Sensitivity of memory subtests and learning slopes from the ADAS-Cog to distinguish along the continuum of the NIA-AA Research Framework for Alzheimer’s Disease

References

• ADNI1. (2004). Alzheimer’s Disease Neuroimaging Initiative: ADNI Procedures Manual. http://adni.loni.usc.edu/wp-content/uploads/2010/09/ADNI_GeneralProceduresManual.pdf
   Google Scholar
• ADNI2. (2011). Alzheimer’s Disease Neuroimaging Initiative: ADNI2 Procedures Manual. https://adni.loni.usc.edu/wp-content/uploads/2008/07/adni2-procedures-manual.pdf
   Google Scholar
• ADNI3. (2016). Alzheimer’s Disease Neuroimaging Initiative: ADNI3 Procedures Manual. Retrieved July 2021 https://adni.loni.usc.edu/wp-content/uploads/2012/10/ADNI3-Procedures-Manual_v3.0_20170627.pdf
   Google Scholar
• ADNIGO. (2009). Alzheimer’s Disease Neuroimaging Initiative: ADNI Grand Opportunities Procedures Manual. http://adni.loni.usc.edu/wp-content/uploads/2008/07/ADNI_GO_Procedures_Manual_06102011.pdf
   Google Scholar
• Avgerinos, K. I., Ferrucci, L., & Kapogiannis, D. (2021). Effects of monoclonal antibodies against amyloid-β on clinical and biomarker outcomes and adverse event risks: A systematic review and meta-analysis of phase III RCTs in Alzheimer’s disease. Ageing Res Rev, 68(1), 101339. https://doi.org/10.1016/j.arr.2021.101339
   PubMedGoogle Scholar
• Bender, A. R., Brandmaier, A. M., Duzel, S., Keresztes, A., Pasternak, O., Lindenberger, U., & Kuhn, S. (2020). Hippocampal Subfields and Limbic White Matter Jointly Predict Learning Rate in Older Adults. Cereb Cortex, 30(4), 2465–2477. https://doi.org/10.1093/cercor/bhz252
   PubMed Web of Science ®Google Scholar
• Benge, J. F., Balsis, S., Geraci, L., Massman, P. J., & Doody, R. S. (2009). How well do the ADAS-cog and its subscales measure cognitive dysfunction in Alzheimer’s disease? Dement Geriatr Cogn Disord, 28(1), 63–69. https://doi.org/10.1159/000230709
   PubMed Web of Science ®Google Scholar
• Birks, J. (2006). Cholinesterase inhibitors for Alzheimer’s disease. Cochrane Database Syst Rev(1), 2006(1) , CD005593. https://doi.org/10.1002/14651858.Cd005593. Published 2006 Jan 25.
   PubMedGoogle Scholar
• Brandt, J., & Benedict, R. (1997). Hopkins Verbal Learning Test-Revised. Psychological Assessment Resources, Inc.
   Google Scholar
• Ciampa, C. J., Parent, J. H., Harrison, T. M., Fain, R. M., Betts, M. J., Maass, A., Winer, J. R., Baker, S. L., Janabi, M., Furman, D. J., D’Esposito, M., Jagust, W. J., & Berry, A. S. (2022). Associations among locus coeruleus catecholamines, tau pathology, and memory in aging. Neuropsychopharmacology, 47(5), 1106–1113. https://doi.org/10.1038/s41386-022-01269-6
   PubMed Web of Science ®Google Scholar
• Devous, M. D.,sSr., Fleisher, A. S., Pontecorvo, M. J., Lu, M., Siderowf, A., Navitsky, M., Kennedy, I., Southekal, S., Harris, T. S., & Mintun, M. A. (2021). Relationships Between Cognition and Neuropathological Tau in Alzheimer’s Disease Assessed by 18F Flortaucipir PET. J Alzheimers Dis, 80(3), 1091–1104. https://doi.org/10.3233/JAD-200808
   PubMed Web of Science ®Google Scholar
