Patterns of Decline in Naming and Semantic Knowledge in Primary Progressive Aphasia

Rajani Sebastian, Carol B Thompson, Nae-Yuh Wang, Amy Wright, Aaron Meyer, Rhonda B Friedman, Argye E Hillis, Donna C Tippett, Rajani Sebastian, Carol B Thompson, Nae-Yuh Wang, Amy Wright, Aaron Meyer, Rhonda B Friedman, Argye E Hillis, Donna C Tippett

Abstract

Background: Individuals with primary progressive aphasia (PPA) and their caregivers want to know what to expect so that they can plan support appropriately. The ability to predict decline in naming and semantic knowledge, and advise individuals with PPA and their caregivers regarding future planning, would be invaluable clinically.

Aims: The aims of this study were to investigate patterns of decline in naming and semantic knowledge in each of the clinical variants of PPA (logopenic variant PPA, lvPPA; nonfluent agrammatic PPA, nfaPPA; and semantic variant PPA, svPPA) and to examine the effects of other variables on rate of decline. We hypothesized that speech-language rehabilitation, higher education, and higher baseline test scores would be associated with slower decline, and older age with faster decline.

Methods and procedures: A total of ninety-four participants with PPA underwent language testing, including thirty six participants with lvPPA, thirty-one participants with nfaPPA, and twenty-seven participants with svPPA. All participant groups were similar in age and education. We focused on decline on three tests: the short form of the Boston Naming Test (BNT), the Hopkins Assessment of Naming Actions (HANA), and the short form of the Pyramids and Palm Trees Test (PPTT).

Outcome and results: Across language tests, the most precipitous rates of decline (loss of points per month) occurred in nfaPPA, followed by svPPA, then lvPPA. Female sex, longer symptom duration, higher baseline test score, and speech-language rehabilitation were associated with slower decline.

Conclusions: PPA variants were distinguishable by rapidity of decline, with nfaPPA having the most precipitous decline. As hypothesized, higher baseline test scores and speech-language rehabilitation were associated with slower decline. Surprisingly, age and education were not important prognostically for individuals in this study. Further study of prognostically-relevant variables in PPA is indicated in this population.

Keywords: Primary progressive aphasia; language symptoms; logopenic variant primary progressive aphasia; nonfluent agrammatic primary progressive aphasia; semantic variant primary progressive aphasia.

Figures

Figure 1:
Figure 1:
Decline in Scores on the Boston Naming Test over Time in PPA Variants lvPPA, logopenic primary progressive aphasia (light gray); nfaPPA, nonfluent agrammatic primary progressive aphasia (black); svPPA semantic variant primary progressive aphasia (medium gray); duration: symptom duration. The solid lines represent data points for each participants and the dashed lines represent the average decline for each variant.
Figure 2:
Figure 2:
Decline in Scores on the Hopkins Assessment of Naming Actions over Time in PPA Variants lvPPA, logopenic primary progressive aphasia (light gray); nfaPPA, nonfluent agrammatic primary progressive aphasia (black); svPPA semantic variant primary progressive aphasia (medium gray); duration: symptom duration. The solid lines represent data points for each participants and the dashed lines represent the average decline for each variant.
Figure 3:
Figure 3:
Decline in Scores on the Pyramids and Palm Trees Test over Time in PPA Variants lvPPA, logopenic primary progressive aphasia (light gray); nfaPPA, nonfluent agrammatic primary progressive aphasia (black); svPPA semantic variant primary progressive aphasia (medium gray); duration: symptom duration. The solid lines represent data points for each participants and the dashed lines represent the average decline for each variant.

