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Intelligence quotient–adjusted memory impairment is associated with abnormal single photon emission computed tomography perfusion

Published online by Cambridge University Press:  14 August 2007

DORENE M. RENTZ
Affiliation:
Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts
TERRI J. HUH
Affiliation:
Department of Psychiatry, University of California, San Francisco, California
LISA M. SARDINHA
Affiliation:
Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts
ERIN K. MORAN
Affiliation:
Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
JOHN A. BECKER
Affiliation:
Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
KIRK R. DAFFNER
Affiliation:
Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts
REISA A. SPERLING
Affiliation:
Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
KEITH A. JOHNSON
Affiliation:
Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts

Abstract

Cognitive reserve among highly intelligent older individuals makes detection of early Alzheimer's disease (AD) difficult. We tested the hypothesis that mild memory impairment determined by IQ-adjusted norms is associated with single photon emission computed tomography (SPECT) perfusion abnormality at baseline and predictive of future decline. Twenty-three subjects with a Clinical Dementia Rating (CDR) score of 0, were reclassified after scores were adjusted for IQ into two groups, 10 as having mild memory impairments for ability (IQ-MI) and 13 as memory-normal (IQ-MN). Subjects underwent cognitive and functional assessments at baseline and annual follow-up for 3 years. Perfusion SPECT was acquired at baseline. At follow-up, the IQ-MI subjects demonstrated decline in memory, visuospatial processing, and phonemic fluency, and 6 of 10 had progressed to a CDR of 0.5, while the IQ-MN subjects did not show decline. The IQ-MI group had significantly lower perfusion than the IQ-MN group in parietal/precuneus, temporal, and opercular frontal regions. In contrast, higher perfusion was observed in IQ-MI compared with IQ-MN in the left medial frontal and rostral anterior cingulate regions. IQ-adjusted memory impairment in individuals with high cognitive reserve is associated with baseline SPECT abnormality in a pattern consistent with prodromal AD and predicts subsequent cognitive and functional decline. (JINS, 2007, 13, 821–831.)

Type
Research Article
Copyright
2007 The International Neuropsychological Society

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References

REFERENCES

Albert, M.S. (2002). Memory decline: The boundary between aging and age-related disease. Annals of Neurology, 51, 282284.Google Scholar
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, 631639.Google Scholar
Alexander, G.E., Furey, M.L., Grady, C.L., Pietrini, P., Brady, D.R., Mentis, M.J., & Schapiro, M.B. (1997). Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: Implications for the cognitive reserve hypothesis. American Journal of Psychiatry, 154, 165172.Google Scholar
Andel, R., Vigen, C., Mack, W.J., Clark, L.J., & Gatz, M. (2006). The effect of education and occupational complexity on rate of cognitive decline in Alzheimer's patients. Journal of the International Neuropsychological Society, 12, 147152.Google Scholar
Andreasen, N. & Blennow, K. (2005). CSF biomarkers for mild cognitive impairment and early Alzheimer's disease. Clinical Neurology and Neurosurgery, 107, 165173.Google Scholar
Barona, A., Reynolds, C.R., & Chastain, R. (1984). A demographically based index of premorbid intelligence for the WAIS-R. Journal of Consulting and Clinical Psychology, 52, 885887.Google Scholar
Bennett, D.A., Schneider, J.A., Arvanitakis, Z., Kelly, J.F., Aggarwal, N.T., Shah, R.C., & Wilson, R.S. (2006). Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology, 66, 18371844.Google Scholar
Benton, A.L., deS Hamsher, K., Varney, N.R., & Spreen, O. (1983). Contributions to neuropsychological assessment. Oxford: Oxford University Press.
