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The dual role of cognitive reserve in subjective cognitive decline and mild cognitive impairment: a 7-year follow-up study

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Abstract

The aim of this study was to evaluate the effect of cognitive reserve (CR), in progression from subjective cognitive decline (SCD) to mild cognitive impairment (MCI) and Alzheimer’s disease (AD). For this purpose, we followed up 263 patients (154 SCD; 109 MCI) for a mean time of 7 years. CR was assessed by the Test di Intelligenza Breve (TIB), functionally equivalent to the National Adult Reading Test. High CR resulted as a protective factor for progression from SCD to MCI. Age at conversion to MCI was delayed 9 years on average in SCD with high CR with respect to SCD with low CR. On the contrary, high CR resulted as a risk factor for progression from MCI to AD dementia only in APOE ε4 carriers. Conversion time from MCI to AD dementia was 3 years shorter in ε4 carriers with high CR than subjects with low CR and ε4 non-carriers with high CR. Consistent with the CR hypothesis, our results showed that higher levels of CR protect against the earliest clinical manifestations of AD. In line with the previous researches, we found an interaction between CR and APOE in progression from MCI to AD dementia.

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Abbreviations

CR:

Cognitive reserve

SCD:

Subjective cognitive decline

TIB:

Test di Intelligenza Breve

HDRS:

Hamilton Depression Rating Scale

NART:

National adult reading test

References

  1. Stern Y (2009) Cognitive reserve. Neuropsychologia 47:2015–2028. https://doi.org/10.1016/j.neuropsychologia.2009.03.004

    Article  PubMed  PubMed Central  Google Scholar 

  2. Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R (1994) Influence of education and occupation on the incidence of Alzheimer’s disease. JAMA 271:1004–1010

    Article  CAS  PubMed  Google Scholar 

  3. Bessi V, Mazzeo S, Padiglioni S, Piccini C, Nacmias B, Sorbi S, Bracco L (2018) From subjective cognitive decline to Alzheimer’s disease: the predictive role of neuropsychological assessment, personality traits, and cognitive reserve. A 7-year follow-up study. J Alzheimers Dis JAD. https://doi.org/10.3233/JAD-171180

    Article  PubMed  Google Scholar 

  4. Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc JINS 8:448–460

    Article  PubMed  Google Scholar 

  5. Cecchetti L, Ricciardi E, Volpi L, Carlesi C, Pagni C, Handjaras G, Leo A, Tognoni G, Pietrini P (2013) Cognitive reserve modulates neural responses in subjective and mild cognitive impairment. Alzheimers Dement J Alzheimers Assoc 9:P490. https://doi.org/10.1016/j.jalz.2013.05.1003

    Article  Google Scholar 

  6. Garibotto V, Borroni B, Sorbi S, Cappa SF, Padovani A, Perani D (2012) Education and occupation provide reserve in both ApoE ε4 carrier and noncarrier patients with probable Alzheimer’s disease. Neurol Sci Off J Ital Neurol Soc Ital Soc Clin Neurophysiol 33:1037–1042. https://doi.org/10.1007/s10072-011-0889-5

    Article  CAS  Google Scholar 

  7. Franzmeier N, Hartmann JC, Taylor ANW, Araque Caballero M, Simon-Vermot L, Buerger K, Kambeitz-Ilankovic LM, Ertl-Wagner B, Mueller C, Catak C, Janowitz D, Stahl R, Dichgans M, Duering M, Ewers M (2017) Left frontal hub connectivity during memory performance supports reserve in aging and mild cognitive impairment. J Alzheimers Dis JAD 59:1381–1392. https://doi.org/10.3233/JAD-170360

    Article  CAS  PubMed  Google Scholar 

  8. Jones RN, Manly J, Glymour MM, Rentz DM, Jefferson AL, Stern Y (2011) Conceptual and measurement challenges in research on cognitive reserve. J Int Neuropsychol Soc JINS 17:593–601. https://doi.org/10.1017/S1355617710001748