References

    1. Alladi S, Xuereb J, Bak T, Nestor P, Knibb J, Patterson K, & Hodges JR (2007). Focal cortical presentations of Alzheimer’s disease. Brain, 130, 2636–2645.
    1. Bak TH, & Hodges JR (2003). Kissing and dancing—a test to distinguish the lexical and conceptual contributions to noun/verb and action/object dissociation. Preliminary results in patients with frontotemporal dementia. Journal of Neurolinguistics, 16(2–3), 169–181.
    1. Beeson PM, King RM, Bonakdarpour B, Henry ML, Cho H, & Rapcsak SZ (2011). Positive effects of language treatment for the logopenic variant of primary progressive aphasia. Journal of Molecular Neuroscience, 45, 724–736. doi: 10.1007/s12031-011-9579-2
    1. Botha H, Duffy JR, Whitwell JL, Strand EA, Machulda MM, Schwarz CG, … Josephs KA (2015). Classification and clinicoradiologic features of primary progressive aphasia (PPA) and apraxia of speech. Cortex, 69, 220–236.
    1. Brambati SM, Amici S, Racine CA, Neuhaus J, Miller Z, Ogar J, ... & Gorno-Tempini ML (2015). Longitudinal gray matter contraction in three variants of primary progressive aphasia: a tenser-based morphometry study. NeuroImage: Clinical, 8, 345–355.
    1. Breining BL, Lala T, Martínez Cuitiño M, Manes F, Peristeri E, Tsapkini K, ... & Hillis AE. (2015a). A brief assessment of object semantics in primary progressive aphasia. Aphasiology, 29(4), 488–505.
    1. Breining BL, Tippett DC, Davis C, Posner J, Sebastian R, Oishie K, ... & Hillis AE (2015b, May). Assessing dissociations of object and action naming in acute stroke. Paper presented at the Clinical Aphasiology Conference, Monterey, CA.
    1. Caramazza A, & Hillis AE (1990). Where do semantic errors come from? Cortex, 26, 95–122.
    1. Corbett F, Jefferies E, Ehsan S, &, Lambon Ralph MA (2009). Different impairments of semantic cognition in semantic dementia and semantic aphasia: Evidence from the non-verbal domain. Brain, 132, 2593–2608. doi: 10.1093/brain/awp146.
    1. Croot K, Ballard K, Leyton CE, & Hodges JR (2012). Apraxia of speech and phonological errors in the diagnosis of nonfluent/agrammatic and logopenic variants of primary progressive aphasia. Journal of Speech, Language, and Hearing Research, 55, S1562–72. doi: 10.1044/1092-4388(2012/11-0323.
    1. Dabul B (2000). Apraxia Battery for Adults–Second Edition. Austin TX: Pro-Ed.
    1. Davies RR, Hodges JR, Kril JJ, Patterson K, Halliday GM, & Xuereb JH (2005). The pathological basis of semantic dementia. Brain, 128, 1984–1995. doi: 10.1093/brain/awh582
    1. Etcheverry L, Seidel B, Grande M, Schulte S, Pieperhoff P, Sudmeyer M, …& Heim S (2012). The time course of neurolinguistic and neurobehavioral symptoms in three cases of logopenic primary progressive aphasia. Neuropsychologia, 50, 1708–1718. doi: 10.1016/j.neuropsychologia.2012.03.028.
    1. Faria AV, Sebastian R, Newhart M, Mori S, & Hillis AE Longitudinal imaging and deterioration in word comprehension in primary progressive aphasia: Potential clinical significance. Aphasiology, 28, 948–963. doi:10.1080/02687038.2014.911241.
    1. Folstein MF, Folstein MF, & McHugh PR (1975). Mini Mental State: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. .
    1. Frattali CM, Thompson CK, Holland AL, Wohl CB, & Ferketic MM (1995). American Speech-Language-Hearing Association Functional Assessment of Communication Skills for Adults. ASHA Fulfilment Operations, Rockville, MD.
    1. Fridriksson J, Nettles C, Davis M, Morrow L, & Montgomery A (2006). Functional communication and executive function in aphasia. Clinical Linguistics and Phonetics, 20, 401–410. doi: 10.1080/02699200500075781.
    1. Giannini LAA, Irwin DJ, McMillan CT, Ash S, Rascovsky K, Wolk DA, . . . & Grossman M (2017). Clinical marker for Alzheimer disease pathology in logopenic primary progressive aphasia. Neurology, 88, 2276–284. Doi: 10.1212?WNL.0000000000004034
    1. Gorno-Tempini ML, Brambati SM, Ginex V, Ogar J, Dronkers NF, Marcone A, . . . & Miller BL (2008). The logopenic/phonological variant of primary progressive aphasia. Neurology, 71, 1227–1234. doi: 10.1212/01.wnl.0000320506.79811.da.