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. British Journal of Psychiatry, 114, 797811.Google Scholar
Bradley, K.M., O'Sullivan, V.T., Soper, N.D., Nagy, Z., King, E.M., Smith, A.D., & Shepstone, B.J. (2002). Cerebral perfusion SPET correlated with Braak pathological stage in Alzheimer's disease. Brain, 125, 17721781.Google Scholar
Brett, M., Anton, J.L., Valabregue, R., & Poline, J.P. (2002). Region of interest analysis using an SPM toolbox [abstract]. Neuroimage, 16, 497.Google Scholar
Bright, P., Jaldow, E., & Kopelman, M.D. (2002). The National Adult Reading Test as a measure of premorbid intelligence: A comparison with estimates derived from demographic variables. Journal of the International Neuropsychological Society, 8, 847854.Google Scholar
Busse, A., Hensel, A., Guhne, U., Angermeyer, M.C., & Riedel-Heller, S.G. (2006). Mild cognitive impairment: Long-term course of four clinical subtypes. Neurology, 67, 21762185.Google Scholar
Cabeza, R., Anderson, N.D., Locantore, J.K., & McIntosh, A.R. (2002). Aging gracefully: Compensatory brain activity in high-performing older adults. Neuroimage, 17, 13941402.Google Scholar
Caselli, R.J., Reiman, E.M., Osborne, D., Hentz, J.G., Baxter, L.C., Hernandez, J.L., & Alexander, G.G. (2004). Longitudinal changes in cognition and behavior in asymptomatic carriers of the APOE e4 allele. Neurology, 62, 19901995.Google Scholar
Chetelat, G., Desgranges, B., de la Seyette, V., Viader, F., Eustache, F., & Baron, J.C. (2003). Mild cognitive impairment: Can FDG-PET predict who is to rapidly convert to Alzheimer's disease? Neurology, 60, 13741377.Google Scholar
Collie, A., Maruff, P., Shafiq-Antonacci, R., Smith, M., Hallup, M., Schofield, P., Masters, C.L., & Currie, J. (2001). Memory decline in healthy older people: Implications for identifying mild cognitive impairment. Neurology, 56, 15331538.Google Scholar
Cooper, D.B., Lacritz, L.H., Weiner, M.F., Rosenberg, R.N., & Cullum, C.M. (2004). Category fluency in mild cognitive impairment: Reduced effect of practice in test-retest conditions. Alzheimer Disease and Associated Disorders, 18, 120122.Google Scholar
Davis, D.G., Schmitt, F.A., Wekstein, D.R., & Markesbery, W.R. (1999). Alzheimer neuropathologic alterations in aged cognitively normal subjects. Journal of Neuropathology and Experimental Neurology, 58, 376388.Google Scholar
Diaz-Asper, C.M., Schretlen, D.J., & Pearlson, G.D. (2004). How well does IQ predict neuropsychological test performance in normal adults? Journal of the International Neuropsychological Society, 10, 8290.Google Scholar
Filskov, S.B. & Leli, D.A. (1981). Assessment of the individual in neuropsychological practice. In S.B. Filskov & T.J. Boll (Eds.), Handbook of clinical neuropsychology (pp. 545576). New York, NY: John Wiley & Sons.
Friedman, R.B., Ferguson, S., Robinson, S., & Sunderland, T. (1992). Dissociation of mechanisms of reading in Alzheimer's disease. Brain and Language, 43, 400413.Google Scholar
Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.P., Frith, C.D., & Frackowiak, R.S. (1995). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2, 189210.Google Scholar
Hall, C.B., Lipton, R.B., Sliwinski, M., & Stewart, W.F. (2000). A change point model for estimating the onset of cognitive decline in preclinical Alzheimer's disease. Statistics in Medicine, 19, 15551566.Google Scholar
Hyman, B.T., Gomez-Isla, T., Briggs, M., Chung, H., Nicholas, S., Kohout, F., & Wallace, R. (1996). Apolipoprotein E and cognitive change in an elderly population. Annals of Neurology, 40, 5566.Google Scholar
Johnson, K.A. & Albert, M.S. (2000). Perfusion abnormalities in prodromal AD. Neurobiology of Aging, 21, 289292.Google Scholar
Johnson, K.A., Jones, K., Holman, B.L., Becker, J.A., Spiers, P.A., Satlin, A., & Albert, M.S. (1998). Preclinical prediction of Alzheimer's disease using SPECT. Neurology, 50, 15631571.Google Scholar
Johnson, K.A., Lopera, F., Jones, K., Becker, A., Sperling, R., Hilson, J., Londono, J., Siegert, I., Arcos, M., Moreno, S., Madrigal, L., Ossa, J., Pineda, N., Ardila, A., Roselli, M., Albert, M.S., Kosik, K.S., & Rios, A. (2001). Presenilin-1-associated abnormalities in regional cerebral perfusion. Neurology, 56, 15451551.Google Scholar
Johnson, K.A., Moran, E.K., Becker, J.A., Fischman, A.J., & Albert, M.S. (2007). SPECT perfusion differences in mild cognitive impairment. Journal of Neurology, Neurosurgery, and Psychiatry, 78, 240247.Google Scholar
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test: Assessment of aphasia and related disorders (2nd ed.) Philadelphia: Lea & Febiger.
