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Memory Complaints with and without Memory Impairment: The Impact of Leukoaraiosis on Cognition

Published online by Cambridge University Press:  19 September 2011

Melissa Lamar*
Affiliation:
Institute of Psychiatry, King's College London, London, United Kingdom
Thomas M. Dannhauser
Affiliation:
University College London, London, United Kingdom North Essex Partnership NHS Foundation Trust, Chelmsford, United Kingdom
Zuzana Walker
Affiliation:
University College London, London, United Kingdom North Essex Partnership NHS Foundation Trust, Chelmsford, United Kingdom
Joanne E. Rodda
Affiliation:
University College London, London, United Kingdom North Essex Partnership NHS Foundation Trust, Chelmsford, United Kingdom
Darren J. Cutinha
Affiliation:
University College London, London, United Kingdom North Essex Partnership NHS Foundation Trust, Chelmsford, United Kingdom
Sukhwinder S. Shergill
Affiliation:
Institute of Psychiatry, King's College London, London, United Kingdom
*
Correspondence and reprint requests to: Melissa Lamar, Department of Psychology, Institute of Psychiatry, King's College London, Box P077 De Crespigny Park, London SE5. E-mail: [email protected]

Abstract

White matter alterations, leukoaraiosis (LA) on structural MRI, are associated with cognitive deficits and increased risk of dementia. LA may also impact on subjective memory complaints in otherwise healthy older adults. Little is known about the interplay between LA memory complaints and cognition. We investigated cognitive phenotypes associated with LA in 42 non-demented older adults categorized as having subjective cognitive complaints with no objective cognitive impairment—the subjective cognitive impairment group (SCI; n = 12), amnesic mild cognitive impairment (aMCI; n = 20), or healthy controls (HC; n = 11). We measured LA severity on MRI with a 40-point visual rating scale. Controlling for age and Mini-Mental State Examination (MMSE) score, analyses revealed multiple between-group differences. Follow-up linear regression models investigating the underlying contributors to each clinic group's cognitive profile indicated that LA contributed to learning slope variance (after accounting for age and MMSE) but only for the SCI group. Although the SCI group showed a significantly steeper learning slope when compared to HC and aMCI, increasing LA severity negatively impacted this group's rate of learning. This, in conjunction with the significant contribution of age on SCI learning slope performance variance suggests that greater LA burden at a younger age may contribute to subtle changes in learning for individuals with subjective cognitive complaints. (JINS, 2011, 17, 1104–1112)

Type
Regular Articles
Copyright
Copyright © The International Neuropsychological Society 2011

