Neuropsychological deficits associated with Alzheimer's disease in the very-old: Discrepancies in raw vs. standardized scores

Journal of the International Neuropsychological Society

Volumn 9, Issue 5, 2003, Pages 783-795

  Bondi, Mark W ^a,b   Houston, Wes S ^a   Salmon, David P ^b   Corey Bloom, Jody ^b   Katzman, Robert ^b   Thal, Leon J ^a,b   Delis, Dean C ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Alzheimer's disease; Apolipoprotein E; Neuropsychology; Very old

Indexed keywords

APOLIPOPROTEIN E;

AGE; AGED; ALZHEIMER DISEASE; BRAIN FUNCTION; CONTROLLED STUDY; DATA ANALYSIS; DEPTH PERCEPTION; DISEASE ASSOCIATION; DISEASE DURATION; DISEASE SEVERITY; EDUCATION; FEMALE; FOLLOW UP; GENDER; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MEMORY; NEUROPSYCHOLOGICAL TEST; PRIORITY JOURNAL; PSYCHOPATHY; REVIEW; SCORING SYSTEM; STANDARDIZATION;

AGED; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; APOLIPOPROTEINS E; COGNITION; EDUCATION; FEMALE; FOLLOW-UP STUDIES; GENOTYPE; HUMANS; LANGUAGE; LEARNING; MALE; MEMORY; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE; REFERENCE VALUES; SEX CHARACTERISTICS;

EID: 0038381880     PISSN: 13556177     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1355617703950119     Document Type: Review

References (77)

