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Influence of APOE Status on Lexical–Semantic Skills in Mild Cognitive Impairment

Published online by Cambridge University Press:  17 March 2011

Roberta Biundo
Affiliation:
Clinical Neuroscience Centre, University of Hull, Hull, United Kingdom
Simona Gardini
Affiliation:
Clinical Neuroscience Centre, University of Hull, Hull, United Kingdom Department of Neuroscience, University of Parma, Parma, Italy
Paolo Caffarra
Affiliation:
Clinical Neuroscience Centre, University of Hull, Hull, United Kingdom Department of Neuroscience, University of Parma, Parma, Italy
Letizia Concari
Affiliation:
Department of Neuroscience, University of Parma, Parma, Italy
Davide Martorana
Affiliation:
Molecular Genetics Unit, Parma University-Hospital, Parma, Italy
Tauro Maria Neri
Affiliation:
Molecular Genetics Unit, Parma University-Hospital, Parma, Italy
Michael F. Shanks
Affiliation:
Clinical Neuroscience Centre, University of Hull, Hull, United Kingdom
Annalena Venneri*
Affiliation:
Clinical Neuroscience Centre, University of Hull, Hull, United Kingdom S. Camillo Hospital (I.R.C.C.S), Venice, Italy
*
Correspondence and reprint requests to: Annalena Venneri, Clinical Neuroscience Centre, University of Hull, Cottingham Road, Hull HU6 7RX, England. E-mail: a.venneri@hull.ac.uk

Abstract

This study characterized the relationship between apolipoprotein E (APOE) status and residual semantic abilities in amnestic mild cognitive impairment (MCI). APOE status (ε4 carrier/non ε4 carrier) was determined in 30 amnestic MCIs and in 22 healthy matched non ε4 carrier controls. The lexical characteristics (age of acquisition, typicality, familiarity) of words produced in a category fluency task were determined. MCIs produced fewer words than controls and these were also earlier acquired and more familiar. The words produced by MCI ε4 carriers were earlier acquired than those of non ε4 carriers. Analyses limited to the first 10 words produced by patients and controls showed similar findings and also revealed that MCI subgroups retrieved first more typical words than controls. Follow up showed higher conversion to Alzheimer's disease (AD) in MCI ε4 carriers than in non ε4 carriers. These findings show that a significant proportion of phenotype variability in performance on category fluency in people at increased AD risk is influenced by genetic factors. These findings explain why category fluency deficits, together with episodic memory deficits, are the only consistent early deficits in MCI patients who convert to AD. (JINS, 2011, 17, 423–430)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2011

