Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-17T05:34:57.066Z Has data issue: false hasContentIssue false

Changes in visual memory in mild cognitive impairment: a longitudinal study with CANTAB

Published online by Cambridge University Press:  07 May 2020

María Campos-Magdaleno*
Affiliation:
Department of Developmental Psychology, University of Santiago de Compostela, Galicia, Spain
David Leiva
Affiliation:
Department of Methodology of Behavioural Sciences, University of Barcelona, Catalunya, Spain
Arturo X. Pereiro
Affiliation:
Department of Developmental Psychology, University of Santiago de Compostela, Galicia, Spain
Cristina Lojo-Seoane
Affiliation:
Department of Developmental Psychology, University of Santiago de Compostela, Galicia, Spain
Sabela C. Mallo
Affiliation:
Department of Developmental Psychology, University of Santiago de Compostela, Galicia, Spain
David Facal
Affiliation:
Department of Developmental Psychology, University of Santiago de Compostela, Galicia, Spain
Onésimo Juncos-Rabadán
Affiliation:
Department of Developmental Psychology, University of Santiago de Compostela, Galicia, Spain
*
Author for correspondence: María Campos-Magdaleno, E-mail: maria.campos@usc.es

Abstract

Background

Mild cognitive impairment (MCI), as a stage in the cognitive continuum between normal ageing and dementia, is mainly characterized by memory impairment. The aims of this study were to examine CANTAB measures of temporal changes of visual memory in MCI and to evaluate the usefulness of the baseline scores for predicting changes in cognitive status.

Methods

The study included 201 participants aged over 50 years with subjective cognitive complaints. Visual memory was assessed with four CANTAB tests [paired associates learning (PAL), delayed matching to sample (DMS), pattern recognition memory (PRM) and spatial span (SSP)] administered at baseline and on two further occasions, with a follow-up interval of 18–24 months. Participants were divided into three groups according to the change in their cognitive status: participants with subjective cognitive complaints who remained stable, MCI participants who remained stable (MCI-Stable) and MCI participants whose cognitive deterioration continued (MCI-Worsened). Linear mixed models were used to model longitudinal changes, with evaluation time as a fixed variable, and multinomial regression models were used to predict changes in cognitive status.

Results

Isolated significant effects were obtained for age and group with all CANTAB tests used. Interactions between evaluation time and group were identified in the PAL and DMS tests, indicating different temporal patterns depending on the changes in cognitive status. Regression models also indicated that CANTAB scores were good predictors of changes in cognitive status.

Conclusions

Decline in visual memory measured by PAL and DMS tests can successfully distinguish different types of MCI, and considered together PAL, DMS, PRM and SSP can predict changes in cognitive status.