    Article  PubMed  Google Scholar 

  9. Stern Y, Alexander GE, Prohovnik I, Mayeux R (1992) Inverse relationship between education and parietotemporal perfusion deficit in Alzheimer’s disease. Ann Neurol 32:371–375. https://doi.org/10.1002/ana.410320311

    Article  CAS  PubMed  Google Scholar 

  10. Scarmeas N, Levy G, Tang M-X, Manly J, Stern Y (2001) Influence of leisure activity on the incidence of Alzheimer’s disease. Neurology 57:2236–2242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Park DC, Lautenschlager G, Hedden T, Davidson NS, Smith AD, Smith PK (2002) Models of visuospatial and verbal memory across the adult life span. Psychol Aging 17:299–320

    Article  PubMed  Google Scholar 

  12. Wisdom NM, Mignogna J, Collins RL (2012) Variability in Wechsler Adult Intelligence Scale-IV subtest performance across age. Arch Clin Neuropsychol Off J Natl Acad Neuropsychol 27:389–397. https://doi.org/10.1093/arclin/acs041

    Article  Google Scholar 

  13. Jessen F, Amariglio RE, van Boxtel M, Breteler M, Ceccaldi M, Chételat G, Dubois B, Dufouil C, Ellis KA, van der Flier WM, Glodzik L, van Harten AC, de Leon MJ, McHugh P, Mielke MM, Molinuevo JL, Mosconi L, Osorio RS, Perrotin A, Petersen RC, Rabin LA, Rami L, Reisberg B, Rentz DM, Sachdev PS, de la Sayette V, Saykin AJ, Scheltens P, Shulman MB, Slavin MJ, Sperling RA, Stewart R, Uspenskaya O, Vellas B, Visser PJ, Wagner M (2014) A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimers Dement J Alzheimers Assoc 10:844–852. https://doi.org/10.1016/j.jalz.2014.01.001

    Article  Google Scholar 

  14. Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183–194. https://doi.org/10.1111/j.1365-2796.2004.01388.x

    Article  CAS  Google Scholar 

  15. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (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. Alzheimers Dement J Alzheimers Assoc 7:270–279. https://doi.org/10.1016/j.jalz.2011.03.008

    Article  Google Scholar 

  16. Reisberg B, Gauthier S (2008) Current evidence for subjective cognitive impairment (SCI) as the pre-mild cognitive impairment (MCI) stage of subsequently manifest Alzheimer’s disease. Int Psychogeriatr 20:1–16. https://doi.org/10.1017/S1041610207006412

    Article  PubMed  Google Scholar 

  17. Mitchell AJ (2008) Is it time to separate subjective cognitive complaints from the diagnosis of mild cognitive impairment? Age Ageing 37:497–499. https://doi.org/10.1093/ageing/afn147

    Article  PubMed  Google Scholar 

  18. Mendonça MD, Alves L, Bugalho P (2016) From subjective cognitive complaints to dementia: who is at risk? A systematic review. Am J Alzheimers Dis Other Demen 31:105–114. https://doi.org/10.1177/1533317515592331

    Article  PubMed  Google Scholar 

  19. Lojo-Seoane C, Facal D, Guàrdia-Olmos J, Juncos-Rabadán O (2014) Structural model for estimating the influence of cognitive reserve on cognitive performance in adults with subjective memory complaints. Arch Clin Neuropsychol 29:245–255. https://doi.org/10.1093/arclin/acu007

    Article  PubMed  Google Scholar 

  20. Perquin M, Diederich N, Pastore J, Lair M-L, Stranges S, Vaillant M, Group on behalf of the M (2015) Prevalence of dementia and cognitive complaints in the context of high cognitive reserve: a population-based study. PLoS One 10:e0138818. https://doi.org/10.1371/journal.pone.0138818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. João AA, Maroco J, Ginó S, Mendes T, Mendonça A de, Martins IP (2015) Education modifies the type of subjective memory complaints in older people. Int J Geriatr Psychiatry 31:153–160. https://doi.org/10.1002/gps.4305