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References

Alberca, R., Salas, D., Perez-Gil, J.A., Lozano, P., Gil-Neciga, E. (1999). [Verbal fluency and Alzheimer's disease]. Neurologia, 14, 344348.Google ScholarPubMed
Basso, A., Capitani, E., Laiacona, M. (1987). Raven's coloured progressive matrices and brain damage: Normative values on 305 adult normal controls. Functional Neurology, II, 189194.Google Scholar
Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J.C., Small, G.W. (2000). Patterns of brain activation in people at risk for Alzheimer's disease. New England Journal of Medicine, 343, 450456.CrossRefGoogle ScholarPubMed
Braak, H., Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathology, 82(4), 239259.CrossRefGoogle ScholarPubMed
Brun, A., Englund, B., Gustafson, L., Passant, V., Mann, D.M.A., Neary, D., Snowden, J.S. (1994). Clinical and neuropathological criteria for frontotemporal dementia. Journal of Neurology, Neurosurgery, and Psychiatry, 57, 416418.Google Scholar
Burggren, A.C., Zeineh, M.M., Ekstrom, A.D., Braskie, M.N., Thompson, P.M., Small, G.W., Bookheimer, S.Y. (2008). Reduced cortical thickness in hippocampal subregions among cognitively normal apolipoprotein E e4 carriers. Neuroimage, 41, 11771183.CrossRefGoogle ScholarPubMed
Cacabelos, R. (2003). The application of functional genomics to Alzheimer's disease. Pharmacogenomics, 4, 597621.CrossRefGoogle ScholarPubMed
Caffarra, P., Vezzadini, G., Dieci, F., Zonato, F., Venneri, A. (2002a). Rey-Osterrieth complex figure: Normative values in an Italian population sample. Neurological Sciences, 22, 443447.CrossRefGoogle Scholar
Caffarra, P., Vezzadini, G., Dieci, F., Zonato, F., Venneri, A. (2002b). Una versione abbreviata del test di Stroop. Dati normativi nella popolazione italiana. Nuova Rivista di Neurologia, 12, 111115.Google Scholar
Clark, L.J., Gatz, M., Zheng, L., Chen, Y.L., McCleary, C., Mack, W.J. (2009). Longitudinal verbal fluency in normal aging, preclinical, and prevalent Alzheimer's disease. American Journal of Alzheimer's Disease and Other Dementias, 24, 461468.CrossRefGoogle ScholarPubMed
Corder, E.H., Saunders, A.M., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Small, , Pericak-Vance, M.A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science, 261, 921923.CrossRefGoogle ScholarPubMed
De Renzi, E., Faglioni, P. (1978). Normative data and screening power of a shortened version of the Token Test. Cortex, 14, 4149.CrossRefGoogle ScholarPubMed
Ellis, A.W. (in press). The acquisition, retention and loss of vocabulary in aphasia, dementia and other neuropsychological conditions. In M. Faust (Ed.), Handbook of the neuropsychology of language (Vol. 2). Oxford: Blackwells.Google Scholar
Ellis, A.W., Burani, C., Izura, C., Bromiley, A., Venneri, A. (2006). Traces of vocabulary acquisition in the brain: Evidence from covert object naming. Neuroimage, 33, 958968.CrossRefGoogle ScholarPubMed
Forbes-McKay, K.E., Ellis, A.W., Shanks, M.F., Venneri, A. (2005). The age of acquisition of words produced in a semantic fluency task can reliably differentiate normal from pathological age related cognitive decline. Neuropsychologia, 43, 16251632.CrossRefGoogle Scholar
Forbes-McKay, K.E., Venneri, A. (2005). Detecting subtle spontaneous language decline in early Alzheimer's disease with a picture description task. Neurological Sciences, 26, 243254.CrossRefGoogle ScholarPubMed
Fox, N.C., Schott, J.M. (2004). Imaging cerebral atrophy: Normal ageing to Alzheimer's disease. Lancet, 363, 392394.CrossRefGoogle ScholarPubMed
Hernandez, A.E., Li, P. (2007). Age of acquisition: Its neural and computational mechanisms. Psychological Bulletin, 133, 638650.CrossRefGoogle ScholarPubMed
Hietanen, H.M., McGeown, W.J., Guerrini, C., Shanks, M.F., Ellis, A.W., Venneri, A. (2006). Differentiating ageing and dementia with a simple word production test. Paper presented at the Alzheimer Research Trust Network annual meeting, Leeds.Google Scholar
Hodges, J.R., Erzinclioglu, S., Patterson, K. (2006). Evolution of cognitive deficits and conversion to dementia in patients with mild cognitive impairment: A very-long-term follow-up study. Dementia and Geriatric Cognitive Disorders, 21, 380391.CrossRefGoogle ScholarPubMed
Holmes, S.J., Jane Fitch, F., Ellis, A.W. (2006). Age of acquisition affects object recognition and naming in patients with Alzheimer's disease. Journal of Clinical and Experimental Neuropsychology, 28, 10101022.CrossRefGoogle ScholarPubMed
Jack, C.R. Jr., Petersen, R.C., Xu, Y.C., O'Brien, P.C., Waring, S.C., Tangalos, E.G., Kokmen, E. (1998) Hippocampal atrophy and apolipoprotein E genotype are independently associated with Alzheimer's disease. Annals of Neurology, 43, 303310.CrossRefGoogle ScholarPubMed
Kukolja, J., Thiel, C.M., Eggermann, T., Zerres, K., Fink, G.R. (2010). Medial temporal lobe dysfunction during encoding and retrieval of episodic memory in non-demented APOE epsilon4 carriers. Neuroscience, 168, 487497.CrossRefGoogle ScholarPubMed
