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Visual memory tests enhance the identification of amnestic MCI cases at greater risk of Alzheimer’s disease

Published online by Cambridge University Press:  25 October 2018

Javier Oltra-Cucarella Open the ORCID record for Javier Oltra-Cucarella [Opens in a new window] ,
Miriam Sánchez-SanSegundo ,
Darren M. Lipnicki ,
John D. Crawford ,
Richard B. Lipton ,
Mindy J. Katz ,
Andrea R. Zammit ,
Nikolaos Scarmeas ,
Efthimios Dardiotis  and
Mary H. Kosmidis
...Show all authors
Javier Oltra-Cucarella*
Affiliation:
Department of Health Psychology, University of Alicante, Alicante, Spain Unit of Cognitive Impairments and Movement Disorders, Hospital General Universitario Santa María del Rosell, Cartagena, Spain
Miriam Sánchez-SanSegundo
Affiliation:
Department of Health Psychology, University of Alicante, Alicante, Spain
Darren M. Lipnicki
Affiliation:
Centre for Healthy Brain Ageing, School of Psychiatry, NPI, Euroa Centre, UNSW Medicine, Randwick, New South Wales, Australia
John D. Crawford
Affiliation:
Centre for Healthy Brain Ageing, School of Psychiatry, NPI, Euroa Centre, UNSW Medicine, Randwick, New South Wales, Australia
Richard B. Lipton
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, NY, USA
Mindy J. Katz
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, NY, USA
Andrea R. Zammit
Affiliation:
Department of Neurology, Albert Einstein College of Medicine, Bronx, NY, USA
Nikolaos Scarmeas
Affiliation:
Department of Neurology, Medical Center, Columbia University, New York, NY, USA Department of Medicine, 1st Neurology Clinic, Aeginition Hospital, National and Kapodistrian University of Athens, Athens, Greece
Efthimios Dardiotis
Affiliation:
Neurology Department, University Hospital of Larissa, University of Thessaly, Volos, Greece
Mary H. Kosmidis
Affiliation:
Laboratory of Cognitive Neuroscience, School of Psychology, Aristotle University of Thessaloniki, Thessaloniki, Greece
Antonio Guaita
Affiliation:
“Golgi Cenci” Foundation, Abbiategrasso, Italy
Roberta Vaccaro
Affiliation:
“Golgi Cenci” Foundation, Abbiategrasso, Italy
Ki Woong Kim
Affiliation:
Department of Psychiatry, Bundang Hospital, Seoul National University, Gyeonggi-do, Korea Department of Brain and Cognitive Science, College of Natural Sciences, Seoul National University, Seoul, Korea Department of Psychiatry, College of Medicine, Seoul National University, Seoul, Korea
Ji Won Han
Affiliation:
Department of Psychiatry, Bundang Hospital, Seoul National University, Gyeonggi-do, Korea
Nicole A. Kochan
Affiliation:
Centre for Healthy Brain Ageing, School of Psychiatry, NPI, Euroa Centre, UNSW Medicine, Randwick, New South Wales, Australia
Henry Brodaty
Affiliation:
Centre for Healthy Brain Ageing, School of Psychiatry, NPI, Euroa Centre, UNSW Medicine, Randwick, New South Wales, Australia Dementia Centre for Research Collaboration, University of New South Wales, Sydney, Australia
José A. Pérez-Vicente
Affiliation:
Unit of Cognitive Impairments and Movement Disorders, Hospital General Universitario Santa María del Rosell, Cartagena, Spain
Luis Cabello-Rodríguez
Affiliation:
Unit of Cognitive Impairments and Movement Disorders, Hospital General Universitario Santa María del Rosell, Cartagena, Spain
Perminder S. Sachdev
Affiliation:
Centre for Healthy Brain Ageing, School of Psychiatry, NPI, Euroa Centre, UNSW Medicine, Randwick, New South Wales, Australia Dementia Centre for Research Collaboration, University of New South Wales, Sydney, Australia
Rosario Ferrer-Cascales*
Affiliation:
Department of Health Psychology, University of Alicante, Alicante, Spain
Cohort Studies of Memory in an International Consortium (COSMIC)
Affiliation:
Department of Health Psychology, University of Alicante, Alicante, Spain Unit of Cognitive Impairments and Movement Disorders, Hospital General Universitario Santa María del Rosell, Cartagena, Spain Centre for Healthy Brain Ageing, School of Psychiatry, NPI, Euroa Centre, UNSW Medicine, Randwick, New South Wales, Australia Department of Neurology, Albert Einstein College of Medicine, Bronx, NY, USA Department of Neurology, Medical Center, Columbia University, New York, NY, USA Department of Medicine, 1st Neurology Clinic, Aeginition Hospital, National and Kapodistrian University of Athens, Athens, Greece Neurology Department, University Hospital of Larissa, University of Thessaly, Volos, Greece Laboratory of Cognitive Neuroscience, School of Psychology, Aristotle University of Thessaloniki, Thessaloniki, Greece “Golgi Cenci” Foundation, Abbiategrasso, Italy Department of Psychiatry, Bundang Hospital, Seoul National University, Gyeonggi-do, Korea Department of Brain and Cognitive Science, College of Natural Sciences, Seoul National University, Seoul, Korea Department of Psychiatry, College of Medicine, Seoul National University, Seoul, Korea Dementia Centre for Research Collaboration, University of New South Wales, Sydney, Australia
*
Correspondence should be addressed to: Rosario Ferrer-Cascales, Department of Health Psychology, University of Alicante, Campus de San Vicente del Raspeig s/n, San Vicente del Raspeig, Alicante 03690, Spain. Phone: +34 965 90 34 00 Ext. 9420. Email: rosario.ferrer@ua.es.
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Abstract