    1. Gorno-Tempini ML, Dronkers NF, Rankin KP, Ogar JM, Phengrasamy L, Rosen HJ, . . . & Miller BL (2004a). Cognition and anatomy in three variants of primary progressive aphasia. Annals of Neurology, 55, 335–346. doi: 10.1002/ana.10825.
    1. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, . . . & Grossman M (2011). Classification of primary progressive aphasia and its variants. Neurology, 76, 1006–1014. doi: 10.1212/WNL.0b013e31821103e6.
    1. Gorno-Tempini ML, Murray RC, Rankin KP, Weiner MW, & Miller BL (2004b). Clinical, cognitive and anatomical evolution from nonfluent progressive aphasia to corticobasal syndrome: A case report. Neurocase, 10, 426–436. doi: 10.1080/13554790490894011.
    1. Gorno-Tempini ML, Ogar JM, Brambati SM, Wang P, Jeong JH, Rankin KP, . . . & Miller BL (2006). Anatomical correlates of early mutism in progressive nonfluent aphasia. Neurology, 67, 1849–1851. doi: 10.1212/01.wnl.0000237038.55627.5b.
    1. Grossman M (2002). Progressive aphasic syndromes: Clinical and theoretical advances. Current Opinion in Neurology, 15, 409–413.
    1. Grossman M (2010). Primary progressive aphasia: Clinicopathological correlations. Nature Reviews Neurology, 6, 88–97.
    1. Grossman M, McMillan C, Moore P, Ding L, Glosser G, Work M, & Gee J (2004). What’s in a name: Voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer’s disease, frontotemporal dementia and corticobasal degeneration. Brain, 127, 628–649. doi: 10.1093/brain/awh075.
    1. Grossman M, Xie SX, Libon DJ, Wang X, Massimo L, Moore P, . . . & Trojanowski JQ (2008). Longitudinal decline in autopsy-defined frontotemporal lobar degeneration. Neurology, 70, 2036–2045. doi: 10.1212/01.wnl.0000303816.25065.bc
    1. Henry ML, Rising K, DeMarco AT, Miller BL, Gorno-Tempini ML, & Beeson PM (2013). Examining the value of lexical retrieval treatment in primary progressive aphasia: Two positive cases. Brain and Language, 127, 145–156.
    1. Hillis AE, Heidler-Gary J, Newhart M, Chang S, Ken L, & Bak T (2006). Naming and comprehension in primary progressive aphasia: The influence of grammatical word class. Aphasiology, 20, 246–256. doi: 10.1080/02687030500473262.
    1. Hillis AE, Oh S, & Ken L (2004). Deterioration of naming nouns versus verbs in primary progressive aphasia. Annals of Neurology, 55, 268–275. doi: 10.1002/ana.10812.
    1. Hillis AE, & Tippett DC (2014). Stroke recovery: Surprising influences and residual consequences. Advances in Medicine, 378263.
    1. Hillis AE, Tuffiash E, & Caramazza A (2002). Modality-specific deterioration in naming verbs in nonfluent primary progressive aphasia. Journal of Cognitive Neuroscience, 14, 1099–1108. doi: 10.1162/089892902320474544.
    1. Hodges JR, Mitchell J Dawson K Spillantini MG, Xuereb JH, McMonagle P, . . .& Patterson K (2010). Semantic dementia: demography, familial factors and survival in a consecutive series of 100 cases. Brain, 133, 300–306. doi:10.1093/brain/awp248
    1. Howard D, & Patterson K (1992). The pyramids and palm trees test: A test of semantic access from words and pictures. Cambridge, UK: Pearson.
    1. Hurley RS, Paller KA, Rogalski EJ, & Mesulam M-M (2012). Neural mechanisms of object naming and word comprehension in primary progressive aphasia. Journal of Neuroscience, 32, 4848–4855. doi: 10.1523/JNEUROSCI.5984-11.2012.
    1. Hurley RS, Paller KA, Wieneke CA, Weintraub S, Thompson CK, Federmeier KD, & Mesulam M-M (2009). Electrophysiology of object naming in primary progressive aphasia. Journal of Neuroscience, 29, 15762–15769. doi: 10.1523/JNEUROSCI.2912-09.2009.
    1. Jokel R, Rochon E, & Anderson ND (2010). Errorless learning of computer-generated words in a patient with semantic dementia. Neuropsychological Rehabilitation, 20, 16–41.
    1. Jokel R, Rochon E, & Leonard C (2006). Treating anomia in semantic dementia: Improvement, maintenance, or both? Neuropsychological Rehabilitation, 16, 241–256.