Lambon Ralph, M.A., Ehsana, S. (2006). Age of acquisition effects depend on the mapping between representations and the frequency of occurrence: Empirical and computational evidence. Visual Cognition, 13, 928948.CrossRefGoogle Scholar
Larochelle, S., Richard, S., Soulieres, I. (2000). What some effects might not be: The time to verify membership in “Well defined” categories. Quarterly Journal of Experimental Psychology, 53, 929961.Google Scholar
Lawton, M.P., Brody, E.M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist, 9, 179186.CrossRefGoogle ScholarPubMed
Luckhaus, C., Cohnen, M., Fluss, M.O., Janner, M., Grass-Kapanke, B., Teipel, S.J., Wittsack, H.J. (2010) The relation of regional cerebral perfusion and atrophy in mild cognitive impairment (MCI) and early Alzheimer's dementia. Psychiatry Research, 183, 4451.CrossRefGoogle ScholarPubMed
Marczinski, C.A., Kertesz, A. (2006). Category and letter fluency in semantic dementia, primary progressive aphasia, and Alzheimer's disease. Brain and Language, 97, 258265.CrossRefGoogle ScholarPubMed
McKeith, I.G., Galasko, D., Kosaka, K., Perry, E.K., Dickson, D.W., Hansen, L.A., Perry, R.H. (1996) Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): Report of the consortium on DLB international workshop. Neurology, 47, 11131124.CrossRefGoogle Scholar
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology, 34, 939944.CrossRefGoogle ScholarPubMed
Measso, G., Cavarzeran, F., Zappalà, G., Lebowitz, B.D., Crook, T.H., Pirozzolo, F.J., Grigoletto, F. (1993) The Mini-Mental State Examination: Normative study of an Italian random sample. Developmental Neuropsychology, 9, 7785.CrossRefGoogle Scholar
Morrison, C.M., Chappell, T.D., Ellis, A.W. (1997). Age of acquisition norms for a large set of object names and their relation to adult estimates and other variables. Quarterly Journal of Experimental Psychology, 50A, 528559.CrossRefGoogle Scholar
Novelli, G., Papagno, C., Capitani, E., Laiacona, M., Cappa, S.F., Vallar, G. (1986a). Tre test clinici di memoria verbale a lungo termine. Taratura su soggetti normali. Archivio di Psicologia, Neurologia e Psichiatria, 47, 278296.Google Scholar
Novelli, G., Papagno, C., Capitani, E., Laiacona, M., Cappa, S.F., Vallar, G. (1986b). Tre test clinici di produzione lessicale. Taratura su soggetti normali. Archivio di Psicologia, Neurologia e Psichiatria, 47, 477506.Google Scholar
Pericak-Vance, M.A., Grubber, J., Bailey, L.R., Hedges, D., West, S., Kemmerer, B., Haines, J.L. (2000) Genomic screen of 739 sibpairs with late onset Alzheimer disease. American Journal of Human Genetics, 67, 4848.Google Scholar
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183194.CrossRefGoogle ScholarPubMed
Petersen, R.C., Doody, R., Kurz, A., Mohs, R.C., Morris, J.C., Rabins, P.V., Winblad, B. (2001) Current concepts in mild cognitive impairment. Archives of Neurology, 58, 19851992.CrossRefGoogle ScholarPubMed
Plassman, B.L., Welsh-Bohmer, K.A., Bigler, E.D., Johnson, S.C., Anderson, C.V., Helms, M.J., Breitner, J.C. (1997) Apolipoprotein E epsilon 4 allele and hippocampal volume in twins with normal cognition. Neurology, 48, 985989.CrossRefGoogle ScholarPubMed
Reiman, E.M., Chen, K.W., Alexander, G.E., Caselli, R.J., Bandy, D., Osborne, D., Hardy, J. (2004) Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proceedings of the National Academy of Sciences of the United States of America, 101, 284289.CrossRefGoogle ScholarPubMed
Roman, G.C., Tatemichi, T.K., Erkinjuntti, T., Cummings, J.L., Masdeu, J.C., Garcia, J.H., Scheinberg, P. (1993) Vascular dementia: Diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology, 43, 250260.CrossRefGoogle ScholarPubMed
Silveri, M.C., Cappa, A., Mariotti, P., Puopolo, M. (2002). Naming in patients with Alzheimer's disease: Influence of age of acquisition and categorical effects. Journal of Clinical and Experimental Neuropsychology, 24, 755764.CrossRefGoogle ScholarPubMed
Smith, C.D., Andersen, A.H., Kryscio, R.J., Schmitt, F.A., Kindy, M.S., Blonder, L.X., Avison, M.J. (2002). Women at risk for AD show increased parietal activation during a fluency task. Neurology, 58, 11971202.CrossRefGoogle ScholarPubMed
Snowdon, D.A., Greiner, L.H., Markesbery, W.R. (2000). Linguistic ability in early life and the neuropathology of Alzheimer's disease and cerebrovascular disease. Findings from the Nun Study. Annals of the New York Academy of Sciences, 903, 3438.CrossRefGoogle ScholarPubMed
Spinnler, H., Tognoni, G. (1987). Standardizzazione e taratura italiana di test neuropsicologici. Italian Journal of Neurological Sciences, 6(Suppl. 8), 1120.Google Scholar
Venneri, A., McGeown, W.J., Biundo, R., Mion, M., Nichelli, P., Shanks, M.F. (2010). The neuroanatomical substrate of lexical semantic decline in MCI ApoE ε4 carriers and non carriers. Alzheimer Disease and Associated Disorders [Epub ahead of print].Google Scholar
Venneri, A., McGeown, W.J., Hietanen, H.M., Guerrini, C., Ellis, A.W., Shanks, M.F. (2008). The anatomical bases of semantic retrieval deficits in early Alzheimer's disease. Neuropsychologia, 46, 497510.CrossRefGoogle ScholarPubMed