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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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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.

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References

  1. 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

    Article  PubMed  Google Scholar 

  2. 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

    Article  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  PubMed  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Italian Ministry of Health (grant number 217/RF-2013-02359074).

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Authors and Affiliations

  1. Laboratory of Clinical and Behavioral Neurology, IRCCS Santa Lucia Foundation, V. Ardeatina, 306, 00179, Rome, Italy

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

  2. Department of Systems Medicine, Tor Vergata University, Rome, Italy

    Lucia Fadda, Carlo Caltagirone & Giovanni Augusto Carlesimo

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  1. Maria Stefania De Simone
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  2. Roberta Perri
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Correspondence to Maria Stefania De Simone.

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This study was approved by the ethics committee of the Santa Lucia Foundation in accordance with the Declaration of Helsinki and its later amendments. All participants gave their written informed consent prior to their inclusion in the study.

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De Simone, M.S., Perri, R., Fadda, L. et al. Predicting progression to Alzheimer’s disease in subjects with amnestic mild cognitive impairment using performance on recall and recognition tests. J Neurol 266, 102–111 (2019). https://doi.org/10.1007/s00415-018-9108-0

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