Abstract
Aim of the present review paper was to evaluate the hypothesis (included in the proposal of new research criteria for Alzheimer’s disease; Dubois et al., Lancet Neurology, 6, 734–746, 2007) that a neuropsychological tool which provides support for the semantic encoding of memorandum at the time of study and supplies category cues at the time of retrieval (i.e. the Grober-Buschke paradigm) is more effective than traditional measures of free recall in 1) differentiating patients affected by the amnestic form of Mild Cognitive Impairment (MCI) or by mild to moderate forms of Alzheimer’s disease (AD) from healthy matches, 2) predicting the conversion of individuals with MCI to AD, and 3) differentiating AD patients from individuals affected by other forms of dementia. Results of the review are controversial regarding the superiority of the Grober-Buschke procedure in differentiating individuals affected by AD or MCI from healthy individuals. The only study that evaluated this issue directly found that the Grober-Buschke procedure was more sensitive and specific than more traditional memory tests in predicting the conversion of MCI patients to AD. Finally, two studies reported that patients affected by AD or other forms of dementia showed different performance patterns in the free and cued recall tasks of the Grober-Buschke procedure. In conclusion, although encouraging results are reported in the few studies that investigated the ability of this procedure to predict the evolution of individuals with amnestic MCI and to differentiate AD patients from patients with other forms of cortical and subcortical dementia, more experimental work is needed to confirm these positive findings.
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American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders (IV-TR), 4th ed. American Psychiatric Association (ed.) Washington, DC.
Blessed, G., Tomlinson, B. E., & Roth, M. (1968). The association between quantitative measures of dementia and of senile change in the cerebral grey matter of elderly subjects. The British Journal of Psychiatry, 114, 1797–1811.
Braak, H., & Braak, E. (1995). Staging of Alzheimer’s disease-related neurofibrillary changes. Neurobiology of Aging, 16, 271–278.
Brown, L. B., & Storandt, M. (2000). Sensitivity of category cued recall to very mild dementia of the Alzheimer type. Archives of Clinical Neuropsychology, 15, 529–534.
Buschke, H., Sliwinski, M. J., Kuslansky, G., & Lipton, R. B. (1997). Diagnosis of early dementia by the Double Memory Test: encoding specificity improves diagnostic sensitivity and specificity. Neurology, 48, 989–997.
Connor, D. J., Salmon, D. P., Sandy, T. J., Galasko, D., Hansen, L. A., & Thal, L. J. (1998). Cognitive profiles of autopsy-confirmed Lewy body variant vs pure Alzheimer disease. Archives of Neurology, 55, 994–1000.
Cummings, J. L. (2003). Toward a molecular neuropsychiatry of neurodegenerative diseases. Annals of Neurology, 54, 147–154.
Davies, R. R., Hodges, J. R., Kril, J. J., Patterson, K., Halliday, G. M., & Xuereb, J. H. (2005). The pathological basis of semantic dementia. Brain, 128, 1984–1995.
De Jager, C., Blackwell, A. D., Budge, M. M., & Sahakian, B. J. (2005). Predicting cognitive decline in healthy older adults. The American Journal of Geriatric Psychiatry, 13, 735–740.
Dubois, B., Feldman, H. H., Jacova, C., Dekosky, S. T., Barberger-Gateau, P., Cummings, J., et al. (2007). Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurology, 6, 734–746.
Erkinjuntti, T., Inzitari, D., Pantoni, L., Wallin, A., Scheltens, P., Rockwood, K., et al. (2000). Research criteria for subcortical vascular dementia in clinical trials. Journal of Neural Transmission. Supplementum, 59, 23–30.
Folstein, M. F., Folstein, S. E., & McHigh, P. R. (1975). The “mini-mental state”: a practical method for grading the cognitive state of patients for the clinicians. Journal of Psychiatric Research, 12, 189–198.
Forman, M. S., Farmer, J., Johnson, J. K., Clark, C. M., Arnold, S. E., Coslett, H. B., et al. (2006). Frontotemporal dementia: clinicopathological correlations. Annals of Neurology, 59, 952–962.
Galasko, D., Katzman, R., Salmon, D. P., & Hansen, L. (1996). Clinical and neuropathological findings in Lewy body dementias. Brain and Cognition, 31, 166–175.
Garrard, P., Lambon-Ralph, M. A., Watson, P. C., Powis, J., Patterson, K., & Hodges, J. R. (2001). Longitudinal profiles of semantic impairment for living and nonliving concepts in dementia of Alzheimer’s type. Journal of Cognitive Neuroscience, 13, 892–909.
Godefroy, O., Roussel, M., Leclerc, X., & Leys, D. (2009). Deficit of episodic memory: anatomy and related patterns in stroke patients. European Neurology, 61, 223–229.
Graham, A., Davies, R., Xuereb, J., Halliday, G., Kril, J., Creasey, H., et al. (2005). Pathologically proven frontotemporal dementia presenting with severe amnesia. Brain, 128, 597–605.