1. Albert, M.S., Moss, M.B., Tanzi, R., & Jones, K. (2001). Preclinical prediction of AD using neuropsychological tests. Journal of the International Neuropsychological Society, 7, 631-639.
2. Bäckman, L., Jonsson Laukka, E., Wahlin, Å, Small, B.J., & Fratiglioni, L. (2002). Influences of preclinical dementia and impending death on the magnitude of age-related cognitive decline. Psychology and Aging, 17, 435-442.
3. Bäckman, L., Small, B.J., & Fratiglioni, L. (2001). Stability of the preclinical episodic memory deficit in Alzheimer's disease. Brain, 124, 96-102.
4. Basun, H., Grut, M., Winblad, B., & Lannfelt, L. (1995). Apolipoprotein ε4 allele and disease progression in patients with late-onset Alzheimer's disease. Neuroscience Letters, 183, 32-34.
5. Bondi, M.W., Monsch, A.U., Galasko, D., Butters, N., Salmon, D.P., & Delis, D.C. (1994). Preclinical cognitive markers of dementia of the Alzheimer type. Neuropsychology, 8, 374-384.
6. Bondi, M.W., Salmon, D.P., Galasko, D., Thomas, R.G., & Thal, L.J. (1999). Neuropsychological function and apolipoprotein E genotype in the preclinical detection of Alzheimer's disease. Psychology and Aging, 14, 295-303.
7. Bondi, M.W., Salmon, D.P., Monsch, A.U., Galasko, D., Butters, N., Klauber, M.R., Thal, L.J., & Saitoh, T. (1995). Episodic memory changes are associated with the ApoE-ε4 allele in nondemented older adults. Neurology, 45, 2203-2206.
8. Bondi, M.W., Serody, A.B., Chan, A.S., Eberson-Shumate, S., Delis, D.C., Hansen, L.A., & Salmon, D.P. (2002). Cognitive and neuropathologic correlates of Stroop color-word test performance in Alzheimer's disease. Neuropsychology, 16, 335-343.
9. Butters, N., Salmon, D.P., Cullum, M.C., Cairns, P., Tröster, A.I., Jacobs, D., Moss, M., & Cermak, L.S. (1988). Differentiation of amnesic and demented patients with the Wechsler Memory Scale-Revised. Clinical Neuropsychologist, 2, 133-148.
10. Chen, P., Ratcliff, G., Belle, S.H., Cauley, J.A., DeKosky, S.T., & Ganguli, M. (2001). Patterns of cognitive decline in presymptomatic Alzheimer disease: A prospective community study. Archives of General Psychiatry, 58, 853-858.
11. Collie, A. & Maruff, P. (2000). The neuropsychology of preclinical Alzheimer's disease and mild cognitive impairment. Neuroscience and Biobehavioral Reviews, 24, 365-374.
12. Corder, E.H., Lannfelt, L., Viitanen, M., Corder, L.S., Manton, K.G., Winblad, B., & Basun, H. (1996). Apolipoprotein E genotype determines survival in the oldest old (85 years or older) who have good cognition. Archives of Neurology, 53, 418-422.
13. Corder, E.H., Saunders, A.M., Risch, N.J., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Jr., Rimmler, J.B., Locke, P.A., Conneally, P.M., Schmader, K.A., Small, G.W., Roses, A.D., Haines, J.L., & Pericak-Vance, M.A. (1994). Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nature Genetics, 7, 180-183.
14. Corder, E.H., Saunders, A.M., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Rimmler, J.B., Locke, P.A., Conneally, P.M., Schmader, K.E., Tanzi, R.E., Gusella, J.F., Small, G.W., Roses, A.D., Pericak-Vance, M.A., & Haines, J.L. (1995). Apolipoprotein E, survival in Alzheimer's disease patients, and the competing risks of death and Alzheimer's disease. Neurology, 45, 1323-1328.
15. Corder, E.H., Saunders, A.M., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Small, G.W., Roses, A.D., Haines, G.L., & Perick-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, 921-923.
16. Corey-Bloom, J., Wiederholt, W.C., Edelstein, S., Salmon, D.P., Cahn, D., & Barrett-Connor, E. (1996). Cognitive and functional status of the oldest old. Journal of the American Geriatrics Society, 44, 671-674.
17. Cullum, C.M., Butters, N., Tröster, A.I., & Salmon, D.P. (1990). Normal aging and forgetting rates on the Wechsler Memory Scale-Revised. Archives of Clinical Neuropsychology, 5, 23-30.
18. Dal Forno, G., Rasmusson, X., Brandt, J., Carson, K.A., Brookmeyer, R., Troncoso, J., & Kawas, C.H. (1996). Apolipoprotein E genotype and rate of decline in probable Alzheimer's disease. Archives of Neurology, 53, 345-350.
19. DeKosky, S.T., Ferrell, R., Kamboh, M.I., & Becker, J.T. (1995). Natural history of definite AD as a function of APOE genotypes. Neurology, 45 (Suppl. 4), A373.
20. Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (1987). The California Verbal Learning Test. New York: Psychological Corporation.
