Clinical Characterization of Atypical Primary Progressive Aphasia in a 3-Year Longitudinal Study: A Case Report.
Journal
Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology
ISSN: 1543-3641
Titre abrégé: Cogn Behav Neurol
Pays: United States
ID NLM: 101167278
Informations de publication
Date de publication:
02 09 2021
02 09 2021
Historique:
received:
21
04
2020
accepted:
04
01
2021
entrez:
2
9
2021
pubmed:
3
9
2021
medline:
29
10
2021
Statut:
epublish
Résumé
The logopenic variant of primary progressive aphasia (lvPPA) is the most recent variant of primary progressive aphasia (PPA) to be identified; thus far, it has been poorly investigated. Despite being typically associated with Alzheimer disease (AD), lvPPA has recently been linked to frontotemporal lobe degeneration (FTLD), with distinctive cognitive and neural features that are worthy of further investigation. Here, we describe the neuropsychological and linguistic profile, as well as cerebral abnormalities, of an individual exhibiting PPA and carrying a pathogenetic variant in the GRN gene, from a 3-year longitudinal perspective. The individual's initial profile resembled lvPPA because it was characterized by word-finding difficulties and phonological errors in spontaneous speech in addition to sentence repetition and phonological short-term memory impairments. The individual's structural and metabolic imaging data demonstrated left temporal and bilateral frontal atrophy and hypometabolism, respectively. On follow-up, as the pathology progressed, dysprosody, stereotypical speech patterns, agrammatism, and orofacial apraxia appeared, suggesting an overlap with the nonfluent variant of PPA (nfvPPA). Severe sentence comprehension impairment also became evident. Our longitudinal and multidisciplinary diagnostic approach allowed us to better characterize the progression of a GRN-positive lvPPA profile, providing neuropsychological and imaging indicators that might be helpful to improve classification between different PPA variants and to address a nosological issue. Finally, we discuss the importance of early diagnosis of PPA given the possible overlap between different PPA variants during the progression of the pathology.
Identifiants
pubmed: 34473676
doi: 10.1097/WNN.0000000000000273
pii: 00146965-202109000-00010
doi:
Types de publication
Case Reports
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
233-244Informations de copyright
Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
The authors declare no conflicts of interest.
Références
Alexopoulos GS, Abrams RC, Young RC, et al. 1988. Cornell Scale for Depression in Dementia. Biol Psychiatry. 23:271–284. doi:10.1016/0006-3223(88)90038-8
doi: 10.1016/0006-3223(88)90038-8
Amici S, Ogar J, Brambati SM, et al. 2007. Performance in specific language tasks correlates with regional volume changes in progressive aphasia. Cogn Behav Neurol. 20:203–211. doi:10.1097/WNN.0b013e31815e6265
doi: 10.1097/WNN.0b013e31815e6265
Appollonio I, Leone M, Isella V, et al. 2005. The Frontal Assessment Battery (FAB): normative values in an Italian population sample. Neurol Sci. 26:108–116. doi:10.1007/s10072-005-0443-4
doi: 10.1007/s10072-005-0443-4
Baddeley A. 2000. The episodic buffer: a new component of working memory? Trends Cogn Sci. 4:417–423. doi:10.1016/S1364-6613(00)01538-2
doi: 10.1016/S1364-6613(00)01538-2
Basso A, Capitani E, Laiacona M. 1987. Raven’s Coloured Progressive Matrices: normative values on 305 adult normal controls. Funct Neurol. 2:189–194.
Bergeron D, Gorno-Tempini ML, Rabinovici GD, et al. 2018. Prevalence of amyloid-β pathology in distinct variants of primary progressive aphasia. Ann Neurol. 84:729–740. doi:10.1002/ana.25333
doi: 10.1002/ana.25333
Borroni B, Archetti S, Alberici A, et al. 2008. Progranulin genetic variations in frontotemporal lobar degeneration: evidence for low mutation frequency in an Italian clinical series. Neurogenetics. 9:197–205. doi:10.1007/s10048-008-0127-3
doi: 10.1007/s10048-008-0127-3
Borroni B, Bonvicini C, Galimberti D, et al. 2011. Founder effect and estimation of the age of the Progranulin Thr272fs mutation in 14 Italian pedigrees with frontotemporal lobar degeneration. Neurobiol Aging. 32:555.e1–555.e8. doi:10.1016/j.neurobiolaging.2010.08.009
doi: 10.1016/j.neurobiolaging.2010.08.009
Borroni B, Ferrari F, Galimberti D, et al. 2014. Heterozygous TREM2 mutations in frontotemporal dementia. Neurobiol Aging. 35:934.e7–934.e10. doi:10.1016/j.neurobiolaging.2013.09.017
doi: 10.1016/j.neurobiolaging.2013.09.017
Botha H, Duffy JR, Strand EA, et al. 2014. Nonverbal oral apraxia in primary progressive aphasia and apraxia of speech. Neurology. 82:1729–1735. doi:10.1212/WNL.0000000000000412
doi: 10.1212/WNL.0000000000000412
Bruni AC, Momeni P, Bernardi L, et al. 2007. Heterogeneity within a large kindred with frontotemporal dementia: a novel progranulin mutation. Neurology. 69:140–147. doi:10.1212/01.wnl.0000265220.64396.b4
doi: 10.1212/01.wnl.0000265220.64396.b4
Caffarra P, Vezzadini G, Dieci F, et al. 2002a. Rey-Osterrieth complex figure: normative values in an Italian population sample. Neurol Sci. 22:443–447. doi:10.1007/s100720200003
doi: 10.1007/s100720200003
Caffarra P, Vezzadini G, Dieci F, et al. 2002b. Una versione abbreviata del test di Stroop: dati normativi nella popolazione Italiana. Nuova Riv Neurol. 12:111–115.