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References

Alexopoulos, G.S., Abrams, R.C., Young, R.C., Shamoian, C.A. (1988). Use of the Cornell scale in nondemented patients. Journal of the American Geriatric Society, 36(3), 230236.Google Scholar
Apostolova, L.G., Mosconi, L., Thompson, P.M., Green, A.E., Hwang, K.S., Ramirez, A., de Leon, M.J. (2010). Subregional hippocampal atrophy predicts Alzheimer's dementia in the cognitively normal. Neurobiology of Aging, 31(7), 10771088.CrossRefGoogle ScholarPubMed
Archer, H.A., Macfarlane, F., Price, S., Moore, E.K., Pepple, T., Cutler, D., Rossor, M.N. (2006). Do symptoms of memory impairment correspond to cognitive impairment: A cross sectional study of a clinical cohort. International Journal of Geriatric Psychiatry, 21(12), 12061212.CrossRefGoogle ScholarPubMed
Bombois, S., Debette, S., Delbeuck, X., Bruandet, A., Lepoittevin, S., Delmaire, C., Pasquier, F. (2007). Prevalence of subcortical vascular lesions and association with executive function in mild cognitive impairment subtypes. Stroke, 38(9), 25952597.Google Scholar
Breteler, M.M. (2000). Vascular risk factors for Alzheimer's disease: An epidemiologic perspective. Neurobiology of Aging, 21(2), 153160.Google Scholar
Burns, J.M., Church, J.A., Johnson, D.K., Xiong, C., Marcus, D., Fotenos, A.F., Buckner, R.L. (2005). White matter lesions are prevalent but differentially related with cognition in aging and early Alzheimer disease. Archives of Neurology, 62(12), 18701876.Google Scholar
Chang, Y.L., Bondi, M.W., Fennema-Notestine, C., McEvoy, L.K., Hagler, D.J. Jr., Jacobson, M.W., Dale, A.M. (2010). Brain substrates of learning and retention in mild cognitive impairment diagnosis and progression to Alzheimer's disease. Neuropsychologia, 48(5), 12371247.CrossRefGoogle ScholarPubMed
Copenhaver, B.R., Rabin, L.A., Saykin, A.J., Roth, R.M., Wishart, H.A., Flashman, L.A., Mamourian, A.C. (2006). The fornix and mammillary bodies in older adults with Alzheimer's disease, mild cognitive impairment, and cognitive complaints: A volumetric MRI study. Psychiatry Research, 147(2-3), 93103.Google Scholar
Dannhauser, T.M., Shergill, S.S., Stevens, T., Lee, L., Seal, M., Walker, R.W., Walker, Z. (2008). An fMRI study of verbal episodic memory encoding in amnestic mild cognitive impairment. Cortex, 44(7), 869880.Google Scholar
de Groot, J.C., de Leeuw, F.E., Oudkerk, M., Hofman, A., Jolles, J., Breteler, M.M. (2001). Cerebral white matter lesions and subjective cognitive dysfunction: The Rotterdam Scan Study. Neurology, 56(11), 15391545.Google Scholar
DeCarli, C., Mungas, D., Harvey, D., Reed, B., Weiner, M., Chui, H., Jagust, W. (2004). Memory impairment, but not cerebrovascular disease, predicts progression of MCI to dementia. Neurology, 63(2), 220227.Google Scholar
Delano-Wood, L., Bondi, M.W., Jak, A.J., Horne, N.R., Schweinsburg, B.C., Frank, L.R., Salmon, D.P. (2008). Stroke risk modifies regional white matter differences in mild cognitive impairment. Neurobiology of Aging, 31, 17211731.Google Scholar
Delano-Wood, L., Bondi, M.W., Sacco, J., Abeles, N., Jak, A.J., Libon, D.J., Bozoki, A. (2009). Heterogeneity in mild cognitive impairment: Differences in neuropsychological profile and associated white matter lesion pathology. Journal of the International Neuropsychological Society, 15(6), 906914.CrossRefGoogle ScholarPubMed
Dufouil, C., Fuhrer, R., Alperovitch, A. (2005). Subjective cognitive complaints and cognitive decline: Consequence or predictor? The epidemiology of vascular aging study. Journal of the American Geriatric Society, 53(4), 616621.Google Scholar
Folstein, M.R., Folstein, S.E., McHugh, P.R. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189198.Google Scholar
Geerlings, M.I., Jonker, C., Bouter, L.M., Ader, H.J., Schmand, B. (1999). Association between memory complaints and incident Alzheimer's disease in elderly people with normal baseline cognition. American Journal of Psychiatry, 156(4), 531537.Google Scholar
Hachinski, V.C., Iliff, L.D., Zilhka, E., Du Boulay, G.H., McAllister, V.L., Marshall, J., Symon, L. (1975). Cerebral blood flow in dementia. Archives of Neurology, 32(9), 632637.Google Scholar