Type
Original Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Albert, M. S., DeKosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., & Phelps, C. H. (2011). The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association work groups on diagnostic guidelines for Alzheimer's disease. Alzheimer's and Dementia: The Journal of the Alzheimer's Association, 7(3), 270279. doi:10.1016/j.jalz.2011.03.008.CrossRefGoogle Scholar
Alescio-Lautier, B., Michel, B. F., Herrera, C., Elahmadi, A., Chambon, C., Touzet, C., & Paban, V. (2007). Visual and visuospatial short-term memory in mild cognitive impairment and Alzheimer disease: Role of attention. Neuropsychologia, 45(8), 19481960. doi:10.1016/j.neuropsychologia.2006.04.033.CrossRefGoogle ScholarPubMed
Alladi, S., Arnold, R., Mitchell, J., Nestor, P. J., & Hodges, J. R. (2006). Mild cognitive impairment: Applicability of research criteria in a memory clinic and characterization of cognitive profile. Psychological Medicine, 36(4), 507515. doi:10.1017/S0033291705006744.CrossRefGoogle Scholar
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders: DSM-5. Washington, DC: American Psychiatric Association.Google Scholar
Barbeau, E. J., Ranjeva, J. P., Didic, M., Confort-Gouny, S., Felician, O., Soulier, E., & Poncet, M. (2008). Profile of memory impairment and gray matter loss in amnestic mild cognitive impairment. Neuropsychologia, 46(4), 10091019. doi:10.1016/j.neuropsychologia.2007.11.019.CrossRefGoogle ScholarPubMed
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 148. doi:10.18637/jss.v067.i01.CrossRefGoogle Scholar
Belleville, S., Fouquet, C., Hudon, C., Zomahoun, H. T. V., & Croteau, J., & Consortium for the Early Identification of Alzheimer's disease-Quevec. (2017). Neuropsychological measures that predict progression from mild cognitive impairment to Alzheimer's type dementia in older adults: A systematic review and meta-analysis. Neuropsychology Review, 27(4), 328353. doi:10.1007/s11065-017-9361-5.CrossRefGoogle ScholarPubMed
Belleville, S., Sylvain-Roy, S., de Boysson, C., & Ménard, M. C. (2008). Characterizing the memory changes in persons with mild cognitive impairment. Progress in Brain Research, 169, 365375. doi:10.1016/S0079-6123(07)00023-4.CrossRefGoogle ScholarPubMed
Benedet, M. J., & Alejandre, M. A. (1998). TAVEC: Test de Aprendizaje Verbal de España-Complutense. Madrid: TEA ediciones.Google Scholar
Benedet, M. J., & Seisdedos, N. (1996). Evaluación Clínica de las Quejas de Memoria en la Vida Cotidiana. Madrid: Editorial Médica Panamericana.Google Scholar
Blackwell, A. D., Sahakian, B. J., Vesey, R., Semple, J. M., Robbins, T. W., & Hodges, J. R. (2004). Detecting dementia: Novel neuropsychological markers of preclinical Alzheimer's disease. Dementia and Geriatric Cognitive Disorders, 17(1-2), 4248. doi:10.1159/000074081.CrossRefGoogle ScholarPubMed
Brambati, S. M., Belleville, S., Kergoat, M. J., Chayer, C., Gauthier, S., & Joubert, S. (2009). Single- and multiple-domain amnestic mild cognitive impairment: Two sides of the same coin? Dementia and Geriatric Cognitive Disorders, 28(6), 541549. doi:10.1159/000255240.CrossRefGoogle ScholarPubMed
Cacciamani, F., Salvadori, N., Eusebi, P., Lisetti, V., Luchetti, E., Calabresi, P., & Parnetti, L. (2018). Evidence of practice effect in CANTAB spatial working memory test in a cohort of patients with mild cognitive impairment. Applied Neuropsychology: Adult, 25(3), 237248. doi:10.1080/23279095.2017.1286346.CrossRefGoogle Scholar