Objectives:

To investigate whether amnestic mild cognitive impairment (aMCI) identified with visual memory tests conveys an increased risk of Alzheimer’s disease (risk-AD) and if the risk-AD differs from that associated with aMCI based on verbal memory tests.

Participants:

4,771 participants aged 70.76 (SD = 6.74, 45.4% females) from five community-based studies, each a member of the international COSMIC consortium and from a different country, were classified as having normal cognition (NC) or one of visual, verbal, or combined (visual and verbal) aMCI using international criteria and followed for an average of 2.48 years. Hazard ratios (HR) and individual patient data (IPD) meta-analysis analyzed the risk-AD with age, sex, education, single/multiple domain aMCI, and Mini-Mental State Examination (MMSE) scores as covariates.

Results:

All aMCI groups (n = 760) had a greater risk-AD than NC (n = 4,011; HR range = 3.66 – 9.25). The risk-AD was not different between visual (n = 208, 17 converters) and verbal aMCI (n = 449, 29 converters, HR = 1.70, 95%CI: 0.88, 3.27, p = 0.111). Combined aMCI (n = 103, 12 converters, HR = 2.34, 95%CI: 1.13, 4.84, p = 0.023) had a higher risk-AD than verbal aMCI. Age and MMSE scores were related to the risk-AD. The IPD meta-analyses replicated these results, though with slightly lower HR estimates (HR range = 3.68, 7.43) for aMCI vs. NC.

Conclusions:

Although verbal aMCI was most common, a significant proportion of participants had visual-only or combined visual and verbal aMCI. Compared with verbal aMCI, the risk-AD was the same for visual aMCI and higher for combined aMCI. Our results highlight the importance of including both verbal and visual memory tests in neuropsychological assessments to more reliably identify aMCI.