Klunk, W.E., Engler, H., Nordberg, A., Bacskai, B.J., Wang, Y., Price, J.C., Bergstrom, M., Hyman, B.T., Langstrom, B., & Mathis, C.A. (2003). Imaging the pathology of Alzheimer's disease: Amyloid-imaging with positron emission tomography. Neuroimaging Clinics of North America, 13, 781789, ix.Google Scholar
Klunk, W.E., Engler, H., Nordberg, A., Wang, Y., Blomqvist, G., Holt, D.P., Bergstrom, M., Savitcheva, I., Huang, G.F., Estrada, S., Ausen, B., Debnath, M.L., Barletta, J., Price, J.C., Sandell, J., Lopresti, B.J., Wall, A., Koivisto, P., Antoni, G., Mathis, C.A., & Langstrom, B. (2004). Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Annals of Neurology, 55, 306319.Google Scholar
Lancaster, J.L., Woldorff, M.G., Parsons, L.M., Liotti, M., Freitas, C.S., Rainey, L., Kochunov, P.V., Nickerson, D., Mikiten, S.A., & Fox, P.T. (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping, 10, 120131.Google Scholar
Loring, D.W. & Papanicolaou, A.C. (1987). Memory assessment in neuropsychology: Theoretical considerations and practical utility. Journal of Clinical and Experimental Neuropsychology, 9, 340358.Google Scholar
Markesbery, W.R., Schmitt, F.A., Kryscio, R.J., Davis, D.G., Smith, C.D., & Wekstein, D.R. (2006). Neuropathologic substrate of mild cognitive impairment. Archives of Neurology, 63, 3846.Google Scholar
Masur, D.M., Fuld, P.A., Blau, A.D., Crystal, H., & Aronson, M.K. (1990). Predicting development of dementia in the elderly with the Selective Reminding Test. Journal of Clinical and Experimental Neuropsychology, 12, 529538.Google Scholar
Masur, D.M., Fuld, P.A., Blau, A.D., Thal, L.J., Levin, H.S., & Aronson, M.K. (1989). Distinguishing normal and demented elderly with the Selective Reminding Test. Journal of Clinical and Experimental Neuropsychology, 11, 615630.Google Scholar
Monsch, A.U., Bondi, M.W., Butters, N., Salmon, D., Katzman, R., & Thal, L.J. (1992). Comparisons of verbal fluency tasks in the detection of dementia of the Alzheimer's type. Archives of Neurology, 49, 12531258.Google Scholar
Morris, J.C. (1993). The Clinical Dementia Rating Scale (CDR): Current version and scoring rules. Neurology, 43, 24122414.Google Scholar
Morris, J.C., Storandt, M., McKeel, D.W., Rubin, E.H., Price, J.L., Grant, E.A., & Berg, L. (1996). Cerebral amyloid deposition and diffuse plaques in “normal” aging: Evidence for presymptomatic and very mild Alzheimer's disease. Neurology, 46, 707719.Google Scholar
Morris, J.C., Storandt, M., Miller, P., McKeel, D., Price, J.L., Rubin, E.H., & Berg, L. (2001). Mild cognitive impairment represents early-stage Alzheimer's disease. Archives of Neurology, 58, 397405.Google Scholar
Mortimer, J.A., Borenstein, A.R., Gosche, K.M., & Snowdon, D.A. (2005). Very early detection of Alzheimer neuropathology and the role of brain reserve in modifying its clinical expression. Journal of Geriatric Psychiatry and Neurology, 18, 218223.Google Scholar
Mungas, D., Reed, B.R., Jagust, W.J., DeCarli, C., Mack, W.J., Kramer, J.H., Weiner, M.W., Schuff, N., & Chui, H.C. (2002). Volumetric MRI predicts rate of cognitive decline related to AD and cerebrovascular disease. Neurology, 59, 867873.Google Scholar
Naugle, R.I., Cullum, C.M., & Bigler, E.D. (1990). Evaluation of intellectual and memory function among dementia patients who were intellectually superior. The Clinical Neuropsychologist, 4, 355374.Google Scholar
Nelson, H.E. & O'Connell, A. (1978). Dementia: The estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex, 14, 234244.Google Scholar
Nestor, P.J., Fryer, T.D., Ikeda, M., & Hodges, J.R. (2003). Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease). The European Journal of Neuroscience, 18, 26632667.Google Scholar
