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Diagnostic Accuracy of Memory Measures in Alzheimer’s Dementia and Mild Cognitive Impairment: a Systematic Review and Meta-Analysis

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Abstract

With an increasing focus on biomarkers in dementia research, illustrating the role of neuropsychological assessment in detecting mild cognitive impairment (MCI) and Alzheimer’s dementia (AD) is important. This systematic review and meta-analysis, conducted in accordance with PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) standards, summarizes the sensitivity and specificity of memory measures in individuals with MCI and AD. Both meta-analytic and qualitative examination of AD versus healthy control (HC) studies (n = 47) revealed generally high sensitivity and specificity (≥ 80% for AD comparisons) for measures of immediate (sensitivity = 87%, specificity = 88%) and delayed memory (sensitivity = 89%, specificity = 89%), especially those involving word-list recall. Examination of MCI versus HC studies (n = 38) revealed generally lower diagnostic accuracy for both immediate (sensitivity = 72%, specificity = 81%) and delayed memory (sensitivity = 75%, specificity = 81%). Measures that differentiated AD from other conditions (n = 10 studies) yielded mixed results, with generally high sensitivity in the context of low or variable specificity. Results confirm that memory measures have high diagnostic accuracy for identification of AD, are promising but require further refinement for identification of MCI, and provide support for ongoing investigation of neuropsychological assessment as a cognitive biomarker of preclinical AD. Emphasizing diagnostic test accuracy statistics over null hypothesis testing in future studies will promote the ongoing use of neuropsychological tests as Alzheimer’s disease research and clinical criteria increasingly rely upon cerebrospinal fluid (CSF) and neuroimaging biomarkers.

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Notes

  1. The selective reminding paradigm has been well described (see Carlesimo et al. 2011) and is best exemplified by the Free and Cued Selective Reminding Test (Grober and Buschke 1987). This paradigm attempts to control for encoding of material by providing the name of each semantic category (4 total) and asking subjects to point to each of 4 items within the semantic category. This is followed by immediate category cued recall (repeated until 4/4 items recalled). Next, individuals are asked to freely recall the items on the list. A category cued recall procedure is then used for any items not freely recalled. This procedure is typically repeated three times and provides a measure of free recall and total recall (free recall + cued recall).

  2. A picture with two interacting pieces is presented (e.g., ape holding an umbrella) and individuals are asked to name both aspects of the picture. Immediately following presentation of six pictures, six cards are presented containing only one aspect of the picture (e.g., the ape alone). With presentation of the card missing an object, the individual is asked to say the item that is missing. Responses are accepted in any format: written, drawn, oral, or mimed.

  3. Eight semantically or associatively unrelated word pairs (four concrete, e.g., horse-forest, and four abstract, e.g., open-fresh). Associate-Recognition task was always completed during the first and the Cued-Recall during the second session. After presentation of the eight pairs, in the Associate-Recognition phase, a cue was presented at the top of the page and individuals identified which from a list of 4 items had been presented with the cue. For the Cued-Recall phase, the cue was presented and the individual was asked to recall the word that had been paired with the cue.

  4. A computerized task that displays boxes on the screen that are randomly opened. Some boxes contain a pattern. Patterns are then displayed in the middle of the screen and the individual must match the pattern in the middle of the screen to the appropriate location (i.e., box). When a mistake is made, the boxes are re-opened to remind the individual. The test becomes more difficult throughout and takes about 10 min to administer.

  5. In the paper and pencil task, 10 faces and 10 objects were presented. The original version of the test showed faces in black and white whereas the novel version presented faces and objects in color. After encoding, individuals are immediately presented with the face or object (one at a time) and report in which quadrant of the page the item was originally presented. The total score is the number placed correctly out of 20. The computerized version was similar with an additional 10 shapes or 10 animals (30 items presented total) and participants were asked to click on the quadrant where the item had initially been presented. For both versions of the test, the 10 items belonging to a category were presented and tested separately, for example, encoding and testing phase of 10 faces followed by encoding and testing of 10 objects.

  6. WMS Verbal Paired Associates (Wechsler 1945, VPA) (Spanish translation), individuals learned 10 pairs of words (6 related, 4 unrelated) across three trials, providing one score of total memory acquisition.

  7. Individuals saw 2 or 3 items on the screen (difficulty varied depending on diagnosis; HC saw 3 items, AD patients saw 2 items) for 2000 ms during the study display. Following the study phase, individuals’ visual short-term memory was assessed for single feature and binding by using “color only” and “shape only” conditions in addition to “shape-color binding” conditions. In single feature conditions, new shapes or new colors were replaced in the test phase, respectively, so that memory for individual features was required to detect the change. In the shape-color binding condition, two shapes changed colors in the test phase compared to the study phase so that memory of both the bound shape and color elements was required to detect change.

  8. This test examines associative memory of spatial location, event-place association, and place-object association memory.

  9. During this test, participants are asked to re-create a 2 by 3 array of six simple geometric figures after three 10 s learning trials. Points are awarded for accuracy and correct object placement.

  10. During this task participants are asked to recall the associated symbol of nine numbers that they initially learn through a coding task (WAIS-III Digit Symbol; (Wechsler 1997)).

  11. Involves three time-based and three event-based prospective memory items embedded within puzzles of attention (Delprado et al. 2012). Two scores can be derived for this measure, an event-based score and a time-based score.

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Acknowledgements

This research was partially supported by the Department of Veterans Affairs, Veterans Health Administration, VISN 1 Career Development Award (N.H.S.), as well as National Institutes of Health grants R01 AG049810 (M.W.B.) and K24 AG026431 (M.W.B.). This material is also based upon work supported by the Office of Academic Affiliations, Department of Veterans Affairs. NHS serves as a consultant to Biogen. MWB serves as a consultant to Novartis and Eisai and receives royalties from Oxford University Press. KS was supported in this work by a University of the Sunshine Coast Research Scholarship. MS reports personal fees from Eli Lily (Australia) Pty Ltd and grants from Novotech Pty Ltd, outside the submitted work. The authors report no conflicts of interest. The contents of this article do not represent the views of the U.S. Department of Veterans Affairs of the United States Government.

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Author notes

  1. Gali H. Weissberger and Jessica V. Strong contributed equally to this work

Authors and Affiliations

  1. Brain, Behavior, and Aging Research Center, VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA

    Gali H. Weissberger

  2. Psychology Service, VA Boston Healthcare System, Boston, MA, USA

    Gali H. Weissberger, Jessica V. Strong & Nikki H. Stricker

  3. New England Geriatric Research, Education and Clinical Center (GRECC), Boston VA Healthcare System, Boston, MA, USA

    Jessica V. Strong

  4. Sunshine Coast Mind and Neuroscience – Thompson Institute, University of the Sunshine Coast, Sippy Downs, Queensland, Australia

    Kayla B. Stefanidis & Mathew J. Summers

  5. VA San Diego Healthcare System, San Diego, CA, USA

    Mark W. Bondi

  6. Department of Psychiatry, University of California San Diego, La Jolla, CA, USA

    Mark W. Bondi

  7. Department of Psychiatry and Psychology, Mayo Clinic, 200 First Street SW, Rochester, MN, 55905, USA

    Nikki H. Stricker

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Correspondence to Nikki H. Stricker.

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Weissberger, G.H., Strong, J.V., Stefanidis, K.B. et al. Diagnostic Accuracy of Memory Measures in Alzheimer’s Dementia and Mild Cognitive Impairment: a Systematic Review and Meta-Analysis. Neuropsychol Rev 27, 354–388 (2017). https://doi.org/10.1007/s11065-017-9360-6

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