    1. Josephs KA, Duffy JR, Strand EA, Whitwell JL, Layton KF, Parisi JE,. . . Petersen RC (2006). Clinicopathological and imaging correlates of progressive aphasia and apraxia of speech. Brain, 129, 1385–1398. doi: 10.1093/brain/awl078.
    1. Josephs KA, Stroh A, Dugger B, & Dickson DW (2009). Evaluation of subcortical pathology and clinical correlations in FTLD-U variants. Acta Neuropathologica, 118, 349–358. doi: 10.1007/s00401-009-0547-7
    1. Josephs KA, Whitwell JL, Duffy JR, Vanvoorst WA, Strand EA, Hu WT, . . . & Petersen RC (2008). Progressive aphasia secondary to Alzheimer disease vs FTLD pathology. Neurology, 70, 25–34. doi: 10.1212/01.wnl.0000287073.12737.35.
    1. Kaplan E, Goodglass H, & Weintraub S (2001). Boston naming test-2 (BNT-2). Austin TX: Pro-Ed.
    1. Kertesz A, McMonagle P, Blair M, Davidson W, & Munoz DG (2005). The evolution and pathology of frontotemporal dementia. Brain, 128, 1996–2005. doi: 10.1093/brain/awh598
    1. Knopman DS, Boeve BF, Parisi JE, Dickson DW, Smith GE, Ivnik RJ, . . . & Petersen RC (2005). Antemortem diagnosis of frontotemporal lobar degeneration. Annals of Neurology. 57, 480–488. doi: 10.1002/ana.20425
    1. Le Rhun E, Richard F, & Pasquier F (2005). Natural history of primary progressive aphasia. Neurology, 65, 887–891. .
    1. Liang J, Bennett JM, Shaw BA, Quiñones AR, Ye W, Xu X, & Ofstedal MB (2008). Gender differences in functional status in middle and older age: Are there any age variations? The Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 63, S282–S292. doi: 10.1093/geronb/63.5.S282
    1. Loonstra AS, Tarlow AR, & Sellers AH (2001). COWAT metanorms across age, education, and gender. Applied Neuropsychology, 8(3), 161–166.
    1. Machulda MM, Whitwell JL, Duffy JR, Strand EA, Dean PM, Senjem ML, & Josephs KA (2013). Identification of an atypical variant of logopenic progressive aphasia. Brain and Language, 127(2), 139–144. doi: 10.1016/j.bandl.2013.02.007
    1. Mack WJ, Freed DM, Williams BW, & Henderson VW (1992). Boston naming test: Shortened versions for use in Alzheimer’s disease. Journal of Gerontology, 47, 154–158. doi: 10.1093/geronj/47.3.P154.
    1. Mackenzie IR, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, . . . & Mann DM (2006). Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: classification and relation to clinical phenotype. Acta Neuropathologica, 112, 539–549. doi: 10.1007/s00401-006-0138-9
    1. Mesulam M-M (1982). Slowly progressive aphasia without generalized dementia. Annals of Neurology, 11, 592–598. doi: 10.1002/ana.410110607.
    1. Mesulam M-M (2001). Primary progressive aphasia. Annals of Neurology, 49, 425–432. doi: 10.1002/ana.91.
    1. Mesulam M-M (2013). Primary progressive aphasia and the language network: The 2013 H. Houston Merritt Lecture. Neurology, 81, 456–462. doi: 10.1212/WNL.0b013e31829d87df.
    1. Mesulam M, Wicklund A, Johnson N, Rogalski E, Léger GC, Rademaker A, . . .& Bigio EH (2008). Alzheimer and frontotemporal pathology in subsets of primary progressive aphasia. Annals of Neurology, 63, 709–719. doi: 10.1002/ana.21388
    1. Mesulam M-M, Wieneke C, Hurley R, Rademaker A, Thompson CK, Weintraub S, & Rogalski EJ (2013). Words and objects at the tip of the left temporal lobe in primary progressive aphasia. Brain, 136, 601–618. doi: 10.1093/brain/aws336.
    1. Mesulam M-M, Wieneke C, Thompson C, Rogalski E, & Weintraub S (2012). Quantitative classification of primary progressive aphasia at early and mild impairment stages. Brain, 135, 1537–1553. doi: 10.1093/brain/aws080.
    1. Meyer AM, Getz HR, Brennan D, Hu T, & Friedman RB (2016). Telerehabilitation of anomia in primary progressive aphasia. Aphasiology, 30, 483–507.
    1. Meyer AM, Snider SF, Eckmann CB, & Friedman RB (2015). Prophylactic treatments for anomia in the logopenic variant of primary progressive aphasia: Cross-language transfer. Aphasiology, 29, 1062–1081.
    1. Newhart M, Davis C, Kannan V, Heidler-Gary J, Cloutman L, & Hillis AE (2009). Therapy for naming deficits in two variants of primary progressive aphasia. Aphasiology, 23, 823–834.