O'Carroll, R. (1995). The assessment of pre-morbid ability: A critical review. Neurocase, 1, 8389.Google Scholar
Petersen, R.C., Parisi, J.E., Dickson, D.W., Johnson, K.A., Knopman, D.S., Boeve, B.F., Jicha, G.A., Ivnik, R.J., Smith, G.E., Tangalos, E.G., Braak, H., & Kokmen, E. (2006). Neuropathologic features of amnestic mild cognitive impairment. Archives of Neurology, 63, 665672.Google Scholar
Petersen, R.C., Smith, G.E., Ivnik, R.J., Kokmen, E., & Tangelos, E.G. (1994). Memory function in very early Alzheimer's disease. Neurology, 44, 867872.Google Scholar
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangelos, E.G., & Kokmen, E. (1999). Mild cognitive impairment. Clinical characterization and outcome. Archives of Neurology, 56, 303308.Google Scholar
Price, J.L. & Morris, J.C. (1999). Tangles and plaques in nondemented aging and “preclinical” Alzheimer's disease. Annals of Neurology, 45, 358368.Google Scholar
Reiman, E.M., Caselli, R.J., Chen, K., Alexander, G.E., Bandy, D., & Frost, J. (2001). Declining brain activity in cognitively normal apolipoprotein E4 heterozygotes: A foundation for using positron emission tomography to efficiently test treatments to prevent Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America, 98, 33343339.Google Scholar
Reiman, E.M., Chen, K., Alexander, G.E., Caselli, R.J., Bandy, D., Osborne, D., Saunders, A.M., & Hardy, J. (2005). Correlations between apolipoprotein E epsilon4 gene dose and brain-imaging measurements of regional hypometabolism. Proceedings of the National Academy of Sciences of the United States of America, 102, 82998302.Google Scholar
Rentz, D.M., Huh, T.J., Faust, R.F., Budson, A.B., Scinto, L.F.M., Sperling, R.A., & Daffner, K.R. (2004). Use of IQ adjusted norms to predict progressive cognitive decline in highly intelligent elders. Neuropsychology, 18, 3849.Google Scholar
Rentz, D. & Weintraub, S. (1999). Neuropsychological detection of early probable Alzheimer's disease. In K.R. Daffner & L.F.M. Scinto (Eds.), Early diagnosis of Alzheimer's disease (pp. 169190). Totowa, NJ: Humana Press.
Richards, M. & Deary, I.J. (2005). A life course approach to cognitive reserve: A model for cognitive aging and development? Annals of Neurology, 58, 617622.Google Scholar
Rutschmann, O.T. & Matchar, D.B. (2002). Usefulness of positron emission tomography in evaluating dementia. Journal of the American Medical Association, 287, 985986.Google Scholar
Ryan, J. & Paolo, A. (1992). A screening procedure for estimating premorbid intelligence in the elderly. The Clinical Neuropsychologist, 6, 5362.Google Scholar
Satz, P. (1993). Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. Neuropsychology, 7, 273295.Google Scholar
Scarmeas, N., Zarahn, E., Anderson, K.E., Habeck, C.G., Hilton, J., Flynn, J., Marder, K.S., Bell, K.L., Sackeim, H.A., Van Heertum, R.L., Moeller, J.R., & Stern, Y. (2003). Association of life activities with cerebral blood flow in Alzheimer disease: Implications for the cognitive reserve hypothesis. Archives of Neurology, 60, 359365.Google Scholar
Schmand, B., Geerlings, M., Jonker, C., & Lindeboom, J. (1998). Reading ability as an estimator of premorbid intelligence: Does it remain stable in emergent dementia? Journal of Clinical and Experimental Neuropsychology, 20, 4251.Google Scholar
Schmand, B., Smit, J., Geerlings, M., & Lindeboom, J. (1997). The effects of intelligence and education on the development of dementia. A test of the brain reserve hypothesis. Psychological Medicine, 27, 13371344.Google Scholar
Schoonenboom, S.N., Visser, P.J., Mulder, C., Lindeboom, J., Van Elk, E.J., Van Kamp, G.J., & Scheltens, P.H. (2005). Biomarker profiles and their relation to clinical variables in mild cognitive impairment. Neurocase, 11, 813.Google Scholar