Grober, E., & Buschke, H. (1987). Genuine memory deficit in dementia. Developmental Neuropsychology, 3, 13–36.
Grober, E., Buschke, H., Crystal, H., Bang, S., & Dresner, R. (1988). Screening for dementia by memory testing. Neurology, 38, 900–903.
Grossman, M., Libon, D. J., Forman, M. S., Massimo, L., Wood, E., Moore, P., et al. (2007). Distinct antemortem profiles in patients with pathologically defined frontotemporal dementia. Archives of Neurology, 64, 1601–1609.
Hamilton, J. M., Salmon, D. P., Galasko, D., Delis, D. C., Hansen, L. A., Masliah, E., et al. (2004). A comparison of episodic memory deficits in neuropathologically-confirmed Dementia with Lewy bodies and Alzheimer’s disease. Journal of the International Neuropsychological Society, 10, 689–697.
Ivanoiu, A., Adam, S., Van der Linden, M., Salmon, E., Juillerat, A. C., Mulligan, R., et al. (2005). Memory evaluation with a new cued recall test in patients with mild cognitive impairment and Alzheimer’s disease. Journal of Neurology, 252, 47–55.
Janowsky, J. S., Shimamura, A. P., Kritchevsky, M., & Squire, L. R. (1989). Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behavioral Neuroscience, 103, 548–560.
Jicha, G. A., Parisi, J. E., Dickson, D. W., Johnson, K., Cha, R., Ivnik, R. J., et al. (2006). Neuropathologic outcome of mild cognitive impairment following progression to clinical dementia. Archives of Neurology, 63, 674–681.
Kazee, A. M., Eskin, T. A., Lapham, L. W., Gabriel, K. R., McDaniel, K. D., & Hamill, R. W. (1993). Clinico-pathological correlates in Alzheimer’s disease: assessment of clinical and pathologic diagnostic criteria. Alzheimer Disease and Associated Disorders, 7, 152–164.
Kovacs, G. G., Botond, G., & Budka, H. (2010). Protein coding of neurodegenerative dementias: the neuropathological basis of biomarker diagnostics. Acta Neuropathologica, 119, 389–408.
Kraybill, M. L., Larson, E. B., Tsuang, D. W., Teri, L., McCormick, W. C., Bowen, J. D., et al. (2005). Cognitive differences in dementia patients with autopsy-verified AD, Lewy body pathology, or both. Neurology, 64, 2069–2073.
Kurz, A., & Perneczky, R. (2010). Novel insights for the treatment of Alzheimer’s disease. Progresses in Neuropsychopharmacology and Biological Psychiatry, doi:10.1016/j.pnpbp.2010.07.018
Lezak, M. D. (2004). Neuropsychological assessment. Oxford University Press United Kingdom.
Libon, D. J., Xie, S. X., Moore, P., Farmer, J., Antani, S., McCawley, G., et al. (2007). Patterns of neuropsychological impairment in frontotemporal dementia. Neurology, 68, 369–375.
Ludolph, A. C., Kassubek, J., Landwehrmeyer, B. G., Mandelkow, E., Mandelkow, E. M., Burn, D. J., et al. (2009). Tauopathies with parkinsonism: clinical spectrum, neuropathologic basis, biological markers, and treatment options. European Journal of Neurology, 16, 297–309.
Mattis, S. (1976). Mental status examination for organic mental syndrome in the elderly patients. In Bellak, L., Karasu, T., B. (eds). Geriatric Psychiatry. (pp 77–101) Grun & Stratton.
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, 939–944.
Mitchell, A. J., & Shiri-Feshki, M. (2008). Temporal trends in the long term risk of progression of mild cognitive impairment: a pooled analysis. Journal of Neurology, Neurosurgery and Psychiatry, 79, 1386–1391.
Mitchell, J., Arnold, R., Dawson, K., Nestor, P. J., & Hodges, J. R. (2009). Outcome in subgroups of mild cognitive impairment (MCI) is highly predictable using a simple algorithm. Journal of Neurology, 256, 1500–1509.
Morris, J., C. (1993). The clinical dementia rating (CDR): current version and scoring rules. Neurology, 43, 2412-2414.
Pasquier, F., Grymonprez, L., Lebert, F., & Van der Linden, M. (2001). Memory impairment differs in frontotemporal dementia and Alzheimer’s disease. Neurocase, 7, 161–171.
Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.
Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen, E. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56, 303–308.
Petersen, R. C., Doody, R., Kurz, A., Mohs, R. C., Morris, J. C., Rabins, P. V., et al. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992.
Pillon, B., Deweer, B., Michon, A., Malapani, C., Agid, Y., & Dubois, B. (1994). Are explicit memory disorders of progressive supranuclear palsy related to damage to striatofrontal circuits? Comparison with Alzheimer’s, Parkinson’s, and Huntington’s diseases. Neurology, 44, 1264–1270.