21. Desgranges, B., Baron, J.C., & Eustache, F. (1998). The functional neuroanatomy of episodic memory: The role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage, 8, 198-213.
22. D'Esposito, M., Zarahn, E., Aguirre, G.K., & Rypma, B. (1999). The effect of normal aging on the coupling of neural activity to the BOLD hemodynamic response. NeuroImage, 10, 6-14.
23. Evans, D.A., Funkenstein, H., Albert, M.S., Scherr, P.A., Cook, N.R., Chown, M.J., Hebert, L.E., Hennekens, C.H., & Taylor, J.O. (1989). Prevalence of Alzheimer's disease in a community population of older persons. Journal of the American Medical Association, 262, 2551-2556.
24. Fichter, M.M., Schröppel, H., & Meller, I. (1996). Incidence of dementia in a Munich community sample of the oldest old. European Archives of Psychiatry and Clinical Neurosciences, 246, 320-328.
25. Galasko, D., Hansen, L.A., Katzman, R., Wiederholt, W., Masliah, E., Terry, R., Hill, L.R., Lessin, P., & Thal, L.J. (1994). Clinical-neuropathological correlations in Alzheimer's disease and related dementias. Archives of Neurology, 51, 888-895.
26. Gebner, R., Reischies, F.M., Kage, A., Geiselmann, B., Borchelt, M., Steinhagen-Thiessen, E., & Köttgen, E. (1997). In an epidemiological sample the apolipoprotein E4 allele is associated to dementia and loss of memory function only in the very old. Neuroscience Letters, 222, 29-32.
27. Gomez-Isla, T., West, H.L., Rebeck, G.W., Harr, S.D., Growdon, J.H., Locasio, J.J., Perls, T.T., Lipsitz, L.A., & Hyman, B.T. (1996). Clinical and pathological correlates of apolipoprotein E ε4 in Alzheimer's disease. Annals of Neurology, 39, 62-70.
28. Grady, C.L., Mcintosh, A.R., Horwitz, B., Maisog, J.M., Ungerleider, L.G., Mentis, M.J., Pietrini, P., Schapiro, M.B., & Haxby, J.V. (1995). Age-related reductions in human recognition memory due to impaired encoding. Science, 269, 218-221.
29. Green, M.S., Kaye, J.A., & Ball, M.J. (2000). The Oregon Brain Aging Study: Neuropathology accompanying healthy aging in the oldest old. Neurology, 54, 105-113.
30. Growdon, J.H., Locascio, J.J., Corkin, S., Gomez-Isla, T., & Hyman, B.T. (1996). Apolipoprotein E genotype does not influence rates of cognitive decline in Alzheimer's disease. Neurology, 47, 444-448.
31. Gunning-Dixon, F.M. & Raz, N. (2000). The cognitive correlates of white matter abnormalities in normal aging: A quantitative review. Neuropsychology, 14, 224-232.
32. Guttman, C.R., Jolesz, F.A., Kikinis, R., Killiany, R.J., Moss, M.B., Sandor, T., & Albert, M.S. (1998). White matter changes with normal aging. Neurology, 50, 972-978.
33. Heaton, R.K., Grant, I., & Mathews, C.G. (1990). Comprehensive norms for an expanded Halstead-Reitan Battery: Demographic corrections, research findings, and clinical applications. Odessa, FL: Psychological Assessment Resources, Inc.
34. Heaton, R.K., Ryan, L., Grant, I., & Matthews, C.G. (1996). Demographic influences on neuropsychological test performance. In I. Grant & K.M. Adams (Eds.), Neuropsychological assessment of neuropsychiatric disorders (2nd ed., pp. 141-163). New York: Oxford University Press.
35. Hulette, C.M., Welsh-Bohmer, K.A., Murray, M.G., Saunders, A.M., Mash, D.C., & McIntyre, L.M. (1998). Neuropathological and neuropsychological changes in "normal" aging: Evidence for preclinical Alzheimer disease in cognitively normal individuals. Journal of Neuropathology and Experimental Neurology, 57, 1168-1174.
36. Incalzi, R.A., Capparella, O., Gemma, A., Marra, C., & Carbonin, P.U. (1995). Effects of aging and of Alzheimer's Disease on verbal memory. Journal of Clinical and Experimental Neuropsychology, 17, 580-589.
37. Ivnik, R.J., Malec, J.F., Smith, G.E., Tangalos, E.G., Petersen, R.C., Kokmen, E., & Kurland, L.T. (1992). Mayo's older americans normative studies: WMS-R norms for ages 56 to 94. Clinical Neuropsychologist, 6 (suppl.), 49-82.
38. Jack, C.R., Petersen, R.C., Xu, Y.C., O'Brien, P.C., Smith, G.E., Ivnik, R.J., Boeve, B.F., Waring, S.C., Tangalos, E.G., & Kokmen, E. (1999). Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology, 52, 1397-1403.
39. Jack, C.R., Petersen, R.C., Xu, Y., O'Brien, P., Waring, S., Tangalos, E., Smith, G., Ivnik, R., Thibodeau, S., & Kokmen, E. (1998b). Hippocampal atrophy and apolipoprotein E genotype are independently associated with Alzheimer's disease. Annals of Neurology, 43, 303-310.