Catricalà E, Gobbi E, Battista P, et al. 2017. SAND: a Screening for Aphasia in NeuroDegeneration. development and normative data. Neurol Sci. 38:1469–1483. doi:10.1007/s10072-017-3001-y
doi: 10.1007/s10072-017-3001-y
Chételat G, Desgranges B, Landeau B, et al. 2008. Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer’s disease. Brain. 131:60–71. doi:10.1093/brain/awm288
doi: 10.1093/brain/awm288
De Renzi E, Motti F, Nichelli P. 1980. Imitating gestures: a quantitative approach to ideomotor apraxia. Arch Neurol. 37:6–10. doi:10.1001/archneur.1980.00500500036003
doi: 10.1001/archneur.1980.00500500036003
Deleon J, Miller BL. 2018. Frontotemporal dementia. Handb Clin Neurol. 148:409–430. doi:10.1016/B978-0-444-64076-5.00027-2
doi: 10.1016/B978-0-444-64076-5.00027-2
Dubois B, Slachevsky A, Litvan I, et al. 2000. The FAB: a frontal assessment battery at bedside. Neurology. 55:1621–1626. doi:10.1212/WNL.55.11.1621
doi: 10.1212/WNL.55.11.1621
Farrajota L, Maruta C, Maroco J, et al. 2012. Speech therapy in primary progressive aphasia: a pilot study. Dement Geriatr Cogn Dis Extra. 2:321–331. doi:10.1159/000341602
doi: 10.1159/000341602
Folstein MF, Folstein SE, McHugh PR. 1975. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 12:189–198. doi:10.1016/0022-3956(75)90026-6
doi: 10.1016/0022-3956(75)90026-6
Giovagnoli AR, Del Pesce M, Mascheroni S, et al. 1996. Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci. 17:305–309. doi:10.1007/BF01997792
doi: 10.1007/BF01997792
Gorno-Tempini ML, Brambati SM, Ginex V, et al. 2008. The logopenic/phonological variant of primary progressive aphasia. Neurology. 71:1227–1234. doi:10.1212/01.wnl.0000320506.79811.da
doi: 10.1212/01.wnl.0000320506.79811.da
Gorno-Tempini ML, Dronkers NF, Rankin KP, et al. 2004. Cognition and anatomy in three variants of primary progressive aphasia. Ann Neurol. 55:335–346. doi:10.1002/ana.10825
doi: 10.1002/ana.10825
Gorno-Tempini ML, Hillis AE, Weintraub S, et al. 2011. Classification of primary progressive aphasia and its variants. Neurology. 76:1006–1014. doi:10.1212/WNL.0b013e31821103e6
doi: 10.1212/WNL.0b013e31821103e6
Grossman M. 2010. Primary progressive aphasia: clinicopathological correlations. Nat Rev Neurol. 6:88–97. doi:10.1038/nrneurol.2009.216
doi: 10.1038/nrneurol.2009.216
Grossman M, Ash S. 2004. Primary progressive aphasia: a review. Neurocase. 10:3–18. doi:10.1080/13554790490960440
doi: 10.1080/13554790490960440
Grossman M, Mickanin J, Onishi K, et al. 1996. Progressive nonfluent aphasia: language, cognitive, and PET measures contrasted with probable Alzheimer’s disease. J Cogn Neurosci. 8:135–154. doi:10.1162/jocn.1996.8.2.135
doi: 10.1162/jocn.1996.8.2.135
Harciarek M, Jodzio K. 2005. Neuropsychological differences between frontotemporal dementia and Alzheimer’s disease: a review. Neuropsychol Rev. 15:131–145. doi:10.1007/s11065-005-7093-4
doi: 10.1007/s11065-005-7093-4
Harris JM, Gall C, Thompson JC, et al. 2013. Classification and pathology of primary progressive aphasia. Neurology. 81:1832–1839. doi:10.1212/01.wnl.0000436070.28137.7b
doi: 10.1212/01.wnl.0000436070.28137.7b
Hodges JR, Patterson K, Oxbury S, et al. 1992. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain. 115:1783–1806. doi:10.1093/brain/115.6.1783
doi: 10.1093/brain/115.6.1783
Josephs KA, Duffy JR, Strand EA, et al. 2014. Progranulin-associated PiB-negative logopenic primary progressive aphasia. J Neurol. 261:604–614. doi:10.1007/s00415-014-7243-9
doi: 10.1007/s00415-014-7243-9
Kertesz A, Harciarek M. 2014. Primary progressive aphasia. Scand J Psychol. 55:191–201. doi:10.1111/sjop.12105
doi: 10.1111/sjop.12105
Lawton MP, Brody EM. 1969. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 9:179–186.
