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01-01-2019 | Original Communication

Predicting progression to Alzheimer’s disease in subjects with amnestic mild cognitive impairment using performance on recall and recognition tests

Authors: Maria Stefania De Simone, Roberta Perri, Lucia Fadda, Carlo Caltagirone, Giovanni Augusto Carlesimo

Published in: Journal of Neurology | Issue 1/2019

Abstract

The research of reliable procedures for predicting cognitive decline or stability in persons with amnestic mild cognitive impairment (a-MCI) is a major goal for the early identification of subjects in the prodromal stages of dementia. The aim of this study was to evaluate whether different memory performances on two procedures commonly used for the neuropsychological assessment of episodic memory (i.e., free recall and recognition) might be a key in predicting a-MCI patients’ subsequent progression to Alzheimer’s disease (AD). For this purpose, 80 patients diagnosed with a-MCI at the first assessment and followed-up for at least 3 years were included. During this time, 41 subjects remained in a stable condition of cognitive impairment or improved (stable-MCI) and 39 patients converted to AD dementia (converter-MCI). Sixty-two age- and education-matched healthy individuals were also recruited as healthy controls (HC). Baseline memory performance on the free recall (5th immediate and 15-min delayed) and yes/no recognition (the sensitivity measure d′) of a 15-word list were analyzed. Results showed that stable-MCIs forgot significantly more information from immediate to delayed recall of the word list than HC, but exhibited a pronounced improvement of memory performance in the recognition test format. On the contrary, converter-MCIs showed diminished sensitivity in benefiting from cues for recognizing studied words. Word list recognition correctly classified group membership with good overall accuracy, which was higher compared to the classification of converter and stable a-MCIs provided by free recall; therefore, it could be a useful diagnostic tool for predicting progression to AD dementia from the prodromal stage.

Albert M, DeKosky S, Dickson D 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. https://doi.org/10.1016/j.jalz.2011.03.008 CrossRefPubMed

Dubois B, Feldman H, Jacova C et al (2007) Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS–ADRDA criteria. Lancet Neurol 6:734–746. https://doi.org/10.1016/s1474-4422(07)70178-3 CrossRefPubMed

Braak H, Braak E (1995) Staging of alzheimer’s disease-related neurofibrillary changes. Neurobiol Aging 16:271–278. https://doi.org/10.1016/0197-4580(95)00021-6 CrossRefPubMed

Scarpazza C, De Simone M (2016) Voxel-based morphometry: current perspectives. Neurosci Neuroecon 5:19–35. https://doi.org/10.2147/nan.s66439 CrossRef

Squire L, Stark C, Clark R (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306. https://doi.org/10.1146/annurev.neuro.27.070203.144130 CrossRefPubMed

Petersen R, Smith G, Waring S et al (1999) Mild cognitive impairment. Arch Neurol 56:303. https://doi.org/10.1001/archneur.56.3.303 CrossRefPubMed

Sarazin M, Berr C, De Rotrou J et al (2007) Amnestic syndrome of the medial temporal type identifies prodromal AD: a longitudinal study. Neurology 69:1859–1867. https://doi.org/10.1212/01.wnl.0000279336.36610.f7 CrossRefPubMed

De Simone M, Perri R, Fadda L et al (2017) Different deficit patterns on word lists and short stories predict conversion to Alzheimer’s disease in patients with amnestic mild cognitive impairment. J Neurol 264:2258–2267. https://doi.org/10.1007/s00415-017-8623-8 CrossRefPubMed

Pasquier F, Grymonprez L, Lebert F, Van der Linden M (2001) Memory impairment differs in frontotemporal dementia and Alzhemier?s disease. Neurocase 7:161–171. https://doi.org/10.1076/neur.7.2.161.16263 CrossRefPubMed

10.

Lemos R, Duro D, Simoes M, Santana I (2014) The free and cued selective reminding test distinguishes frontotemporal dementia from Alzheimer’s disease. Arch Clin Neuropsychol 29:670–679. https://doi.org/10.1093/arclin/acu031 CrossRefPubMedPubMedCentral

11.