Campos-Magdaleno, M., Díaz-Bóveda, R., Juncos-Rabadán, O., Facal, D., & Pereiro, A. X. (2016). Learning and serial effects on verbal memory in mild cognitive impairment. Applied Neuropsychology: Adult, 23(4), 237250. doi:10.1080/23279095.2015.1053887.CrossRefGoogle ScholarPubMed
CANTAB® [Cognitive assessment software]. Cambridge Cognition. (2012). All rights reserved. www.cantab.com.Google Scholar
Chamberlain, S. R., Blackwell, A. D., Nathan, P. J., Hammond, G., Robbins, T. W., Hodges, J. R., & Sahakian, B. J. (2011). Differential cognitive deterioration in dementia: A two year longitudinal study. Journal of Alzheimer's Disease, 24(1), 125136. doi:10.3233/JAD-2010-100450.CrossRefGoogle ScholarPubMed
De Anna, F., Felician, O., Barbeau, E., Mancini, J., Didic, M., & Ceccaldi, M. (2014). Cognitive changes in mild cognitive impairment patients with impaired visual recognition memory. Neuropsychology, 28(1), 98105. doi:10.1037/neu0000032.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
De Jager, C. A., Milwain, E., & Budge, M. (2002). Early detection of isolated memory deficits in the elderly: The need for more sensitive neuropsychological tests. Psychological Medicine, 32(3), 483491. doi:10.1017/S003329170200524X.CrossRefGoogle ScholarPubMed
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. (1987). California verbal learning test. San Antonio, TX: Psychological Corporation.Google Scholar
De Rover, M., Pironti, V. A., McCabe, J. A., Acosta-Carbonero, J., Arana, F. S., Morein-Zamir, S., et al. (2011). Hippocampal dysfunction in patients with mild cognitive impairment: A functional neuroimaging study of a visuospatial paired associates learning task. Neuropsychologia, 49(7), 20602070. doi:10.1016/j.neuropsychologia.2011.03.037.CrossRefGoogle ScholarPubMed
Didic, M., Felician, O., Barbeau, E. J., Mancini, J., Latger-Florence, C., Tramoni, E., & Ceccaldi, M. (2013). Impaired visual recognition memory predicts Alzheimer's disease in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 35(5-6), 291299. doi:10.1159/000347203.CrossRefGoogle ScholarPubMed
Dubois, B., Feldman, H. H., Jacova, C., Dekosky, S. T., Barberger-Gateau, P., Cummings, J., & Scheltens, P. (2007). Research criteria for the diagnosis of Alzheimer's disease: Revising the NINCDS-ADRDA criteria. Lancet Neurology, 6(8), 734746. doi:10.1016/S1474-4422(07)70178-3.CrossRefGoogle Scholar
Economou, A., Papageorgiou, S., & Karageorgiou, C. (2006). Working-delayed memory difference detects mild cognitive impairment without being affected by age and education. Journal of Clinical and Experimental Neuropsychology, 28(4), 528535. doi:10.1080/13803390590949340.CrossRefGoogle ScholarPubMed
Facal, D., Guàrdia-Olmos, J., & Juncos-Rabadán, O. (2015). Diagnostic transitions in mild cognitive impairment by use of simple Markov models. International Journal of Geriatric Psychiatry, 30(7), 669676. doi:10.1002/gps.4197.CrossRefGoogle ScholarPubMed
Fowler, K, Saling, S., Conway, M. M., Semple, E. L., & & Louis, J. M., W. (2002). Paired associate performance in the early detection of DAT. Journal of the International Neuropsychological Society, 8(1), 5871. doi:10.1017/S1355617702811067.CrossRefGoogle ScholarPubMed
Fox, J. (2016). Applied regression analysis and generalized linear models (3rd ed.). Thousand Oaks, CA: SAGE.Google Scholar
Gagnon, L. G., & Belleville, S. (2011). Working memory in mild cognitive impairment and Alzheimer's disease: Contribution of forgetting and predictive value of complex span tasks. Neuropsychology, 25(2), 226236. doi:10.1037/a0020919.CrossRefGoogle ScholarPubMed