Huppert, F.A., Brayne, C., Gill, C., Paykel, E.S., Beardsall, L. (1995). CAMCOG--A concise neuropsychological test to assist dementia diagnosis: Socio-demographic determinants in an elderly population sample. British Journal of Clinical Psychology, 34(Pt 4), 529541.CrossRefGoogle Scholar
Jak, A.J., Bangen, K.J., Wierenga, C.E., Delano-Wood, L., Corey-Bloom, J., Bondi, M.W. (2009). Contributions of neuropsychology and neuroimaging to understanding clinical subtypes of mild cognitive impairment. International Review of Neurobiology, 84, 81103.CrossRefGoogle ScholarPubMed
Jessen, F., Wiese, B., Bachmann, C., Eifflaender-Gorfer, S., Haller, F., Kolsch, H., Bickel, H. (2010). Prediction of dementia by subjective memory impairment: Effects of severity and temporal association with cognitive impairment. Archives of General Psychiatry, 67(4), 414422.Google Scholar
Jones, D.K., Catani, M., Pierpaoli, C., Reeves, S.J., Shergill, S.S., O'Sullivan, M., Howard, R.J. (2006). Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Human Brain Mapping, 27(3), 230238.CrossRefGoogle ScholarPubMed
Junque, C., Pujol, J., Vendrell, P., Bruna, O., Jodar, M., Ribas, J., Marti-Vilalta, J.L. (1990). Leuko-araiosis on magnetic resonance imaging and speed of mental processing. Archives of Neurology, 47(2), 151156.CrossRefGoogle ScholarPubMed
Lamar, M., Charlton, R.A., Morris, R.G., Markus, H.S. (2010). The impact of subcortical white matter disease on mood in euthymic older adults: A diffusion tensor imaging study. American Journal of Geriatric Psychiatry, 18(7), 634642.Google Scholar
Lamar, M., Resnick, S.M., Zonderman, A.B. (2003). Longitudinal changes in verbal memory in older adults: Distinguishing the effects of age from repeat testing. Neurology, 60(1), 8286.Google Scholar
Libon, D.J., Xie, S.X., Eppig, J., Wicas, G., Lamar, M., Lippa, C., Wambach, D.M. (2010). The heterogeneity of mild cognitive impairment: A neuropsychological analysis. Journal of the International Neuropsychological Society, 16(1), 8493.Google Scholar
Lopez, O.L., Jagust, W.J., Dulberg, C., Becker, J.T., DeKosky, S.T., Fitzpatrick, A., Kuller, L.H. (2003). Risk factors for mild cognitive impairment in the Cardiovascular Health Study Cognition Study: Part 2. Archives of Neurology, 60(10), 13941399.Google Scholar
Lyketsos, C.G., Toone, L., Tschanz, J., Rabins, P.V., Steinberg, M., Onyike, C.U., Williams, M. (2005). Population-based study of medical comorbidity in early dementia and “cognitive impairment, no dementia (CIND)”: Association with functional and cognitive impairment: The Cache County Study. American Journal of Geriatric Psychiatry, 13(8), 656664.Google 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(7), 939944.Google Scholar
Minett, T.S., Dean, J.L., Firbank, M., English, P., O'Brien, J.T. (2005). Subjective memory complaints, white-matter lesions, depressive symptoms, and cognition in elderly patients. American Journal of Geriatric Psychiatry, 13(8), 665671.Google Scholar
Miranda, B., Madureira, S., Verdelho, A., Ferro, J., Pantoni, L., Salvadori, E., Inzitarion, D. (2008). Self-perceived memory impairment and cognitive performance in an elderly independent population with age-related white matter changes. Journal of Neurology, Neurosurgery, and Psychiatry, 79(8), 869873.CrossRefGoogle Scholar
Morris, J.C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43(11), 24122414.Google Scholar
Mosconi, L., De Santi, S., Li, J., Tsui, W.H., Li, Y., Boppana, M., de Leon, M.J. (2008). Hippocampal hypometabolism predicts cognitive decline from normal aging. Neurobiology of Aging, 29(5), 676692.CrossRefGoogle ScholarPubMed
O'Sullivan, M., Jones, D.K., Summers, P.E., Morris, R.G., Williams, S.C., Markus, H.S. (2001). Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology, 57(4), 632638.Google Scholar
Oulhaj, A., Wilcock, G.K., Smith, A.D., de Jager, C.A. (2009). Predicting the time of conversion to MCI in the elderly: Role of verbal expression and learning. Neurology, 73(18), 14361442.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(12), 19851992.Google Scholar