Lemos R, Marôco J, Simões M et al (2015) The free and cued selective reminding test for predicting progression to Alzheimer’s disease in patients with mild cognitive impairment: a prospective longitudinal study. J Neuropsychol 11:40–55. https://doi.org/10.1111/jnp.12075 CrossRefPubMed

12.

Apostolova L, Dutton R, Dinov I et al (2006) Conversion of mild cognitive impairment to alzheimer disease predicted by hippocampal atrophy maps. Arch Neurol 63:693. https://doi.org/10.1001/archneur.63.5.693 CrossRefPubMed

13.

Yang J, Pan P, Song W et al (2012) Voxelwise meta-analysis of gray matter anomalies in Alzheimer’s disease and mild cognitive impairment using anatomic likelihood estimation. J Neurol Sci 316:21–29. https://doi.org/10.1016/j.jns.2012.02.010 CrossRefPubMed

14.

Perri R, Carlesimo G, Serra L, Caltagirone C (2009) When the amnestic mild cognitive impairment disappears. Cogn Behav Neurol 22:109–116. https://doi.org/10.1097/wnn.0b013e3181a7225c CrossRefPubMed

15.

Burke D, Light L (1981) Memory and aging: The role of retrieval processes. Psychol Bull 90:513–546. https://doi.org/10.1037//0033-2909.90.3.513 CrossRefPubMed

16.

Bennett I, Golob E, Parker E, Starr A (2006) Memory Evaluation in Mild Cognitive Impairment using Recall and Recognition Tests. J Clin Exp Neuropsychol 28:1408–1422. https://doi.org/10.1080/13803390500409583 CrossRefPubMed

17.

Gainotti G, Marra C (1994) Some aspects of memory disorders clearly distinguish dementia of the Alzheimer’s type from depressive pseudo-dementia. J Clin Exp Neuropsychol 16:65–78. https://doi.org/10.1080/01688639408402617 CrossRefPubMed

18.

Delis D, Massman P, Butters N et al (1991) Profiles of demented and amnesic patients on the California verbal learning test: implications for the assessment of memory disorders. Psychol Assess 3:19–26. https://doi.org/10.1037//1040-3590.3.1.19 CrossRef

19.

Glosser G, Gallo J, Clark C, Grossman M (2002) Memory encoding and retrieval in frontotemporal dementia and Alzheimer’s disease. Neuropsychology 16:190–196. https://doi.org/10.1037//0894-4105.16.2.190 CrossRefPubMed

20.

Lee A, Rahman S, Hodges J et al (2003) Associative and recognition memory for novel objects in dementia: implications for diagnosis. Eur J Neurosci 18:1660–1670. https://doi.org/10.1046/j.1460-9568.2003.02883.x CrossRefPubMed

21.

Fine E, Delis D, Wetter S et al (2008) Identifying the “source” of recognition memory deficits in patients with Huntington’s disease or Alzheimer’s disease: evidence from the CVLT-II. J Clin Exp Neuropsychol 30:463–470. https://doi.org/10.1080/13803390701531912 CrossRefPubMedPubMedCentral

22.

Tierney M, Black S, Szalai J et al (2001) Recognition memory and verbal fluency differentiate probable Alzheimer disease from subcortical ischemic vascular dementia. Arch Neurol 58:1654. https://doi.org/10.1001/archneur.58.10.1654 CrossRefPubMed

23.

Flanagan E, Wong S, Dutt A et al (2016) False recognition in behavioral variant frontotemporal dementia and Alzheimer’s disease—disinhibition or amnesia? Front Aging Neurosci. https://doi.org/10.3389/fnagi.2016.00177 CrossRefPubMedPubMedCentral

24.

Hornberger M, Piguet O, Graham A et al (2010) How preserved is episodic memory in behavioral variant frontotemporal dementia? Neurology 74:472–479. https://doi.org/10.1212/wnl.0b013e3181cef85d CrossRefPubMedPubMedCentral

25.