Keywords

Alzheimer’s diseasememorymild cognitive impairmentprogression
Type
Original Research Article
Information
International Psychogeriatrics , Volume 31 , Issue 7: Issue Theme: Diverse Approaches to Stemming Cognitive Decline , July 2019 , pp. 997 - 1006
Copyright
© International Psychogeriatric Association 2018 

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References

Albert, M. S. et al. (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, 270–279. doi: 10.1016/j.jalz.2011.03.008.CrossRefGoogle Scholar
Artero, S., Petersen, R. C., Touchon, J. and Ritchie, K. (2006). Revised criteria for mild cognitive impairment: validation within a longitudinal population study. Dementia and Geriatric Cognitive Disorders, 22, 465–470. doi: 10.1159/000096287.CrossRefGoogle ScholarPubMed
Azuero, A. (2016). A note on the magnitude of hazard ratios: correspondence. Cancer, 122, 1298–1299. doi: 10.1002/cncr.29924.CrossRefGoogle Scholar
Beekly, D. L. et al. (2007). The National Alzheimer’s Coordinating Center (NACC) database: the uniform data set. Alzheimer Disease & Associated Disorders, 21, 249–258. doi: 10.1097/WAD.0b013e318142774e.CrossRefGoogle ScholarPubMed
Bonner-Jackson, A., Mahmoud, S., Miller, J. and Banks, S. J. (2015). Verbal and non-verbal memory and hippocampal volumes in a memory clinic population. Alzheimer’s Research & Therapy, 7, 61. doi: 10.1186/s13195-015-0147-9.CrossRefGoogle Scholar
Burke, D. L., Ensor, J. and Riley, R. D. (2017). Meta-analysis using individual participant data: one-stage and two-stage approaches, and why they may differ. Statistics in Medicine, 36, 855–875. doi: 10.1002/sim.7141.CrossRefGoogle ScholarPubMed
Crowther, M. J., Look, M. P. and Riley, R. D. (2014). Multilevel mixed effects parametric survival models using adaptive Gauss-Hermite quadrature with application to recurrent events and individual participant data meta-analysis. Statistics in Medicine, 33, 3844–3858. doi: 10.1002/sim.6191.CrossRefGoogle ScholarPubMed
Dardiotis, E., Kosmidis, M. H., Yannakoulia, M., Hadjigeorgiou, G. M. and Scarmeas, N. (2014). The Hellenic Longitudinal Investigation of Aging and Diet (HELIAD): rationale, study design, and cohort description. Neuroepidemiology, 43, 9–14. doi: 10.1159/000362723.CrossRefGoogle ScholarPubMed
Didic, M. et al. (2013). Impaired visual recognition memory predicts Alzheimer’s disease in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 35, 291–299. doi: 10.1159/000347203.CrossRefGoogle ScholarPubMed
Dierckx, E. et al. (2009). Verbal cued recall as a predictor of conversion to Alzheimer’s disease in mild cognitive impairment. International Journal of Geriatric Psychiatry, 24, 1094–1100. doi: 10.1002/gps.2228.CrossRefGoogle ScholarPubMed
Ferreira, L. K., Diniz, B. S., Forlenza, O. V., Busatto, G. F. and Zanetti, M. V. (2011). Neurostructural predictors of Alzheimer’s disease: a meta-analysis of VBM studies. Neurobiology of Aging, 32, 1733–1741. doi: 10.1016/j.neurobiolaging.2009.11.008.CrossRefGoogle ScholarPubMed
Guaita, A. et al. (2013). Brain aging and dementia during the transition from late adulthood to old age: design and methodology of the “Invece.Ab” population-based study. BMC Geriatrics, 13, 98. doi: 10.1186/1471-2318-13-98.CrossRefGoogle ScholarPubMed
Hoffman, J. M. et al. (2000). FDG PET imaging in patients with pathologically verified dementia. Journal of Nuclear Medicine, 41, 1920–1928.Google ScholarPubMed