    1. Ng JH, Kaftarian SK, Tilson WM, Gorrell P, Chen X, Chesley FD, & Scholle SH (2010). Self-reported delays in receipt of health care among women with diabetes and cardiovascular conditions. Women’s Health Issues, 20, 316–322.
    1. Rogalski E, Cobia D, Harrison TM, Wieneke C, Thompson CK, Weintraub S, & Mesulam M-M (2011a). Anatomy in language impairments in primary progressive aphasia. Journal of Neuroscience, 31, 3344–3350. doi: 10.1523/JNEUROSCI.5544-10.2011.
    1. Rogalski E, Cobia D, Harrison TM, Wieneke C, Weintraub S, & Mesulam M-M (2011b). Progression of language decline and cortical atrophy in variants of primary progressive aphasia. Neurology, 76, 1804–1810.
    1. Rogalsky C, Love T, Driscoll D, Anderson SW, & Hickok G (2011. c). Are mirror neurons the basis of speech perception? Evidence from five cases with damage to the purported human mirror system. Neurocase, 7, 178–187.
    1. Rohrer JD, Caso F, Mahoney C, Henry M, Rosen HJ, Rabinovici G, . . .& Gorno-Tempini ML (2013). Patterns of longitudinal brain atrophy in the logopenic variant of primary progressive aphasia. Brain and Language, 127, 121–126. doi: 10.1016/j.bandl.2012.12.008.
    1. Rohrer JD, Warren JD, Modat M, Ridgway GR, Douiri A, Rossor MN, . . . & Fox NC (2009). Patterns of cortical thinning in the language variants of frontotemporal lobar degeneration. Neurology, 72, 1562–1569. doi: 10.1212/WNL.0b013e3181a4124e
    1. Seeley WW, Bauer AM, Miller BL, Gorno-Tempini ML, Kramer JH, Weiner M, & Rosen HJ (2005). The natural history of temporal variant frontotemporal dementia. Neurology, 64, 1384–1390. doi: 10.1212/01.WNL.0000158425.46019.5C.
    1. Seeley WW, Crawford R, Rascovsky K, Kramer JH, Weiner M, Miller BL, & Gorno-Tempini ML (2008). Frontal paralimbic network atrophy in very mild behavioral variant frontotemporal dementia. Archives of Neurology, 65, 249–255. doi: 10.1001/archneurol.2007.38.
    1. Snowden J, Neary D, & Mann D (2007). Frontotemporal lobar degeneration: clinical and pathological relationships. Acta Neuropathologica, 114, 31–38. doi: 10.1007/s00401-007-0236-3
    1. Spinelli EG, Mandelli ML, Miller ZA, Santos-Santos MA, Wilson SM, Agosta F, . . . & Gorno-Tempini ML (2017). Typical and atypical pathology in primary progressive aphasia variants. Annals of Neurology, 81, 430–43. doi:10.1002/ana.24885
    1. Sun Y, Lee R, Chen Y, Collinson S, Thakor N, Bezerianos A, & Sim K (2015). Progressive gender differences of structural brain networks in healthy adults: A longitudinal, diffusion tensor imaging study. PLoS ONE, 10, e0118857 10.1371/journal.pone.0118857
    1. Suneja A, Gonzalez-Fernandez M, & Hillis A (2014). Predictors of recovery of chronic aphasia. Neurology, 82, Supplement P6228.
    1. Thompson CK, Lukic S, King MC, Mesulam MM, & Weintraub S (2012). Verb and noun deficits in stroke-induced and primary progressive aphasia: The Northwestern Naming Battery. Aphasiology, 26, 632–655.
    1. Tree J, & Kay J (2015). Longitudinal assessment of short-term memory deterioration in a logopenic variant primary progressive aphasia with post-mortem confirmed Alzheimer’s Disease pathology. Journal of Neuropsychology, 9, 184–202. doi: 10.1111/jnp
    1. Van Langenhove T, Leyton CE, Piguet O, & Hodges JR (2016). Comparing longitudinal behavior changes in the primary progressive aphasias. Journal of Alzheimer’s Disease, 18, 1033–1042. doi: 10.3233/JAD-160010.
    1. Wilson SM, Galantucci S, Tartaglia MC, Rising K, Patterson DK, Henry ML, . . . & Gorno-Tempini ML (2011). Syntactic processing depends on dorsal language tracts. Neuron, 72, 397–403. doi: 10.1016/j.neuron.2011.09.014.
    1. Woods SP, Scott JC, Sires DA, Grant I, Heaton RK, Tröster AI, & HIV Neurobehavioral Research Center (HNRC) Group. (2005). Action (verb) fluency: Test–retest reliability, normative standards, and construct validity. Journal of the International Neuropsychological Society, 11(4), 408–415.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться