Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T03:13:48.593Z Has data issue: false hasContentIssue false

Aggregation of Abnormal Memory Scores and Risk of Incident Alzheimer’s Disease Dementia: A Measure of Objective Memory Impairment in Amnestic Mild Cognitive Impairment

Published online by Cambridge University Press:  10 August 2020

Nicholas I. Bradfield*
Affiliation:
St Vincent’s Hospital, Fitzroy, Victoria, Australia
Kathryn A. Ellis
Affiliation:
Academic Unit for Psychiatry of Old Age, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia
Greg Savage
Affiliation:
Department of Psychology, Macquarie University, Sydney, NSW, Australia
Paul Maruff
Affiliation:
Cogstate Pty Ltd, Melbourne, Victoria, Australia
Samantha Burnham
Affiliation:
CSIRO, Parkville, Victoria, Australia
David Darby
Affiliation:
The Florey Institute of Neurosciences and Mental Health, Parkville, Victoria, Australia
Nicola T. Lautenschlager
Affiliation:
Academic Unit for Psychiatry of Old Age, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia NorthWestern Mental Health, Melbourne Health, Parkville, Victoria, Australia
Ralph N. Martins
Affiliation:
Centre of Excellence for Alzheimer’s Disease Research and Care, School of Medical and Health Sciences, Edith Cowan University, Perth, Western Australia, Australia
Colin L. Masters
Affiliation:
Florey Institute, The University of Melbourne, Victoria, Australia
Stephanie R. Rainey-Smith
Affiliation:
Centre of Excellence for Alzheimer’s Disease Research and Care, School of Medical and Health Sciences, Edith Cowan University, Perth, Western Australia, Australia
Joanne Robertson
Affiliation:
The Florey Institute of Neurosciences and Mental Health, Parkville, Victoria, Australia
Christopher Rowe
Affiliation:
PET Centre, Austin Hospital, Heidelberg, Victoria, Australia
Michael Woodward
Affiliation:
Department of Geriatric Medicine, Repatriation Campus, Austin Hospital, Heidelberg, Victoria, Australia
David Ames
Affiliation:
Academic Unit for Psychiatry of Old Age, Department of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia The Florey Institute of Neurosciences and Mental Health, Parkville, Victoria, Australia National Ageing Research Institute, Parkville, Victoria, Australia
*
*Correspondence and reprint requests to: Nicholas I. Bradfield, St Vincent’s Hospital, Fitzroy, Victoria, Australia. Tel: +61 3 9231 2211. E-mail: [email protected]

Abstract

Objectives:

The criteria for objective memory impairment in mild cognitive impairment (MCI) are vaguely defined. Aggregating the number of abnormal memory scores (NAMS) is one way to operationalise memory impairment, which we hypothesised would predict progression to Alzheimer’s disease (AD) dementia.

Methods:

As part of the Australian Imaging, Biomarkers and Lifestyle Flagship Study of Ageing, 896 older adults who did not have dementia were administered a psychometric battery including three neuropsychological tests of memory, yielding 10 indices of memory. We calculated the number of memory scores corresponding to z ≤ −1.5 (i.e., NAMS) for each participant. Incident diagnosis of AD dementia was established by consensus of an expert panel after 3 years.

Results:

Of the 722 (80.6%) participants who were followed up, 54 (7.5%) developed AD dementia. There was a strong correlation between NAMS and probability of developing AD dementia (r = .91, p = .0003). Each abnormal memory score conferred an additional 9.8% risk of progressing to AD dementia. The area under the receiver operating characteristic curve for NAMS was 0.87 [95% confidence interval (CI) .81–.93, p < .01]. The odds ratio for NAMS was 1.67 (95% CI 1.40–2.01, p < .01) after correcting for age, sex, education, estimated intelligence quotient, subjective memory complaint, Mini-Mental State Exam (MMSE) score and apolipoprotein E ϵ4 status.

Conclusions:

Aggregation of abnormal memory scores may be a useful way of operationalising objective memory impairment, predicting incident AD dementia and providing prognostic stratification for individuals with MCI.

Type
Regular Research
Copyright
Copyright © INS. The International Neuropsychological Society, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albert, M.S., DeKosky, S.T., Dickson, D., Dubois, B., Feldman, H.H., Fox, N.C., … Petersen, R.C. (2011). The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 270279.CrossRefGoogle Scholar
Altman, D.G., & Bland, J.M. (1994). Statistics Notes: Diagnostic tests 2: predictive values. BMJ, 309(6947), 102.CrossRefGoogle Scholar
American Psychiatric Association. (1994). Diagnostic And Statistical Manual Of Mental Disorders (4th ed.). Washington, DC: American Psychiatric Association.Google Scholar
American Psychiatric Association. (2013). Diagnostic And Statistical Manual Of Mental Disorders (DSM-5®). Arlington, VA: Author.Google Scholar
Anastasi, A., & Urbina, S. (1997). Psychological Testing. In (7 ed.). New Jersey: Prentice Hall.Google Scholar
Arevalo-Rodriguez, I., Smailagic, N., Roqué i Figuls, M., Ciapponi, A., Sanchez-Perez, E., Giannakou, A., … Cullum, S. (2015). Mini-Mental State Examination (MMSE) for the detection of Alzheimer’s disease and other dementias in people with mild cognitive impairment (MCI). The Cochrane Library.Google Scholar
Bermejo-Pareja, F., Contador, I., Trincado, R., Lora, D., Sanchez-Ferro, A., Mitchell, A.J., … Benito-Leon, J. (2016). Prognostic significance of mild cognitive impairment subtypes for dementia and mortality: Data from the NEDICES cohort. Journal of Alzheimer’s Disease, 50(3), 719731. doi: 10.3233/jad-150625 CrossRefGoogle ScholarPubMed
Binder, L.M., Iverson, G.L., & Brooks, B.L. (2009). To err is human: “Abnormal” neuropsychological scores and variability are common in healthy adults. Archives of Clinical Neuropsychology, 24(1), 3146. doi: 10.1093/arclin/acn001 CrossRefGoogle Scholar
Bradfield, N.I., & Ames, D. (2020). Mild cognitive impairment: narrative review of taxonomies and systematic review of their prediction of incident Alzheimer’s disease dementia. BJPsych Bulletin, 44(2), 6774. doi: 10.1192/bjb.2019.77 CrossRefGoogle ScholarPubMed
Bradfield, N.I., Ellis, K.A., Savage, G., Maruff, P., Burnham, S., Darby, D.G., … Ames, A. (2018). Baseline amnestic severity predicts progression from amnestic mild cognitive impairment to Alzheimer disease dementia at 3 years. Alzheimer Disease and Associated Disorders, 32(3), 190196. doi: 10.1097/WAD.0000000000000252 CrossRefGoogle ScholarPubMed
Brodaty, H., Aerts, L., Crawford, J.D., Heffernan, M., Kochan, N.A., Reppermund, S., … Trollor, J.N. (2017). Operationalizing the diagnostic criteria for mild cognitive impairment: the salience of objective measures in predicting incident dementia. American Journal of Geriatric Psychiatry, 25(5), 485497.CrossRefGoogle ScholarPubMed
Brooks, B.L., Iverson, G.L., Holdnack, J.A., & Feldman, H.H. (2008). Potential for misclassification of mild cognitive impairment: a study of memory scores on the Wechsler Memory Scale-III in healthy older adults. Journal of the International Neuropsychological Society, 14(3), 463478. doi: 10.1017/s1355617708080521 CrossRefGoogle ScholarPubMed
Brooks, B.L., Iverson, G.L., & White, T. (2007). Substantial risk of “Accidental MCI” in healthy older adults: base rates of low memory scores in neuropsychological assessment. Journal of the International Neuropsychological Society, 13(3), 490500. doi: 10.1017/s1355617707070531 CrossRefGoogle ScholarPubMed
Clark, L.R., Delano-Wood, L., Libon, D.J., McDonald, C.R., Nation, D.A., Bangen, K.J., … Bondi, M.W. (2013). Are empirically-derived subtypes of mild cognitive impairment consistent with conventional subtypes? Journal of the International Neuropsychological Society, 19(6), 635645.CrossRefGoogle ScholarPubMed
Cohen, J. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement, 20(1), 3746.CrossRefGoogle Scholar
Crook, T., Bartus, R.T., Ferris, S.H., Whitehouse, P., Cohen, G.D., & Gershon, S. (1986). Age associated memory impairment: proposed diagnostic criteria and measures of clinical change—report of a national institute of mental health work group. Developmental Neuropsychology, 2(4), 261276.CrossRefGoogle Scholar
Damian, M., Hausner, L., Jekel, K., Richter, M., Froelich, L., Almkvist, O., … Visser, P.J. (2013). Single-domain amnestic mild cognitive impairment identified by cluster analysis predicts Alzheimer’s disease in the European prospective DESCRIPA study. Dementia and Geriatric Cognitive Disorders, 36(1–2), 119. doi: 10.1159/000348354 CrossRefGoogle ScholarPubMed
Defrancesco, M., Marksteiner, J., Deisenhammer, E., Kemmler, G., Djurdjevic, T., & Schocke, M. (2013). Impact of white matter lesions and cognitive deficits on conversion from mild cognitive impairment to Alzheimer’s disease. Journal of Alzheimer’s Disease, 34(3), 665672. doi: 10.3233/jad-122095 CrossRefGoogle ScholarPubMed
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. doi: 10.1017/s1355617709990257 CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J., Kaplan, E., & Ober, B.A. (2000). CVLT-II: California Verbal Learning Test: Adult Version. San Antonio, TX: Psychological Corporation.Google Scholar
Dubois, B., Feldman, H.H., Jacova, C., Cummings, J.L., DeKosky, S.T., Barberger-Gateau, P., … Galasko, D. (2010). Revising the definition of Alzheimer’s disease: a new lexicon. The Lancet Neurology, 9(11), 11181127.CrossRefGoogle ScholarPubMed
Edmonds, E.C., Delano-Wood, L., Clark, L.R., Jak, A.J., Nation, D.A., McDonald, C.R., … Salmon, D.P. (2015). Susceptibility of the conventional criteria for mild cognitive impairment to false-positive diagnostic errors. Alzheimer’s & Dementia, 11(4), 415424.CrossRefGoogle ScholarPubMed
Edmonds, E.C., McDonald, C.R., Marshall, A., Thomas, K.R., Eppig, J., Weigand, A.J., … Bondi, M.W. (2019). Early versus late MCI: improved MCI staging using a neuropsychological approach. Alzheimer’s & Dementia, 15(5), 699708.CrossRefGoogle ScholarPubMed
Ellis, K.A., Bush, A. I, Darby, D., De Fazio, D., Foster, J., Hudson, P., … Maruff, P. (2009). The Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging: methodology and baseline characteristics of 1112 individuals recruited for a longitudinal study of Alzheimer’s disease. International Psychogeriatrics, 21(04), 672687.CrossRefGoogle ScholarPubMed
Eppig, J.S., Edmonds, E.C., Campbell, L., Sanderson-Cimino, M., Delano-Wood, L., Bondi, M.W., & Initiative, A. s. D. N. (2017). Statistically derived subtypes and associations with cerebrospinal fluid and genetic biomarkers in mild cognitive impairment: a latent profile analysis. Journal of the International Neuropsychological Society, 23(7), 564576.CrossRefGoogle ScholarPubMed
Folstein, M.F., 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(3), 189198.CrossRefGoogle ScholarPubMed
Forlenza, O.V., Diniz, B.S., Nunes, P.V., Memoria, C.M., Yassuda, M.S., & Gattaz, W.F. (2009). Diagnostic transitions in mild cognitive impairment subtypes. International Psychogeriatrics, 21(6), 10881095. doi: 10.1017/s1041610209990792 CrossRefGoogle ScholarPubMed
Gladsjo, J.A., Heaton, R.K., Palmer, B.W., Taylor, M.J., & Jeste, D.V. (1999). Use of oral reading to estimate premorbid intellectual and neuropsychological functioning. Journal of the International Neuropsychological Society, 5(3), 247254.CrossRefGoogle ScholarPubMed
Graham, J.E., Rockwood, K., Beattie, B.L., Eastwood, R., Gauthier, S., Tuokko, H., & McDowell, I. (1997). Prevalence and severity of cognitive impairment with and without dementia in an elderly population. The Lancet, 349(9068), 17931796.CrossRefGoogle Scholar
Holdnack, H.A. (2001). Wechsler Test Of Adult Reading: WTAR. San Antonio: The Psychological Corporation.Google Scholar
Hooper, S.R., Burchinal, M.R., Roberts, J.E., Zeisel, S., & Neebe, E.C. (1998). Social and family risk factors for infant development at one year: An application of the cumulative risk model. Journal of Applied Developmental Psychology, 19(1), 8596.CrossRefGoogle Scholar
Hughes, C.P., Berg, L., Danziger, W.L., Coben, L.A., & Martin, R.L. (1982). A new clinical scale for the staging of dementia. British Journal of Psychiatry, 140, 566572.CrossRefGoogle ScholarPubMed
Jack, C.R. Jr, Bennett, D.A., Blennow, K., Carrillo, M.C., Dunn, B., Haeberlein, S.B., … Karlawish, J. (2018). NIA-AA research framework: toward a biological definition of Alzheimer’s disease. Alzheimer’s & Dementia, 14(4), 535562.CrossRefGoogle Scholar
Jak, A.J., Preis, S.R., Beiser, A.S., Seshadri, S., Wolf, P.A., Bondi, M.W., & Au, R. (2016). Neuropsychological criteria for mild cognitive impairment and dementia risk in the Framingham Heart Study. Journal of the International Neuropsychological Society, 22(9), 937943. doi: 10.1017/s1355617716000199 CrossRefGoogle ScholarPubMed
Julayanont, P., Brousseau, M., Chertkow, H., Phillips, N., & Nasreddine, Z.S. (2014). Montreal Cognitive Assessment Memory Index Score (MoCA-MIS) as a predictor of conversion from mild cognitive impairment to Alzheimer’s disease. Journal of the American Geriatrics Society, 62(4), 679684. doi: 10.1111/jgs.12742 CrossRefGoogle ScholarPubMed
Kral, V. (1962). Senescent forgetfulness: benign and malignant. Canadian Medical Association Journal, 86(6), 257260.Google ScholarPubMed
Lee, S.J., Ritchie, C.S., Yaffe, K., Stijacic Cenzer, I., & Barnes, D.E. (2014). A clinical index to predict progression from mild cognitive impairment to dementia due to Alzheimer’s disease. PLoS One, 9(12), e113535. doi: 10.1371/journal.pone.0113535 CrossRefGoogle ScholarPubMed
Lee, Y.M., Park, J.M., Lee, B.D., Moon, E., Chung, Y.I., & Kang, C.J. (2012). Memory impairment, in mild cognitive impairment without significant cerebrovascular disease, predicts progression to Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 33(4), 240244. doi: 10.1159/000339159 CrossRefGoogle ScholarPubMed
Levy, R. (1994). Aging-associated cognitive decline. Working Party of the International Psychogeriatric Association in collaboration with the World Health Organization. International Psychogeriatrics, 6(1), 6368.Google ScholarPubMed
Lobo, A., Launer, L., Fratiglioni, L., Andersen, K., Di Carlo, A., Breteler, M., … Martinez-Lage, J. (2000). Prevalence of dementia and major subtypes in Europe: a collaborative study of population-based cohorts. Neurology, 54(11; S5), S4S9.Google ScholarPubMed
Luchsinger, J.A., Reitz, C., Honig, L.S., Tang, M.-X., Shea, S., & Mayeux, R. (2005). Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology, 65(4), 545551.CrossRefGoogle ScholarPubMed
McKhann, G.M., 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.CrossRefGoogle ScholarPubMed
McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R. Jr, Kawas, C.H., … Mayeux, R. (2011). The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 263269.CrossRefGoogle Scholar
Meyers, J., & Meyers, K. (1995). Rey Complex Figure Test And Recognition Trial. Odessa: Psychological Assessment Resources.Google Scholar
Mistridis, P., Egli, S.C., Iverson, G.L., Berres, M., Willmes, K., Welsh-Bohmer, K.A., & Monsch, A.U. (2015). Considering the base rates of low performance in cognitively healthy older adults improves the accuracy to identify neurocognitive impairment with the Consortium to Establish a Registry for Alzheimer’s Disease-Neuropsychological Assessment Battery (CERAD-NAB). European Archives of Psychiatry and Clinical Neuroscience, 265(5), 407417. doi: 10.1007/s00406-014-0571-z CrossRefGoogle Scholar
Nordlund, A., Rolstad, S., Klang, O., Edman, A., Hansen, S., & Wallin, A. (2010). Two-year outcome of MCI subtypes and aetiologies in the Goteborg MCI study. Journal of Neurology, Neurosurgery and Psychiatry, 81(5), 541546. doi: 10.1136/jnnp.2008.171066 CrossRefGoogle ScholarPubMed
O’Connor, D.W., Blessed, G., Cooper, B., Jonker, C., Morris, J.C., Presnell, I.B., … Schaufele, M. (1996). Cross-national interrater reliability of dementia diagnosis in the elderly and factors associated with disagreement. Neurology, 47(5), 11941199.CrossRefGoogle ScholarPubMed
Oltra-Cucarella, J., Sanchez-SanSegundo, M., Lipnicki, D.M., Sachdev, P.S., Crawford, J.D., Perez-Vicente, J.A., … Ferrer-Cascales, R. (2018). Using base rate of low scores to identify progression from amnestic mild cognitive impairment to Alzheimer’s disease. Journal of the American Geriatrics Society, 66(7), 13601366. doi: 10.1111/jgs.15412 CrossRefGoogle ScholarPubMed
Palmer, B.W., Boone, K.B., Lesser, I.M., & Wohl, M.A. (1998). Base rates of “impaired” neuropsychological test performance among healthy older adults. Archives of Clinical Neuropsychology, 13(6), 503511.Google ScholarPubMed
Palmer, K., Bäckman, L., Winblad, B., & Fratiglioni, L. (2008). Mild cognitive impairment in the general population: occurrence and progression to Alzheimer disease. American Journal of Geriatric Psychiatry, 16(7), 603611.CrossRefGoogle ScholarPubMed
Parikh, R., Mathai, A., Parikh, S., Chandra Sekhar, G., & Thomas, R. (2008). Understanding and using sensitivity, specificity and predictive values. Indian Journal of Ophthalmology, 56(1), 4550. doi: 10.4103/0301-4738.37595 CrossRefGoogle ScholarPubMed
Petersen, R.C., Aisen, P., Beckett, L.A., Donohue, M., Gamst, A., Harvey, D.J., … Toga, A. (2010). Alzheimer’s disease neuroimaging initiative (ADNI): clinical characterization. Neurology, 74(3), 201209.CrossRefGoogle Scholar
Petersen, R.C., Smith, G.E., Ivnik, R.J., Tangalos, E.G., Schaid, D.J., Thibodeau, S.N., … Kurland, L.T. (1995). Apolipoprotein E status as a predictor of the development of Alzheimer’s disease in memory-impaired individuals. JAMA, 273(16), 12741278.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ravaglia, G., Forti, P., Maioli, F., Martelli, M., Servadei, L., Brunetti, N., … Mariani, E. (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(1), 5158. doi: 10.1159/000089515 CrossRefGoogle ScholarPubMed
Summers, M.J., & Saunders, N.L. (2012). Neuropsychological measures predict decline to Alzheimer’s dementia from mild cognitive impairment. Neuropsychology, 26(4), 498508. doi: 10.1037/a0028576 CrossRefGoogle ScholarPubMed
Tabert, M.H., Manly, J.J., Liu, X., Pelton, G.H., Rosenblum, S., Jacobs, M., … Devanand, D.P. (2006). Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Archives of General Psychiatry, 63(8), 916924. doi: 10.1001/archpsyc.63.8.916 CrossRefGoogle ScholarPubMed
Verhey, F.R., Jolles, J., Ponds, R.W., Rozendaal, N., Plugge, L.A., De Vet, R., … Van der Lugt, P. (1993). Diagnosing dementia: A comparison between a monodisciplinary and a multidisciplinary approach. Journal of Neuropsychiatry and Clinical Neurosciences, 5(1), 7885. doi: 10.1176/jnp.5.1.78 Google ScholarPubMed
Wechsler, D. (1945). A standardized memory scale for clinical use. The Journal of Psychology, 19(1), 8795.CrossRefGoogle Scholar
Weintraub, S., Wicklund, A.H., & Salmon, D.P. (2012). The neuropsychological profile of Alzheimer disease. Cold Spring Harbor Perspectives in Medicine, 2(4), a006171.CrossRefGoogle ScholarPubMed
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L.O., … 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(3), 240246. doi: 10.1111/j.1365-2796.2004.01380.x CrossRefGoogle Scholar
World Health Organization. (1992). The ICD-10 Classification Of Mental And Behavioural Disorders: Clinical Descriptions And Diagnostic Guidelines: Geneva: World Health Organization.Google Scholar