Katz, M. J. et al. (2012). Age-specific and sex-specific prevalence and incidence of mild cognitive impairment, dementia, and Alzheimer dementia in blacks and whites: a report from the Einstein aging study. Alzheimer Disease & Associated Disorders, 26, 335–343. doi: 10.1097/WAD.0b013e31823dbcfc.CrossRefGoogle ScholarPubMed
Kawas, C. H. et al. (2003). Visual memory predicts Alzheimer’s disease more than a decade before diagnosis. Neurology, 60, 1089–1093. doi: 10.1212/01.WNL.0000055813.36504.BF.CrossRefGoogle ScholarPubMed
Kim, M. J. et al. (2011). Cortical thinning in verbal, visual, and both memory-predominant mild cognitive impairment. Alzheimer Disease & Associated Disorders, 25, 242–249. doi: 10.1097/WAD.0b013e3182076d31.CrossRefGoogle ScholarPubMed
Kim, T. H. et al. (2013). Overview of the Korean Longitudinal Study on Cognitive Aging and Dementia. Alzheimer’s & Dementia, 9, P626–P627. doi: 10.1016/j.jalz.2013.05.1268.CrossRefGoogle Scholar
Larrieu, S. et al. (2002). Incidence and outcome of mild cognitive impairment in a population-based. Neurology, 59, 1594–1599. doi: 10.1212/01.WNL.0000034176.07159.F8.CrossRefGoogle Scholar
Marcus, C., Mena, E. and Subramaniam, R. M. (2014). Brain PET in the diagnosis of Alzheimer’s disease. Clinical Nuclear Medicine, 39, e413–e426. doi: 10.1097/RLU.0000000000000547.CrossRefGoogle Scholar
McKhann, G. M., Drachman, D., Folstein, M., Katzman, R., Price, D. and 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, 939–93944. doi: 10.1212/WNL.34.7.939.CrossRefGoogle ScholarPubMed
McKhann, G. M. et al. (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, 263–269. doi: 10.1016/j.jalz.2011.03.005.CrossRefGoogle Scholar
Mistridis, P., Krumm, S., Monsch, A. U., Berres, M. and 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, 1095–1107. doi: 10.3233/JAD-150137.CrossRefGoogle ScholarPubMed
Mitchell, A. and Shiri-Feshki, M. (2009). Rate of progression of mild cognitive impairment to dementia: meta-analysis of 41 robust inception cohort studies. Acta Psychiatrica Scandinavica, 119, 252–265. doi: 10.1111/j.1600-0447.2008.01326.x.CrossRefGoogle ScholarPubMed
Moye, J. (1997). Nonverbal memory assessment with designs: construct validity and clinical utility. Neuropsychology Review, 7, 157–170. doi: 10.1023/B:NERV.0000005907.34499.43.CrossRefGoogle ScholarPubMed
Oltra-Cucarella, J. et al. (2018). Using the base rate of low scores helps to identify progression from amnestic MCI to AD. Journal of the American Geriatrics Society, 66, 1360–1366. doi: 10.1111/jgs.15412.CrossRefGoogle Scholar
Petersen, R. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194. doi: 10.1111/j.1365-2796.2004.01388.x.CrossRefGoogle ScholarPubMed
Petersen, R. et al. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992. doi: 10.1001/archneur.58.12.1985.CrossRefGoogle ScholarPubMed
Petersen, R. et al. (2010). Alzheimer’s Disease Neuroimaging Initiative (ADNI): clinical characterization. Neurology, 74, 201–209. doi: 10.1212/WNL.0b013e3181cb3e25.CrossRefGoogle Scholar
Petersen, R., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G. and Kokmen, E. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56, 303–308. doi: 10.1001/archneur.56.3.303.CrossRefGoogle ScholarPubMed
Richardson, J. T. E. (2011). Eta squared and partial eta squared as measures of effect size in educational research. Educational Research Review, 6, 135–147. doi: 10.1016/j.edurev.2010.12.001.CrossRefGoogle Scholar