• Farrell, M. E., Papp, K. V., Buckley, R. F., Jacobs, H. I. L., Schultz, A. P., Properzi, M. J., Vannini, P., Hanseeuw, B. J., Rentz, D. M., Johnson, K. A., & Sperling, R. A. (2022). Association of Emerging β-Amyloid and Tau Pathology With Early Cognitive Changes in Clinically Normal Older Adults. Neurology, 98(15), e1512–e1524. https://doi.org/10.1212/wnl.0000000000200137
   PubMed Web of Science ®Google Scholar
• 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. J Psychiatr Res, 12(3), 189–198. https://doi.org/10.1016/0022-3956(75)90026-6
   PubMed Web of Science ®Google Scholar
• Gifford, K. A., Phillips, J. S., Samuels, L. R., Lane, E. M., Bell, S. P., Liu, D., Hohman, T. J., Romano, R. R.,s3rd, Fritzsche, L. R., Lu, Z., & Jefferson, A. L., & Alzheimer’s Disease Neuroimaging, I. (2015). Associations between Verbal Learning Slope and Neuroimaging Markers across the Cognitive Aging Spectrum. J Int Neuropsychol Soc, 21(6), 455–467. https://doi.org/10.1017/S1355617715000430
   PubMed Web of Science ®Google Scholar
• Grober, E., & Sliwinski, M. (1991). Development and validation of a model for estimating premorbid verbal intelligence in the elderly. J Clin Exp Neuropsychol, 13(6), 933–949. https://doi.org/10.1080/01688639108405109
   PubMed Web of Science ®Google Scholar
• Hammers, D. B., Atkinson, T. J., Dalley, B. C. A., Suhrie, K. R., Horn, K. P., Rasmussen, K. M., Beardmore, B. E., Burrell, L. D., Duff, K., & Hoffman, J. M. (2017). Amyloid Positivity Using [18F]Flutemetamol-PET and Cognitive Deficits in Nondemented Community-Dwelling Older Adults. Am J Alzheimers Dis Other Demen, 32(6), 320–328. https://doi.org/10.1177/1533317517698795
   PubMed Web of Science ®Google Scholar
• Hammers, D. B., Gradwohl, B. D., Kucera, A., Abildskov, T., Wilde, E. A., & Spencer, R. J. (2021). Preliminary validation of a measure for learning slope for the HVLT-R and BVMT-R in older adults. Cognitive and Behavioral Neurology, 34(3), 170–181. https://doi.org/10.1097/WNN.0000000000000277
   PubMed Web of Science ®Google Scholar
• Hammers, D. B., Spencer, R. J., & Apostolova, L. G. (2022). Validation of and Demographically Adjusted Normative Data for the Learning Ratio Derived from the RAVLT in Robustly Intact Older Adults. Arch Clin Neuropsychol, 37(5), 981–993. https://doi.org/10.1093/arclin/acac002
   PubMed Web of Science ®Google Scholar
• Hammers, D. B., Suhrie, K. R., Dixon, A., Gradwohl, B. D., Archibald, Z. G., King, J. B., Spencer, R. J., Duff, K., & Hoffman, J. M. (2021). Relationship between a novel learning slope metric and Alzheimer’s disease biomarkers. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn, 6(1), 1–21. https://doi.org/10.1080/13825585.2021.1919984
   Google Scholar
• Hammers, D. B., Suhrie, K., Dixon, A., Gradwohl, B. D., Duff, K., & Spencer, R. J. (2021). Validation of HVLT-R, BVMT-R, and RBANS Learning Slope Scores along the Alzheimer’s Continuum. Arch Clin Neuropsychol. https://doi.org/10.1093/arclin/acab023
   Web of Science ®Google Scholar
• Hosmer, D., Lemeshow, S., & Sturdivant, R. (2013). Applied Logistic Regression (Third ed.). John Wiley & Sons, INC.
