIB Center for Molecular Neurology, University of Antwerp, Antwerp, Belgium.

Jennifer L Whitwell (JL)

Department of Radiology, Mayo Clinic, Rochester, MN, 55905, USA.

Keith A Josephs (KA)

Department of Neurology, Behavioral Neurology & Movement Disorders, Mayo Clinic, College of Medicine and Science, Rochester, MN, 55905, USA. josephs.keith@mayo.edu.
ORCID: 0000-0003-2930-8634

Classifications MeSH