Schretlen, D.J., Buffington, A.L., Meyer, S.M., & Pearlson, G.D. (2005). The use of word-reading to estimate “premorbid” ability in cognitive domains other than intelligence. Journal of the International Neuropsychological Society, 11, 784787.Google Scholar
Small, G.W. (2002). Use of neuroimaging to detect early brain changes in people at genetic risk for Alzheimer's disease. Advanced Drug Delivery Reviews, 54, 15611566.Google Scholar
Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society, 8, 448460.Google Scholar
Stern, Y. (2006). Cognitive reserve and Alzheimer disease. Alzheimer Disease and Associated Disorders, 20, 112117.Google Scholar
Stern, Y., Albert, S., Tang, M.X., & Tsai, W.Y. (1999). Rate of memory decline in AD is related to education and occupation. Neurology, 53, 19421947.Google Scholar
Stern, Y., Alexander, G.E., Prohovnik, I., Stricks, L., Link, B., Lennon, M., & Mayeux, R. (1995). Relationship between lifetime occupation and parietal flow: Implications for a reserve against Alzheimer's disease pathology. Neurology, 45, 5560.Google Scholar
Stern, Y., Gurlad, B.J., Tatemichi, T., Tang, M.X., Wilder, D., & Mayeux, R. (1994). Influence of education and occupation on the incidence of Alzheimer's disease. Journal of the American Medical Association, 271, 10041010.Google Scholar
Stern, Y., Habeck, C., Moeller, J., Scarmeas, N., Anderson, K.E., Hilton, H.J., Flynn, J., Sackeim, H., & van Heertum, R. (2005). Brain networks associated with cognitive reserve in healthy young and old adults. Cerebral Cortex, 15, 394402.Google Scholar
Sternberg, S., Wolfson, C., & Baumgarten, M. (2001). Undetected dementia in community-dwelling older people: The Canadian Study of Health and Aging. Journal of the American Geriatrics Society, 48, 14301434.Google Scholar
Storandt, M., Grant, E.A., Miller, J.P., & Morris, J.C. (2006). Longitudinal course and neuropathologic outcomes in original vs revised MCI and in pre-MCI. Neurology, 67, 467473.Google Scholar
Storandt, M., Stone, K., & LaBarge, E. (1995). Deficits in reading performance in very mild dementia of the Alzheimer type. Neuropsychology, 9, 174176.Google Scholar
Talairach, J. & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. 3-Dimensional proportional system: An approach to cerebral imaging. Stuttgart, Germany: George Thieme Verlag.
Tombaugh, T.N. & Hubley, A.M. (1997). The 60-item Boston Naming Test: Norms for cognitively intact adults aged 25 to 88 years. Journal of Clinical and Experimental Neuropsychology, 19, 922932.Google Scholar
WAIS-III-WMS-III Technical Manual. (1997). Wechsler Adult Intelligence Scale-Third Edition. San Antonio, TX: The Psychological Corporation, Harcourt Brace and Company.
Whalley, L.J., Deary, I.J., Appleton, C.L., & Starr, J.M. (2004). Cognitive reserve and the neurobiology of cognitive aging. Ageing Research Reviews, 3, 369382.Google Scholar
Wiens, A.N., Bryan, J.E., & Crossen, J.R. (1993). Estimating WAIS-R FSIQ from National Adult Reading Test-Revised in normal subjects. The Clinical Neuropsychologist, 7, 7084.Google Scholar
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L.O., Nordberg, A., Backman, L., Albert, M., Almkvist, O., Arai, H., Basun, H., Blennow, K., de Leon, M., DeCarli, C., Erkinjuntti, T., Giacobini, E., Graff, C., Hardy, J., Jack, C., Jorm, A., Ritchie, K., van Duijn, C., Visser, P., & Petersen, R.C. (2004). Mild cognitive impairment–beyond controversies, towards a consensus: Report of the International Working Group on Mild Cognitive Impairment. Journal of Internal Medicine, 256, 240246.Google Scholar
Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M., & Leirer, V.O. (1983). Development and validation of a geriatric depression screening scale. Journal of Psychiatric Research, 17, 3749.Google Scholar