   Google Scholar
• Kawas, C. H., Greenia, D. E., Bullain, S. S., Clark, C. M., Pontecorvo, M. J., Joshi, A. D., & Corrada, M. M. (2013). Amyloid imaging and cognitive decline in nondemented oldest-old: The 90+ Study. Alzheimers Dement, 9(2), 199–203. https://doi.org/10.1016/j.jalz.2012.06.005
   PubMed Web of Science ®Google Scholar
• Kueper, J. K., Speechley, M., & Montero-Odasso, M. (2018). The Alzheimer’s Disease Assessment Scale-Cognitive Subscale (ADAS-Cog): Modifications and Responsiveness in Pre-Dementia Populations. A Narrative Review. J Alzheimers Dis, 63(2), 423–444. https://doi.org/10.3233/jad-170991
   PubMed Web of Science ®Google Scholar
• Li, J. Q., Tan, L., Wang, H. F., Tan, M. S., Tan, L., Xu, W., Zhao, Q. F., Wang, J., Jiang, T., & Yu, J. T. (2016). Risk factors for predicting progression from mild cognitive impairment to Alzheimer’s disease: A systematic review and meta-analysis of cohort studies. J Neurol Neurosurg Psychiatry, 87(5), 476–484. https://doi.org/10.1136/jnnp-2014-310095
   PubMed Web of Science ®Google Scholar
• Lowe, D. A., Balsis, S., Benge, J. F., & Doody, R. (2015). Adding delayed recall to the ADAS-cog improves measurement precision in mild Alzheimer’s disease: Implications for predicting instrumental activities of daily living. Psychological Assessment, 27(4), 1234–1240. https://doi.org/10.1037/pas0000133
   PubMed Web of Science ®Google Scholar
• Manning, J. R., & Kahana, M. J. (2012). Interpreting semantic clustering effects in free recall. Memory, 20(5), 511–517. https://doi.org/10.1080/09658211.2012.683010
   PubMed Web of Science ®Google Scholar
• Mohs, R. C., Knopman, D., Petersen, R. C., Ferris, S. H., Ernesto, C., Grundman, M., Sano, M., Bieliauskas, L., Geldmacher, D., Clark, C., & Thal, L. J. (1997). Development of cognitive instruments for use in clinical trials of antidementia drugs: Additions to the Alzheimer’s Disease Assessment Scale that broaden its scope. The Alzheimer’s Disease Cooperative Study. Alzheimer Dis Assoc Disord, 11(Suppl 2), S13–21. https://doi.org/10.1097/00002093-199700112-00003
   PubMed Web of Science ®Google Scholar
• Morris, J. C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43(11), 2412–2414. https://doi.org/10.1212/WNL.43.11.2412-a
   PubMed Web of Science ®Google Scholar
• Morrison, R. L., Pei, H., Novak, G., Kaufer, D. I., Welsh-Bohmer, K. A., Ruhmel, S., & Narayan, V. A. (2018). A computerized, self-administered test of verbal episodic memory in elderly patients with mild cognitive impairment and healthy participants: A randomized, crossover, validation study. Alzheimers Dement (Amst), 10(1), 647–656. https://doi.org/10.1016/j.dadm.2018.08.010
   PubMedGoogle Scholar
• Nasreddine, Z. S., Phillips, N. A., Bedirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J. L., & Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. J Am Geriatr Soc, 53(4), 695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x
   PubMed Web of Science ®Google Scholar
• Jack, C. R.,sJr., Bennett, D. A., Blennow, K. et al. (2018). NIA-AA Research Framework: Toward a biological definition of Alzheimer’s disease. Alzheimers Dement, 14(4), 535–562. doi:10.1016/j.jalz.2018.02.018.
   PubMed Web of Science ®Google Scholar
• Ossenkoppele, R., Madison, C., Oh, H., Wirth, M., van Berckel, B. N., & Jagust, W. J. (2014). Is verbal episodic memory in elderly with amyloid deposits preserved through altered neuronal function? [Research Support, N.I.H., Extramural]. Cereb Cortex, 24(8), 2210–2218. https://doi.org/10.1093/cercor/bht076
   PubMed Web of Science ®Google Scholar
• Randolph, C. (2012). Repeatable Battery for the Assessment of Neuropsychological Status. The Psychological Corporation.
   Google Scholar
• Rosen, W. G., Mohs, R. C., & Davis, K. L. (1984). A new rating scale for Alzheimer’s disease. Am J Psychiatry, 141(11), 1356–1364. https://doi.org/10.1176/ajp.141.11.1356
   PubMed Web of Science ®Google Scholar
• Sano, M., Raman, R., Emond, J., Thomas, R. G., Petersen, R., Schneider, L. S., & Aisen, P. S. (2011). Adding delayed recall to the Alzheimer Disease Assessment Scale is useful in studies of mild cognitive impairment but not Alzheimer disease. Alzheimer Dis Assoc Disord, 25(2), 122–127. https://doi.org/10.1097/WAD.0b013e3181f883b7
   PubMed Web of Science ®Google Scholar
• Schmidt, M. (1996). The Rey Auditory Verbal Learning Test. Western Psychological Services.