Griffith, R. H., Netson, K. L., Harrell, L. E., Zamrini, E. Y., Brockington, J. C., & Marson, D. C. (2006). Amnestic mild cognitive impairment: Diagnostic outcomes and clinical prediction over a two-year time period. Journal of the International Neuropsychological Society, 12(2), 166175. doi:10.1017/S1355617706060267.CrossRefGoogle Scholar
Guarch, J., Marcos, T., Salamero, M., Gastó, C., & Blesa, R. (2008). Mild cognitive impairment: A risk indicator of later dementia, or a preclinical phase of the disease? International Journal of Geriatric Psychiatry, 23(3), 257265. doi:10.1002/gps.1871.CrossRefGoogle ScholarPubMed
Han, J. W., Kim, T. H., Lee, S. B., Park, J. H., Lee, J. J., & Kim, K. W. (2012). Predictive validity and diagnostic stability of mild cognitive impairment subtypes. Alzheimer's & Dementia. 8, 553559. doi:10.1016/j.jalz.2011.08.007.CrossRefGoogle ScholarPubMed
Huppert, F., Jorm, A. F., Brayne, C., Girling, D. M., Barkely, C., Beardsall, L., & Paykel, E. S. (1996). Psychometric properties of the CAMCOG. Ageing, Neuropsychology, and Cognition, 3, 14. doi:10.1080/13825589608256624.Google Scholar
Jessen, F., Amariglio, R. E., van Boxtel, M., Breteler, M., Ceccaldi, M., & Chételat, G., … Subjective Cognitive Decline Initiative (SCD-I) Working Group. (2014). A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer's disease. Alzheimer's and Dementia, 10(6), 844852. doi:10.1016/j.jalz.2014.01.001.CrossRefGoogle ScholarPubMed
Juncos-Rabadán, O., Facal, D., Pereiro, A. X., & Lojo-Seoane, C. (2014a). Visual memory profiling with CANTAB in mild cognitive impairment (MCI) subtypes. International Journal of Geriatric Psychiatry, 29(10), 10401049. doi:10.1002/gps.4095.CrossRefGoogle Scholar
Juncos-Rabadan, O., Pereiro, A. X., Facal, D., Lojo-Seoane, C., Mallo, S. C., & Campos-Magdaleno, M. (2016). Longitudinal changes in visual memory in mild cognitive impairment versus normal aging in people with subjective cognitive complaint. Alzheimer's & Dementia, 12(7), 754P755. doi:10.1016/j.jalz.2016.06.1438.CrossRefGoogle Scholar
Juncos-Rabadán, O., Pereiro, A. X., Facal, D., Reboredo, A., & Lojo-Seoane, C. (2014b). Do the Cambridge Neuropsychological Test Automated Battery episodic memory measures discriminate amnestic mild cognitive impairment? International Journal of Geriatric Psychiatry, 29(6), 602609. doi:10.1002/gps.4042.CrossRefGoogle Scholar
Juncos-Rabadán, O., Pereiro, A. X., Facal, D., Rodríguez, N., Lojo, C., Caamaño, J. A., & Eiroa, P. (2012). Prevalence and correlates of cognitive impairment in adults with subjective cognitive complaints in primary care centres. Dementia and Geriatric Cognitive Disorders, 33(4), 226232. doi:10.1159/000338607.CrossRefGoogle ScholarPubMed
Junkkila, J., Oja, S., Laine, M., & Karrasch, M. (2012). Applicability of the CANTAB-PAL computerized memory test in identifying amnestic mild cognitive impairment and Alzheimer's disease. Dementia and Geriatric Cognitive Disorders, 34(2), 8389. doi:10.1159/000342116.CrossRefGoogle ScholarPubMed
Kessels, R. P. C., Overbeek, A., & Bouman, Z. (2015). Assessment of verbal and visuospatial working memory in mild cognitive impairment and Alzheimer's dementia. Dementia & Neuropsychologia, 9(3), 301305. doi:10.1590/1980-57642015DN93000014.CrossRefGoogle ScholarPubMed