Leyton CE, Britton AK, Hodges JR, et al. 2016. Distinctive pathological mechanisms involved in primary progressive aphasias. Neurobiol Aging. 38:82–92. doi:10.1016/j.neurobiolaging.2015.10.017
doi: 10.1016/j.neurobiolaging.2015.10.017
Leyton CE, Hodges JR, McLean CA, et al. 2015. Is the logopenic-variant of primary progressive aphasia a unitary disorder? Cortex. 67:122–133. doi:10.1016/j.cortex.2015.03.011
doi: 10.1016/j.cortex.2015.03.011
Leyton CE, Hsieh S, Mioshi E, et al. 2013. Cognitive decline in logopenic aphasia: more than losing words. Neurology. 80:897–903. doi:10.1212/WNL.0b013e318285c15b
doi: 10.1212/WNL.0b013e318285c15b
Leyton CE, Villemagne VL, Savage S, et al. 2011. Subtypes of progressive aphasia: application of the International Consensus Criteria and validation using β-amyloid imaging. Brain. 134:3030–3043. doi:10.1093/brain/awr216
doi: 10.1093/brain/awr216
Luzzatti C, Willmes K, De Bleser R, et al. 1994. Nuovi dati normativi per la versione italiana dell’Aachener Aphasie Test (A.A.T.). [New normative data for the Italian version of the Aachener Aphasia Test (A.A.T.)]. Arch Psicol Neurol Psichiatr. 55:1086–1131.
Martino MG, Pappalardo F, Re AM, et al. 2011. La valutazione della dislessia nell’adulto. Un contributo alla standardizzazione della Batteria dell’Università di Padova [Dyslexia assessment in adults: A contribution to the standardization of a battery of the University of Padova]. Dislessia. 2:119–134.
Matías-Guiu JA, Cabrera-Martín MN, Moreno-Ramos T, et al. 2015. Amyloid and FDG-PET study of logopenic primary progressive aphasia: evidence for the existence of two subtypes. J Neurol. 262:1463–1472. doi:10.1007/s00415-015-7738-z
doi: 10.1007/s00415-015-7738-z
Mauri M, Carlesimo G, Graceffa A, et al. 1997. Standardizzazione di due nuovi test di memoria: apprendimento di liste di parole correlate e non correlate semanticamente. Arch Psicol Neurol Psichiatr. 58:621–645.
Measso G, Cavarzeran F, Zappalà G, et al. 1993. The Mini-Mental State Examination: normative study of an Italian random sample. Dev Neuropsychol. 9:77–85. doi:10.1080/87565649109540545
doi: 10.1080/87565649109540545
Mesulam M, Johnson N, Krefft TA, et al. 2007. Progranulin mutations in primary progressive aphasia: the PPA1 and PPA3 families. Arch Neurol. 64:43–47. doi:10.1001/archneur.64.1.43
doi: 10.1001/archneur.64.1.43
Mesulam M, Wicklund A, Johnson N, et al. 2008. Alzheimer and frontotemporal pathology in subsets of primary progressive aphasia. Ann Neurol. 63:709–719. doi:10.1002/ana.21388
doi: 10.1002/ana.21388
Mesulam MM, Weintraub S, Rogalski EJ, et al. 2014. Asymmetry and heterogeneity of Alzheimer’s and frontotemporal pathology in primary progressive aphasia. Brain. 137:1176–1192. doi:10.1093/brain/awu024
doi: 10.1093/brain/awu024
Minoshima S, Drzezga AE, Barthel H, et al. 2016. SNMMI procedure standard/EANM practice guideline for amyloid PET imaging of the brain 1.0. J Nucl Med. 57:1316–1322. doi:10.2967/jnumed.116.174615
doi: 10.2967/jnumed.116.174615
Monaco M, Costa A, Caltagirone C, et al. 2013. Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci. 34:749–754. doi:10.1007/s10072-014-2019-7
doi: 10.1007/s10072-014-2019-7
Murley AG, Coyle-Gilchrist I, Rouse MA, et al. 2020. Redefining the multidimensional clinical phenotypes of frontotemporal lobar degeneration syndromes. Brain. 143:1555–1571. doi:10.1093/brain/awaa097
doi: 10.1093/brain/awaa097
Novelli G, Papagno C, Capitani E, et al. 1986a. Tre test clinici di memoria verbale a lungo termine: Taratura su soggetti normali [Three clinical tests for the assessment of verbal long-term memory function: norms from 320 normal subjects]. Arch Psicol Neurol Psichiatr. 47:278–296.