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(3), 303308.Google Scholar
Petrovitch, H., Ross, G.W., He, Q., Uyehara-Lock, J., Markesbery, W., Davis, D., White, L.R. (2007). Characterization of Japanese-American men with a single neocortical AD lesion type. Neurobiology of Aging, 29, 14481455.CrossRefGoogle ScholarPubMed
Price, C.C., Jefferson, A.L., Merino, J.G., Heilman, K.M., Libon, D.J. (2005). Subcortical vascular dementia: Integrating neuropsychological and neuroradiologic data. Neurology, 65(3), 376382.Google Scholar
Reid, L.M., Maclullich, A.M. (2006). Subjective memory complaints and cognitive impairment in older people. Dementia and Geriatric Cognitive Disorders, 22(5-6), 471485.Google Scholar
Reitan, R.M., Wolfson, D. (1995). Category Test and Trail Making Test as measures of frontal lobe functions. The Clinical Neuropsychologist, 9, 5056.Google Scholar
Rodda, J.E., Dannhauser, T.M., Cutinha, D.J., Shergill, S.S., Walker, Z. (2009). Subjective cognitive impairment: Increased prefrontal cortex activation compared to controls during an encoding task. International Journal of Geriatric Psychiatry, 24(8), 865874.Google Scholar
Roth, M., Tym, E., Mountjoy, C.Q., Huppert, F.A., Hendrie, H., Verma, S., Goddard, R. (1986). CAMDEX. A standardised instrument for the diagnosis of mental disorder in the elderly with special reference to the early detection of dementia. British Journal of Psychiatry, 149, 698709.Google Scholar
Saykin, A.J., Wishart, H.A., Rabin, L.A., Santulli, R.B., Flashman, L.A., West, J.D., Mamourian, A.C. (2006). Older adults with cognitive complaints show brain atrophy similar to that of amnestic MCI. Neurology, 67(5), 834842.Google Scholar
Schofield, P.W., Marder, K., Dooneief, G., Jacobs, D.M., Sano, M., Stern, Y. (1997). Association of subjective memory complaints with subsequent cognitive decline in community-dwelling elderly individuals with baseline cognitive impairment. American Journal of Psychiatry, 154(5), 609615.Google Scholar
Sharpe, K., O'Carroll, R. (1991). Estimating premorbid intellectual level in dementia using the National Adult Reading Test: A Canadian study. British Journal of Clinical Psychology, 30(Pt 4), 381384.Google Scholar
Spreen, O., Benton, A.L. (1969). Neurosensory Center Comprehensive Examination for Aphasia (NCCEA). Victoria, British Columbia, Canada: University of Victoria Neuropsychology Laboratory.Google Scholar
Stewart, R., Dufouil, C., Godin, O., Ritchie, K., Maillard, P., Delcroix, N., Tzourio, C. (2008). Neuroimaging correlates of subjective memory deficits in a community population. Neurology, 70(18), 16011607.Google Scholar
van der Flier, W.M., van Buchem, M.A., Weverling-Rijnsburger, A.W., Mutsaers, E.R., Bollen, E.L., Admiraal-Behloul, F., Middelkoop, H.A. (2004). Memory complaints in patients with normal cognition are associated with smaller hippocampal volumes. Journal of Neurology, 251(6), 671675.Google Scholar
van Oijen, M., de Jong, F.J., Hofman, A., Koudstaal, P.J., Breteler, M.M. (2007). Subjective memory complaints, education, and risk of Alzheimer's disease. Alzheimers Dementia, 3(2), 9297.Google Scholar
van Straaten, E.C., Harvey, D., Scheltens, P., Barkhof, F., Petersen, R.C., Thal, L.J., DeCarli, C. (2008). Periventricular white matter hyperintensities increase the likelihood of progression from amnestic mild cognitive impairment to dementia. Journal of Neurology, 255(9), 13021308.Google Scholar
Wechsler, D., Wycherley, R.J., Benjamin, L., Callanan, M., LavenderT., J.R., C. T., J.R., C., Mockler, D. (1998). Wechsler Memory Scale-III (Third ed.). London, UK: The Psychological Corporation.Google Scholar
Yip, A.G., McKee, A.C., Green, R.C., Wells, J., Young, H., Cupples, L.A., Farrer, L.A. (2005). APOE, vascular pathology, and the AD brain. Neurology, 65(2), 259265.Google Scholar
Yoshita, M., Fletcher, E., Harvey, D., Ortega, M., Martinez, O., Mungas, D.M., DeCarli, C.S. (2006). Extent and distribution of white matter hyperintensities in normal aging, MCI, and AD. Neurology, 67(12), 21922198.CrossRefGoogle ScholarPubMed
Zigmond, A.S., Snaith, R.P. (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica, 67(6), 361370.Google Scholar