   Google Scholar
• Schwarz, A. J., Shcherbinin, S., Slieker, L. J., Risacher, S. L., Charil, A., Irizarry, M. C., Fleisher, A. S., Southekal, S., Joshi, A. D., Devous, M. D.,sSr., Miller, B. B., & Saykin, A. J. (2018). Topographic staging of tau positron emission tomography images. Alzheimers Dement (Amst), 10(1), 221–231. https://doi.org/10.1016/j.dadm.2018.01.006
   PubMedGoogle Scholar
• Sheikh, J. I., & Yesavage, J. (1986). Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version. Clinical Gerontologist, 5(1–2), 165–172. https://doi.org/10.1300/J018v05n01_09
   Google Scholar
• Spencer, R. J., Gradwohl, B. D., Williams, T. F., Kordovski, V. M., & Hammers, D. B. (2020). Developing learning slope scores for the repeatable battery for the assessment of neuropsychological status. Appl Neuropsychol Adult, 27(1), 1–7. https://doi.org/10.1080/23279095.2020.1791870
   PubMedGoogle Scholar
• Sperling, R. A., Johnson, K. A., Doraiswamy, P. M., Reiman, E. M., Fleisher, A. S., Sabbagh, M. N., Sadowsky, C. H., Carpenter, A., Davis, M. D., Lu, M., Flitter, M., Joshi, A. D., Clark, C. M., Grundman, M., Mintun, M. A., Skovronsky, D. M., & Pontecorvo, M. J. (2013). Amyloid deposition detected with florbetapir F 18 ((18)F-AV-45) is related to lower episodic memory performance in clinically normal older individuals. Neurobiol Aging, 34(3), 822–831. https://doi.org/10.1016/j.neurobiolaging.2012.06.014
   PubMed Web of Science ®Google Scholar
• Lagarde, J., Olivieri, P., Tonietto, M. et al. (2022). Tau-PET imaging predicts cognitive decline and brain atrophy progression in early Alzheimer’s disease. J Neurol Neurosurg Psychiatry, 93(5), 459–467. doi:10.1136/jnnp-2021-328623 .
   PubMed Web of Science ®Google Scholar
• Thomas, K. R., Bangen, K. J., Weigand, A. J., Edmonds, E. C., Wong, C. G., Cooper, S., Delano-Wood, L., Bondi, M. W., & Alzheimer’s Disease Neuroimaging, I. (2020). Objective subtle cognitive difficulties predict future amyloid accumulation and neurodegeneration. Neurology, 94(4), e397–e406. https://doi.org/10.1212/WNL.0000000000008838
   PubMed Web of Science ®Google Scholar
• Wechsler, D. (1987). WMS-R: Wechsler Memory Scale–Revised: Manual. The Psychological Corporation.
   Google Scholar
• Weiner, M. W., Veitch, D. P., Aisen, P. S., Beckett, L. A., Cairns, N. J., Green, R. C., Harvey, D., Jack, C. R.,sJr., Jagust, W., Morris, J. C., Petersen, R. C., Salazar, J., Saykin, A. J., Shaw, L. M., Toga, A. W., Trojanowski, J. Q., & Alzheimer’s Disease Neuroimaging, I. (2017). The Alzheimer’s Disease Neuroimaging Initiative 3: Continued innovation for clinical trial improvement. Alzheimers Dement, 13(5), 561–571. https://doi.org/10.1016/j.jalz.2016.10.006
   PubMed Web of Science ®Google Scholar
• Wesnes, K. A. (2008). Assessing Change in Cognitive Function in Dementia: The Relative Utilities of the Alzheimer’s Disease Assessment Scale – Cognitive Subscale and the Cognitive Drug Research System. Neurodegenerative Diseases, 5(3–4), 261–263. https://doi.org/10.1159/000113719
   PubMed Web of Science ®Google Scholar
• Wolk, D., Salloway, S., & Dickerson, B. (2019). Putting the New Alzheimer Disease Amyloid, Tau, Neurodegeneration (AT[N]) Diagnostic System to the Test. JAMA, 321(23), 2289–2291. https://doi.org/10.1001/jama.2019.7534
   PubMed Web of Science ®Google Scholar