Rademakers, R., & Rovelet-Lecrux, A. (2009). Recent insights into the molecular genetics of dementia. Trends in Neurosciences, 32, 451–461.
Rascovsky, K., Salmon, D. P., Ho, G. J., Galasko, D., Peavy, G. M., Hansen, L. A., et al. (2002). Cognitive profiles differ in autopsy-confirmed frontotemporal dementia and AD. Neurology, 58, 1801–1808.
Rascovsky, K., Salmon, D. P., Hansen, L. A., & Galasko, D. (2008). Distinct cognitive profiles and rates of decline on the Mattis Dementia Rating Scale in autopsy-confirmed frontotemporal dementia and Alzheimer’s disease. Journal of the International Neuropsychological Society, 14, 373–383.
Ravaglia, G., Forti, P., Maioli, F., Martelli, M., Servadei, L., Brunetti, N., et al. (2006). Conversion of mild cognitive impairment to dementia: predictive role of mild cognitive impairment subtypes and vascular risk factors. Dementia and Geriatric Cognitive Disorders, 21, 51–58.
Saka, E., Mihci, E., Topcuoglu, M. A., & Balkan, S. (2006). Enhanced cued recall has a high utility as a screening test in the diagnosis of Alzheimer’s disease and mild cognitive impairment in Turkish people. Archives of Clinical Neuropsychology, 21, 745–751.
Salmon, D. P., Thomas, R. G., Pay, M. M., Booth, A., Hofstetter, C. R., Thal, L. J., et al. (2002). Alzheimer’s disease can be accurately diagnosed in very mildly impaired individuals. Neurology, 59, 1022–1028.
Sarazin, M., Berr, C., De Rotrou, J., Fabrigoule, C., Pasquier, F., Legrain, S., et al. (2007). Amnestic syndrome of the medial temporal type identifies prodromal AD: a longitudinal study. Neurology, 69, 1859–1867.
Shimamura, A. P., Janowsky, J. S., & Squire, L. R. (1990). Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia, 28, 803–813.
Sonnen, J. A., Larson, E. B., Crane, P. K., Haneuse, S., Li, G., Schellenberg, G. D., et al. (2007). Pathological correlates of dementia in a longitudinal, population-based sample of aging. Annals of Neurology, 62, 406–413.
Squire, L. R., Stark, C. E., & Clark, R. E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279–306.
Tabert, M. H., Manly, J. J., Liu, X., Pelton, G. H., Rosenblum, S., Jacobs, M., et al. (2006). Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Archives of General Psychiatry, 63, 916–924.
Tounsi, H., Deweer, B., Ergis, A. M., Van der Linden, M., Pillon, B., Michon, A., et al. (1999). Sensitivity to semantic cuing: an index of episodic memory dysfunction in early Alzheimer disease. Alzheimer Disease and Associated Disorders, 13, 38–46.
Van Hoesen, G. W., & Damasio, A. R. (1987). Neural correlates of cognitive impairment in Alzheimer’s disease. In F. Plum (Ed.), The handbook of physiology, the nervous system, V (pp. 871–898). Baltimore: Williams and Wilkins.
Varma, A. R., Snowden, J. S., Lloyd, J. J., Tablot, P. R., Mann, D. N., & Neary, D. (1999). Evaluation of the NINCDS-ADRDA criteria in the differentiation of Alzheimer’s disease and frontotemporal dementia. Journal of Neurology, Neurosurgery and Psychiatry, 66, 184–188.
Visser, P. J., Verhey, F. R., Ponds, R. W., Cruts, M., Van Broeckhoven, C. L., & Jolles, J. (2000). Course of objective memory impairment in non-demented subjects attending a memory clinic and predictors of outcome. International Journal of Geriatric Psychiatry, 15, 363–372.
Vogel, A., Mortensen, E. L., Gade, A., & Waldemar, G. (2007). The category cued recall test in very mild Alzheimer’s disease: discriminative validity and correlation with semantic memory functions. European Journal of Neurology, 14, 102–108.
von Gunten, A., Bouras, C., Kövari, E., Giannakopoulos, P., & Hof, P. R. (2006). Neural substrates of cognitive and behavioral deficits in atypical Alzheimer’s disease. Brain Research Reviews, 51(2), 176–211.
Wahlund, L. O., Pihlstrand, E., & Jonhagen, M. E. (2003). Mild cognitive impairment: experience from a memory clinic. Acta Neurologica Scandinavica. Supplementum, 179, 21–24.
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All authors report no conflicts of interest. They have full control of all primary data and they agree to allow the journal to review the data if requested.
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Carlesimo, G.A., Perri, R. & Caltagirone, C. Category Cued Recall Following Controlled Encoding as a Neuropsychological Tool in the Diagnosis of Alzheimer’s Disease: A Review of the Evidence. Neuropsychol Rev 21, 54–65 (2011). https://doi.org/10.1007/s11065-010-9153-7
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DOI: https://doi.org/10.1007/s11065-010-9153-7