Ritchie, K. et al. (2017). The midlife cognitive profiles of adults at high risk of late-onset Alzheimer’s disease: the PREVENT study. Alzheimer’s & Dementia, 13, 1089–1097. doi: 10.1016/j.jalz.2017.02.008.CrossRefGoogle ScholarPubMed
Sachdev, P. S. et al. (2010). The Sydney Memory and Ageing Study (MAS): methodology and baseline medical and neuropsychiatric characteristics of an elderly epidemiological non-demented cohort of Australians aged 70–90 years. International Psychogeriatrics, 22, 1248–1264. doi: 10.1017/S1041610210001067.CrossRefGoogle ScholarPubMed
Sachdev, P. S. et al. (2013). COSMIC (Cohort Studies of Memory in an International Consortium): an international consortium to identify risk and protective factors and biomarkers of cognitive ageing and dementia in diverse ethnic and sociocultural groups. BMC Neurology, 13. doi: 10.1186/1471-2377-13-165.CrossRefGoogle Scholar
Schmid, N. S., Taylor, K. I., Foldi, N. S., Berres, M. and Monsch, A. U. (2013). Neuropsychological signs of Alzheimer’s disease 8 years prior to diagnosis. Journal of Alzheimer’s Disease, 34, 537–546. doi: 10.3233/JAD-121234.CrossRefGoogle Scholar
Szamosi, A., Levy-Gigi, E., Kelemen, O. and Kéri, S. (2013). The hippocampus plays a role in the recognition of visual scenes presented at behaviorally relevant points in time: evidence from amnestic mild cognitive impairment (aMCI) and healthy controls. Cortex, 49, 1892–1900. doi: 10.1016/j.cortex.2012.11.001.CrossRefGoogle Scholar
Vittinghoff, E., Glidden, D. V., Shiboski, S. C. and McCulloch, C. E. (2005). Regression Methods in Biostatistics: Linear, Logistic, Survival, and Repeated Measures Models. Statistics for Biology and Health. New York: Springer.Google Scholar
Weintraub, S. et al. (2018). Version 3 of the Alzheimer Disease Centers’ neuropsychological test battery in the Uniform Data Set (UDS). Alzheimer Disease & Associated Disorders, 32, 10–17. doi: 10.1097/WAD.0000000000000223.CrossRefGoogle Scholar
Weissberger, G. H., Strong, J. V., Stefanidis, K. B., Summers, M. J., Bondi, M. W. and Stricker, N. H. (2017). Diagnostic accuracy of memory measures in Alzheimer’s dementia and mild cognitive impairment: a systematic review and meta-analysis. Neuropsychology Review, 27, 354–388. doi: 10.1007/s11065-017-9360-6.CrossRefGoogle ScholarPubMed
Winblad, B. et al. (2004). Mild cognitive impairment – beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. Journal of Internal Medicine, 256, 240–246. doi: 10.1111/j.1365-2796.2004.01380.x.CrossRefGoogle Scholar
Ye, B. S. et al. (2015). The heterogeneity and natural history of mild cognitive impairment of visual memory predominant type. Journal of Alzheimer’s Disease, 43, 143–152. doi: 10.3233/JAD-140318.CrossRefGoogle ScholarPubMed
Zammit, A. R., Ezzati, A., Zimmerman, M. E., Lipton, R. B., Lipton, M. L. and Katz, M. J. (2017a). Roles of hippocampal subfields in verbal and visual episodic memory. Behavioural Brain Research, 317, 157–162. doi: 10.1016/j.bbr.2016.09.038.CrossRefGoogle ScholarPubMed
Zammit, A. R. et al. (2017b). The association of visual memory with hippocampal volume. PLOS ONE, 12, e0187851. doi: 10.1371/journal.pone.0187851.CrossRefGoogle ScholarPubMed
Zonderman, A. B., Giambra, L. M., Arenberg, D., Resnick, S. M., Costa, P. T. and Kawas, C. H. (1995). Changes in immediate visual memory predict cognitive impairment. Archives of Clinical Neuropsychology, 10, 111–123. doi: 10.1093/arclin/10.2.111.CrossRefGoogle ScholarPubMed
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