Ranjith N, Mathuranath P, Sharma G, Alexander A (2010) Qualitative aspects of learning, recall, and recognition in dementia. Ann Indian Acad Neurol 13:117. https://doi.org/10.4103/0972-2327.64639 CrossRefPubMedPubMedCentral

26.

Harciarek M, Jodzio K (2005) Neuropsychological differences between frontotemporal dementia and Alzheimer’s disease: a review. Neuropsychol Rev 15:131–145. https://doi.org/10.1007/s11065-005-7093-4 CrossRefPubMed

27.

Ricci M, Graef S, Blundo C, Miller L (2012) Using the Rey Auditory Verbal Learning Test (RAVLT) to differentiate Alzheimer’s dementia and behavioural variant fronto-temporal dementia. Clin Neuropsychol 26:926–941. https://doi.org/10.1080/13854046.2012.704073 CrossRefPubMed

28.

Barbeau E, Didic M, Tramoni E et al (2004) Evaluation of visual recognition memory in MCI patients. Neurology 62:1317–1322. https://doi.org/10.1212/01.wnl.0000120548.24298.db CrossRefPubMed

29.

Wolk D, Signoff E, DeKosky S (2008) Recollection and familiarity in amnestic mild cognitive impairment: a global decline in recognition memory. Neuropsychologia 46:1965–1978. https://doi.org/10.1016/j.neuropsychologia.2008.01.017 CrossRefPubMedPubMedCentral

30.

Algarabel S, Fuentes M, Escudero J et al (2012) Recognition memory deficits in mild cognitive impairment. Aging Neuropsychol Cogn 19:608–619. https://doi.org/10.1080/13825585.2011.640657 CrossRef

31.

Russo M, Cohen G, Campos J et al (2016) Usefulness of discriminability and response bias indices for the evaluation of recognition memory in mild cognitive impairment and Alzheimer disease. Dement Geriatr Cogn Disord 43:1–14. https://doi.org/10.1159/000452255 CrossRefPubMed

32.

Zakzanis K, Leach L, Kaplan E (1999) Neuropsychological differential diagnosis. Swets & Zeitlinger, Lisse

33.

Parker E, Landau S, Whipple S, Schwartz B (2004) Aging, recall and recognition: a study on the sensitivity of the University of Southern California Repeatable Episodic Memory Test (USC-REMT). J Clin Exp Neuropsychol 26:428–440. https://doi.org/10.1080/13803390490510130 CrossRefPubMed

34.

Griffith H, Netson K, Harrell L et al (2006) Amnestic mild cognitive impairment: diagnostic outcomes and clinical prediction over a two-year time period. J Int Neuropsychol Soc. https://doi.org/10.1017/s1355617706060267 CrossRefPubMed

35.

Rabin L, Paré N, Saykin A et al (2009) Differential memory test sensitivity for diagnosing amnestic mild cognitive impairment and predicting conversion to Alzheimer’s disease. Aging Neuropsychol Cogn 16:357–376. https://doi.org/10.1080/13825580902825220 CrossRef

36.

Yang H, Yang Y, Legesse B, Kim S (2012) Subtypes of amnestic mild cognitive impairment based on memory impairment pattern and its potential clinical significance. Dement Neurocogn Disord 11:59. https://doi.org/10.12779/dnd.2012.11.2.59 CrossRef

37.

García-Herranz S, Díaz-Mardomingo M, Peraita H (2015) Neuropsychological predictors of conversion to probable Alzheimer disease in elderly with mild cognitive impairment. J Neuropsychol 10:239–255. https://doi.org/10.1111/jnp.12067 CrossRefPubMed

38.

Russo M, Campos J, Vázquez S et al (2017) Adding recognition discriminability index to the delayed recall is useful to predict conversion from mild cognitive impairment to Alzheimer’s disease in the Alzheimer’s disease neuroimaging initiative. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2017.00046 CrossRefPubMedPubMedCentral

39.