40. Jack, C.R., Petersen, R.C., Xu, Y.C., Waring, S.C., O'Brien, P.C., Tangalos, E.G., Smith, G.E., Ivnik, R.J., & Kokmen, E. (1997). Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology, 49, 786-794.
41. Jernigan, T.J., Archibald, S.L., Fennema-Notestine, C., Gamst, A.C., Stout, J.C., Bonner, J., & Hesselink, J.R. (2001). Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiology of Aging, 22, 581-594.
42. Kawas, C. & Katzman, R. (1999). Epidemiology of dementia and Alzheimer disease. In R.D. Terry, R. Katzman, K.L. Bick, & S.S. Sisodia (Eds.), Alzheimer disease (pp. 95-116). New York: Raven Press.
43. Kurz, A., Egensperger, R., Haupt, M., Lautenschlager, N., Romero, B., Graeber, M.B., & Muller, U. (1996). Apolipoprotein E ε4 allele, cognitive decline, and deterioration of everyday performance in Alzheimer's disease. Neurology, 47, 440-443.
44. Lange, K.L., Bondi, M.W., Salmon, D.P., Galasko, D., Delis, D.C., Thomas, R.G., & Thal, L.J. (2002). Decline in verbal memory during preclinical Alzheimer's disease: Examination of the effect of APOE genotype. Journal of the International Neuropsychological Society, 8, 943-955.
45. La Rue, A., Matsuyama, S.S., McPherson, S., Sherman, J., & Jarvik, L.F. (1992). Cognitive performance in relatives of patients with probable Alzheimer disease: An age at onset effect? Journal of Clinical and Experimental Neuropsychology, 14, 533-538.
46. Linn, R.T., Wolf, P.A., Bachman, D.L., Knoefel, J.E., Cobb, J.L., Belanger, A.J., Kaplan, E.F., & D'Agostino, R.B. (1995). The 'preclinical phase' of probable Alzheimer's disease. Archives of Neurology, 52, 485-490.
47. Malec, J.F., Ivnik, R.J., Smith, G.E., Tangalos, E.G., Petersen, R.C., Kokmen, E., & Kurland, L.T. (1992). Mayo's older americans normative studies: Utility of corrections for age and education for the WAIS-R. The Clinical Neuropsychologist, 6 (suppl.), 31-47.
48. Masliah, E., Mallory, M., Hansen, L.A., DeTeresa, R., & Terry, R.D. (1993). Quantitative synaptic alterations in the human neocortex during normal aging. Neurology, 43, 192-197.
49. Masur, D.M., Sliwinski, M., Lipton, R.B., Blau, A.D., & Crystal, H.A. (1994). Neuropsychological prediction of dementia and the absence of dementia in healthy elderly persons. Neurology, 44, 1427-1432.
50. Mattis, S. (1988). Dementia Rating Scale. Odessa, FL: Psychological Assessment Resources.
51. McDowell, I., Hill, G.B., Lindsay, J.P., & Helliwell, B. (1998, July). The Canadian study of health and aging: Incidence of dementia. Paper presented at the Sixth International Conference on Alzheimer's Disease and Related Disorders, Amsterdam, The Netherlands.
52. 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 the Department of Health and Human Services Task Force on Alzheimer's disease. Neurology, 34, 939-944.
53. Mittenberg, W., Seidenberg, M., O'Leary, D.S., & DiGiulio, D.V. (1989). Changes in cerebral functioning associated with normal aging. Journal of Clinical and Experimental Neuropsychology, 11, 918-932.
54. Normann, J., Brookes, A.J., Yates, C., & St. Clair, D. (1995). Apolipoprotein E genotype and its effect on duration and severity of early and late onset Alzheimer's disease. British Journal of Psychiatry, 167, 533-536.
55. Payami, H., Grimslid, H., Oken, B., Camicioli, R., Sexton, G., Dame, A., Howieson, D., & Kaye, J. (1997). A prospective study of cognitive health in the elderly (Oregon Brain Aging Study): Effects of family history and apolipoprotein E genotype. American Journal of Human Genetics, 60, 948-956.
56. Petersen, R.C., Smith, G., Ivnik, R.J., Tangalos, E.G., Schaid, D.J., Thibodeau, S.N., Kokmen, E., Waring, S.C., & Kurland, L.T. (1995). APOE status as a predictor of the development of Alzheimer's disease in memory-impaired individuals. Journal of the American Medical Association, 273, 1274-1278.
57. 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.
58. Pfefferbaum, A., Mathalon, D.H., Sullivan, E.V., Rawles, J.M., Zipursky, R.B., & Lim, K.O. (1994). Archives of Neurology, 51, 874-887.
59. Rebeck, G.W., Perls, T.T., West, H.L., Sodhi, P., Lipsitz, L.A., & Hyman, B.T. (1994). Reduced apolipoprotein e4 allele frequency in the oldest old Alzheimer's patients and cognitively normal individuals. Neurology, 44, 1513-1516.
60. Rocca, W.A., Cha, R.H., Waring, S.C., & Kokmen, E. (1998). Incidence of dementia and Alzheimer's disease: A reanalysis of data from Rochester, Minnesota, 1975-1984. American Journal of Epidemiology, 148, 51-62.