Novelli G, Papagno C, Capitani E, et al. 1986b. Tre test clinici di ricerca e produzione lessicale. Taratura su sogetti normali [Three clinical tests for the assessment of lexical retrieval and production: norms from 320 normal subjects]. Arch Psicol Neurol Psichiatr. 47:477–506.
Orsini A, Grossi D, Capitani E, et al. 1987. Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. Ital J Neurol Sci. 8:539–548. doi:10.1007/BF02333660
doi: 10.1007/BF02333660
Rabinovici GD, Jagust WJ, Furst AJ, et al. 2008. A beta amyloid and glucose metabolism in three variants of primary progressive aphasia. Ann Neurol. 64:388–401. doi:10.1002/ana.21451
doi: 10.1002/ana.21451
Rogalski E, Cobia D, Harrison TM, et al. 2011. Anatomy of language impairments in primary progressive aphasia. J Neurosci. 31:3344–3350. doi:10.1523/JNEUROSCI.5544-10.2011
doi: 10.1523/JNEUROSCI.5544-10.2011
Rohrer JD, Crutch SJ, Warrington EK, et al. 2010a. Progranulin-associated primary progressive aphasia: a distinct phenotype? Neuropsychologia. 48:288–297. doi:10.1016/j.neuropsychologia.2009.09.017
doi: 10.1016/j.neuropsychologia.2009.09.017
Rohrer JD, Ridgway GR, Crutch SJ, et al. 2010b. Progressive logopenic/phonological aphasia: erosion of the language network. Neuroimage. 49:984–993. doi:10.1016/j.neuroimage.2009.08.002
doi: 10.1016/j.neuroimage.2009.08.002
Rudner M, Rönnberg J. 2008. The role of the episodic buffer in working memory for language processing. Cogn Process. 9:19–28. doi:10.1007/s10339-007-0183-x
doi: 10.1007/s10339-007-0183-x
Santos-Santos MA, Rabinovici GD, Iaccarino L, et al. 2018. Rates of amyloid imaging positivity in patients with primary progressive aphasia. JAMA Neurol. 75:342–352. doi:10.1001/jamaneurol.2017.4309
doi: 10.1001/jamaneurol.2017.4309
Spinelli EG, Mandelli ML, Miller ZA, et al. 2017. Typical and atypical pathology in primary progressive aphasia variants. Ann Neurol. 81:430–443. doi:10.1002/ana.24885
doi: 10.1002/ana.24885
Spinnler H, Tognoni G. 1987. Standardizzazione e taratura italiana di test neuropsicologici. Gruppo Italiano per lo Studio Neuropsicologico dell’Invecchiamento [Italian standardization and classification of neuropsychological tests. The Italian Group on the Neuropsychological Study of Aging]. Ital J Neurol Sci. 8:1–120.
Tee BL, Gorno-Tempini ML. 2019. Primary progressive aphasia: a model for neurodegenerative disease. Curr Opin Neurol. 32:255–265. doi:10.1097/WCO.0000000000000673
doi: 10.1097/WCO.0000000000000673
Teichmann M, Kas A, Boutet C, et al. 2013. Deciphering logopenic primary progressive aphasia: a clinical, imaging and biomarker investigation. Brain. 136:3474–3488. doi:10.1093/brain/awt266
doi: 10.1093/brain/awt266
Varrone A, Asenbaum S, Vander Borght T, et al. 2009. EANM procedure guidelines for PET brain imaging using [18F] FDG, version 2. Eur J Nucl Med Mol Imaging. 36:2103–2110. doi:10.1007/s00259-009-1264-0
doi: 10.1007/s00259-009-1264-0
Whitwell JL, Duffy JR, Strand EA, et al. 2015. Clinical and neuroimaging biomarkers of amyloid-negative logopenic primary progressive aphasia. Brain Lang. 142:45–53. doi:10.1016/j.bandl.2015.01.009
doi: 10.1016/j.bandl.2015.01.009
Zhang M, Xi Z, Zinman L, et al. 2015. Mutation analysis of CHCHD10 in different neurodegenerative diseases. Published online March 31. Brain. 138:e380–e380.