Petersen R, Caracciolo B, Brayne C et al (2014) Mild cognitive impairment: a concept in evolution. J Intern Med 275:214–228. https://doi.org/10.1111/joim.12190 CrossRefPubMedPubMedCentral

40.

McKhann G, Drachman D, Folstein M et al (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 34:939–939. https://doi.org/10.1212/wnl.34.7.939 CrossRefPubMed

41.

McKhann G, Knopman D, Chertkow H 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 Dement 7:263–269. https://doi.org/10.1016/j.jalz.2011.03.005 CrossRef

42.

Carlesimo G, Caltagirone C, Gainotti G et al (1996) The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. Eur Neurol 36:378–384. https://doi.org/10.1159/000117297 CrossRefPubMed

43.

Carlesimo GA, Buccione I, Fadda LM, Graceffa A, Mauri M, Lorusso S, Caltagirone C (2002) Standardizzazione di due test di memoria per uso clinico. Nuova Rivista di Neurologia 12(1):1–13

44.

Monaco M, Costa A, Caltagirone C, Carlesimo G (2012) Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci 34:749–754. https://doi.org/10.1007/s10072-012-1130-x CrossRefPubMed

45.

Nocentini U, Di Vincenzo S, Panella M, Pasqualetti P, Caltagirone C (2002) La valutazione delle funzioni esecutive nella pratica neuropsicologica: dal Modified Card Sorting Test al Modified Card Sorting Test: Roma Version. Dati di standardizzazione. Nuova Rivista di Neurologia 12(1):14–24

46.

Miceli G, Laudanna A, Burani C, Capasso R (1994) Batteria per l’Analisi dei Deficit Afasici BADA: Università Cattolica del Sacro Cuore. Servizio di Neuropsicologia, Consiglio Nazionale delle Ricerche. Istituto di Psicologia

47.

Kamman R (1970) Signal detection theory and recognition memory: Part I (basic calculation). In: Workbook for general psychology. Practice-Hall, City

48.

Gifford D, Cummings J (1999) Evaluating dementia screening tests. Neurology 52:224–224. https://doi.org/10.1212/wnl.52.2.224 CrossRefPubMed

49.

Perri R, Serra L, Carlesimo G, Caltagirone C (2007) Amnestic mild cognitive impairment: difference of memory profile in subjects who converted or did not convert to Alzheimer’s disease. Neuropsychology 21:549–558. https://doi.org/10.1037/0894-4105.21.5.549 CrossRefPubMed

50.

Borroni B, Anchisi D, Paghera B et al (2006) Combined 99mTc-ECD SPECT and neuropsychological studies in MCI for the assessment of conversion to AD. Neurobiol Aging 27:24–31. https://doi.org/10.1016/j.neurobiolaging.2004.12.010 CrossRefPubMed

51.

Tabert M, Manly J, Liu X et al (2006) Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Arch Gen Psychiatry 63:916. https://doi.org/10.1001/archpsyc.63.8.916 CrossRefPubMed

52.

Fleisher A, Sowell B, Taylor C et al (2007) Clinical predictors of progression to Alzheimer disease in amnestic mild cognitive impairment. Neurology 68:1588–1595. https://doi.org/10.1212/01.wnl.0000258542.58725.4c CrossRefPubMed

53.

Gauthier S, Reisberg B, Zaudig M et al (2006) Mild cognitive impairment. Lancet 367:1262–1270. https://doi.org/10.1016/s0140-6736(06)68542-5 CrossRefPubMed

Title: Predicting progression to Alzheimer’s disease in subjects with amnestic mild cognitive impairment using performance on recall and recognition tests
Authors: Maria Stefania De Simone
Roberta Perri
Lucia Fadda
Carlo Caltagirone
Giovanni Augusto Carlesimo
Publication date: 01-01-2019
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue 1/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-018-9108-0

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Predicting progression to Alzheimer’s disease in subjects with amnestic mild cognitive impairment using performance on recall and recognition tests

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