61. Rubin, E.H., Storandt, M., Miller, J.P., Kinscherf, D.A., Grant, E.A., Morris, J.C., & Berg, L. (1998). A prospective study of cognitive function and onset of dementia in cognitively healthy elders. Archives of Neurology, 55, 395-401.
62. Salat, D.H., Kaye, J.A., & Janowsky, J.S. (1999). Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease. Archives of Neurology, 56, 338-344.
63. Salmon, D.P. & Bondi, M.W. (1999). Neuropsychology of Alzheimer disease. In R.D. Terry, R. Katzman, K.L. Bick, & S.S. Sisodia (Eds.), Alzheimer disease (2nd ed., pp. 39-56). Philadelphia: Lippincott Williams & Wilkins.
64. Salmon, D.P. & Butters, N. (1992). Neuropsychological assessment of dementia in the elderly. In R. Katzman & J.W. Rowe (Eds.), Principles of geriatric neurology (pp. 144-163). Philadelphia: F. A. Davis.
65. Saunders, A.M., Strittmatter, W.J., Schmechel, D., St. George-Hyslop, P.H., Perick-Vance, M.A., Joo, S.H., Rosi, B.L., Gusella, J.F., Crapper-MacLachlan, D.R., Alberts, M.J., Hulette, C., Crain, B., Goldgaber, D., & Roses, A.D. (1993). Association of apolipoprotein E allele ε4 with late-onset familial and sporadic Alzheimer's disease. Neurology, 43, 1467-1472.
66. Schacter, D.L., Savage, C.R., Alpert, N.M., Rauch, S.L., & Albert, M.S. (1996). The role of hippocampus and frontal cortex in age-related memory changes: A PET study. NeuroReport, 7, 1165-1169.
67. Sliwinski, M., Lipton, R.B., Buschke, H., & Stewart, W.F. (1996). The effect of preclinical dementia on estimates of normal cognitive function in aging. Journal of Gerontology: Psychological Sciences, 51B, P217-P225.
68. Small, B.J., Basun, H., & Bäckman, L. (1998). Three-year changes in cognitive performance as a function of apolipoprotein E genotype: Evidence from very old adults without dementia. Psychology and Aging, 13, 80-87.
69. Small, B.J., Fratiglioni, L., Viitanen, M., Winblad, B., & Bäckman, L. (2000). The course of cognitive impairment in preclinical Alzheimer disease: Three- and 6-year follow-up of a population-based sample. Archives of Neurology, 57, 839-844.
70. Smith, G.E., Bohac, D.L., Waring, S.C., Kokmen, E., Tangalos, E.G., Ivnik, R.J., & Petersen, R.C. (1998). Apolipoprotein E genotype influences cognitive 'phenotype' in patients with Alzheimer's disease but not in healthy control subjects. Neurology, 50, 355-362.
71. Strittmatter, W.J., Saunders, A.M., Schemchel, D., Pericak-Vance, M., Enghild, J., Salvesen, G.S., & Roses, A.D. (1993). Apolipoprotein E: High-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proceedings of the National Academy of Sciences (USA), 90, 1977-1981.
72. Strittmatter, W.J., Weisgraber, K.H., Goedert, M., Saunders, A.M., Huang, D., Corder, E.H., Dong, L.-M., Jakes, R., Alberts, M.J., Gilbert, J.R., Han, S.-H., Hulette, C., Einstein, G., Schmechel, D.E., Pericak-Vance, M.A., & Roses, A.D. (1994). Hypothesis: Microtubule instability and paired helical filament formation in the Alzheimer disease brain are related to apolipoprotein E genotype. Experimental Neurology, 125, 163-171.
73. Terry, R.D., Masliah, E., & Hansen, L. A. (1999). The neuropathology of Alzheimer disease and the structural basis of its cognitive alterations. In R.D. Terry, R. Katzman, K.L. Bick, & S.S. Sisodia (Eds.), Alzheimer disease (2nd ed., pp. 187-206). Philadelphia: Lippincott Williams & Wilkins.
74. Thal, L.J. (1999). Clinical trials in Alzheimer disease. In R.D. Terry, R. Katzman, K.L. Bick, & S.S. Sisodia (Eds.), Alzheimer disease (2nd ed., pp. 423-440). Philadelphia: Lippincott Williams & Wilkins.
75. Tröster, A.I., Butters, N., Salmon, D.P., Cullum, C.M., Jacobs, D., Brandt, J., and White, R.F. (1993). The diagnostic utility of savings scores: differentiating Alzheimer's and Huntington's diseases with the logical memory and visual reproduction tests. Journal of Clinical and Experimental Neuropsychology, 15, 773-788.
76. U.S. Bureau of the Census. (1992). Growth of America's Very-Old population. Profiles in America's elderly, No. 2. Washington, DC: U.S. Government Printing Office.
77. Ylikoski, R., Ylikoski, A., Erkinjuntti, T., Sulkava, R., Raininko, R., Tilvis, R. (1993). White matter changes in healthy elderly persons correlate with attention and speed of mental processing. Archives of Neurology, 50, 818-824.