Landau, S. M., Harvey, D., Madison, C. M., Reiman, E. M., Foster, N. I., Aisen, P. S., & Jagust, W. J. (2010). Comparing predictors of conversion and decline in mild cognitive impairment. Neurology, 75(3), 230238. doi:10.1212/WNL.0b013e3181e8e8b8.CrossRefGoogle ScholarPubMed
Lawton, M. P., & Brody, E. M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist, 9(3), 179186.10.1093/geront/9.3_Part_1.179CrossRefGoogle ScholarPubMed
Lenehan, M. E., Summers, M. J., Saunders, N. L., Summers, J. J., & Vickers, J. C. (2016). Does the Cambridge Automated Neuropsychological Test Battery (CANTAB) distinguish between cognitive domains in healthy older adults?. Assessment, 23(2), 163172. doi:10.1177/1073191115581474.CrossRefGoogle ScholarPubMed
López-Pousa, S. (2003). CAMDEX-R: prueba de exploración Cambridge revisada para la valoración de los trastornos mentales en la vejez. TEA Ediciones: Adaptación española. Madrid: TEA Ediciones.Google Scholar
Mistridis, P., Krumm, S., Monsch, A. U., Berres, M., & Taylor, K. I. (2015). The 12 years preceding mild cognitive impairment due to Alzheimer's disease: The temporal emergence of cognitive decline. Journal of Alzheimer's Disease, 48(4), 10951107. doi:10.3233/JAD-150137.CrossRefGoogle ScholarPubMed
Molinuevo, J. L., Rabin, L. A., Amariglio, R., Buckley, R., Dubois, B., & Ellis, K. A. (2017). Implementation of subjective cognitive decline criteria in research studies. Alzheimer's & Dementia, 13(3), 296311. doi:10.1016/j.jalz.2016.09.012.CrossRefGoogle ScholarPubMed
Nathan, P. J., Lim, Y. Y., Abbott, R., Galluzzi, S., Marizzoni, M., & Babiloni, C., … PharmaCog Consortium. (2017). Association between CSF biomarkers, hippocampal volume and cognitive function in patients with amnestic Mild Cognitive Impairment (MCI). Neurology of Aging, 53, 110. doi:10.1016/j.neurobiolaging.2017.01.013.CrossRefGoogle Scholar
O'Connell, H., Coen, R., Kidd, N., Warsi, M., Chin, A. V., & Lawlor, B. A. (2004). Early detection of Alzheimer's Disease (AD) using the CANTAB paired Associates Learning Test. International Journal of Geriatric Psychiatry, 19(12), 12071208. doi:10.1002/gps.1180.CrossRefGoogle ScholarPubMed
Oltra-Cucarella, J., Sánchez-Sansegundo, M., Lipnicki, D. M., Crawford, J. D., Lipton, R. B., & Katz, M. J., … Cohort Studies of Memory in an International Consortium (COSMIC). (2018). Visual memory tests enhance the identification of amnestic MCI cases at greater risk of Alzheimer's disease. International Psychogeriatrics, 25, 110. doi:10.1017/S104161021800145X.Google Scholar
Owen, A. M., Beksinska, M., Jamnes, M., Leigh, P. N., Summers, B. A., Marsden, C. D., & Robbins, T. W. (1993). Visuospatial memory deficits at different stages of Parkinson's disease. Neuropsychologia, 31(7), 627644. doi:10.1016/0028-3932(93)90135-M.CrossRefGoogle ScholarPubMed
Pereiro, A. X., Ramos-Lema, S., Juncos-Rabadán, O., Facal, D., & Lojo-Seoane, C. (2015). Normative scores of the Cambridge Cognitive Examination-Revised in healthy Spanish population. Psicothema, 27(1), 3239. doi:10.7334/psicothema2014.169.Google ScholarPubMed
Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183194. doi:10.1111/j.1365-2796.2004.01388.x.CrossRefGoogle ScholarPubMed
Petersen, R. C., Lopez, O., Armstrong, M. J., Getchius, T. S., Ganguli, M., Gloss, D., & Sager, M. (2018). Practice guideline update summary: Mild cognitive impairment: Report of the guideline development, dissemination, and implementation subcommittee of the American Academy of Neurology. Neurology, 90(3), 126135. doi:10.1212/WNL.0000000000004826.CrossRefGoogle ScholarPubMed
Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D., & R Core Team (2018). nlme: Linear and nonlinear mixed effects models [Computer Software]. Retrieved from https://CRAN.R-project.org/package=nlme.Google Scholar
Polcher, A., Frommann, I., Koppara, A., Wolfsgruber, S., Jessen, F., & Wagner, M. (2017). Face-name associative recognition deficits in subjective cognitive decline and mild cognitive impairment. Journal of Alzheimer's Disease, 56(3), 11851196. doi:10.3233/JAD-160637.CrossRefGoogle ScholarPubMed
R Core Team. (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, [Computer Software]. Retrieved from https://www.R-project.org/.Google Scholar
Reijs, B. L., Ramakers, I. H., Köhler, S., Teunissen, C. E., Koel-Simmelink, M., Nathan, P. J., & Vandenberghe, R. (2017). Memory correlates of Alzheimer's disease cerebrospinal fluid markers: A longitudinal cohort study. Journal of Alzheimer's Disease, 60(3), 11191128. doi:10.3233/JAD-160766.CrossRefGoogle ScholarPubMed
Sahakian, B. J., Morris, R. G., Evenden, J. L., Heald, A., Levy, R., Philpot, M., & Robbins, T. W. (1988). A comparative study of visuospatial memory and learning in Alzheimer-type dementia and Parkinson's disease. Brain, 111, 695718. doi:10.1093/brain/111.3.695.CrossRefGoogle ScholarPubMed
Saunders, N. L. J., & Summers, M. J. (2010). Attention and working memory deficits in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 32(4), 350357. doi:10.1080/13803390903042379.CrossRefGoogle ScholarPubMed
Saxton, J., Lopez, O. L., Ratcliff, G., Dulberg, C., Fried, L. P., Carlson, M. C., & Kuller, L. (2004). Preclinical Alzheimer disease: Neuropsychological test performance 1.5 to 8 years prior to onset. Neurology, 63(12), 23412347. doi:10.1212/01.WNL.0000147470.58328.50.CrossRefGoogle Scholar
Summers, M. J., & Saunders, N. L. J. (2012). Neuropsychological measures predict decline to Alzheimer's dementia from mild cognitive impairment. Neuropsychology, 26(4), 498508. doi:10.1037/a0028576.CrossRefGoogle ScholarPubMed
Swainson, R., Hodges, J. R., Galton, C. J., Semple, J., Michael, A., Dunn, B. D., & Sahakian, B. J. (2001). Early detection and differential diagnosis of Alzheimer's Disease and depression with neuropsychological tasks. Dementia and Geriatric Cognitive Disorders, 12(4), 265280. doi:10.1159/000051269.CrossRefGoogle ScholarPubMed
Sweeney, J. A., Kmiec, J. A., & Kupfer, D. J. (2000). Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biological Psychiatry, 48(7), 674684. doi:10.1016/S0006-3223(00)00910-0.CrossRefGoogle ScholarPubMed
Van Geldrop, B., Heringa, S. M., van den Berg, E., Olde Rikkert, M. G., Biessels, G. J., & Kessels, R. P. (2015). Working memory binding and episodic memory formation in aging, mild cognitive impairment, and Alzheimer's dementia. Journal of Clinical and Experimental Neuropsychology, 37(5), 538548. doi:10.1080/13803395.2015.1037722.CrossRefGoogle Scholar
Weisberg, S. (2014). Applied linear regression (4th ed.). Hoboken, NY: Wiley.Google Scholar
Westerberg, C., Mayes, A., Florczak, S. M., Chen, Y., Creery, J., Parrish, T., Weintraub, S., & Paller, K. A. (2013). Distinct medial temporal contributions to different forms of recognition in amnestic mild cognitive impairment and Alzheimer's disease. Neuropsychologia, 51(12), 24502461. doi:10.1016/j.neuropsychologia.2013.06.025.CrossRefGoogle ScholarPubMed
Supplementary material: File

Campos-Magdaleno et al. supplementary material

Campos-Magdaleno et al. supplementary material

Download Campos-Magdaleno et al. supplementary material(File)
File 229.6 KB