    Article  Google Scholar 

  22. Lenehan ME, Summers MJ, Saunders NL, Summers JJ, Vickers JC (2015) Relationship between education and age-related cognitive decline: a review of recent research. Psychogeriatrics 15:154–162. https://doi.org/10.1111/psyg.12083

    Article  PubMed  Google Scholar 

  23. Soldan A, Pettigrew C, Cai Q, Wang J, Wang M-C, Moghekar A, Miller MI, Albert M, BIOCARD Research Team (2017) Cognitive reserve and long-term change in cognition in aging and preclinical Alzheimer’s disease. Neurobiol Aging 60:164–172. https://doi.org/10.1016/j.neurobiolaging.2017.09.002

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lojo-Seoane C, Facal D, Guàrdia-Olmos J, Pereiro AX, Juncos-Rabadán O (2018) Effects of cognitive reserve on cognitive performance in a follow-up study in older adults with subjective cognitive complaints. The role of working memory. Front Aging Neurosci 10:189. https://doi.org/10.3389/fnagi.2018.00189

    Article  PubMed  PubMed Central  Google Scholar 

  25. Aghjayan SL, Buckley RF, Vannini P, Rentz DM, Jackson JD, Sperling RA, Johnson KA, Amariglio RE (2017) The influence of demographic factors on subjective cognitive concerns and beta-amyloid. Int Psychogeriatr 29:645–652. https://doi.org/10.1017/S1041610216001502

    Article  PubMed  Google Scholar 

  26. Rawle MJ, Davis D, Bendayan R, Wong A, Kuh D, Richards M (2018) Apolipoprotein-E (Apoe) ε4 and cognitive decline over the adult life course. Transl Psychiatry 8:18. https://doi.org/10.1038/s41398-017-0064-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Caselli RJ, Dueck AC, Osborne D, Sabbagh MN, Connor DJ, Ahern GL, Baxter LC, Rapcsak SZ, Shi J, Woodruff BK, Locke DEC, Snyder CH, Alexander GE, Rademakers R, Reiman EM (2009) Longitudinal modeling of age-related memory decline and the APOE epsilon4 effect. N Engl J Med 361:255–263. https://doi.org/10.1056/NEJMoa0809437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Soldan A, Pettigrew C, Lu Y, Wang M-C, Selnes O, Albert M, Brown T, Ratnanather JT, Younes L, Miller MI, BIOCARD Research Team (2015) Relationship of medial temporal lobe atrophy, APOE genotype, and cognitive reserve in preclinical Alzheimer’s disease. Hum Brain Mapp 36:2826–2841. https://doi.org/10.1002/hbm.22810

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hong YJ, Yoon B, Shim YS, Kim S-O, Kim HJ, Choi SH, Jeong JH, Yoon SJ, Yang DW, Lee J-H (2015) Predictors of clinical progression of subjective memory impairment in elderly subjects: data from the clinical research centers for dementia of South Korea (CREDOS). Dement Geriatr Cogn Disord 40:158–165. https://doi.org/10.1159/000430807

    Article  PubMed  Google Scholar 

  30. Jessen F, Wolfsgruber S, Wiese B, Bickel H, Mösch E, Kaduszkiewicz H, Pentzek M, Riedel-Heller SG, Luck T, Fuchs A, Weyerer S, Werle J, van den Bussche H, Scherer M, Maier W, Wagner M, German Study on Aging, Cognition and Dementia in Primary Care Patients (2014) AD dementia risk in late MCI, in early MCI, and in subjective memory impairment. Alzheimers Dement J Alzheimers Assoc 10:76–83. https://doi.org/10.1016/j.jalz.2012.09.017

    Article  Google Scholar 

  31. Kaup AR, Nettiksimmons J, Harris TB, Sink KM, Satterfield S, Metti AL, Ayonayon HN, Yaffe K (2015) Cognitive resilience to apolipoprotein E ε4: contributing factors in black and white older adults. JAMA Neurol 72:340–348. https://doi.org/10.1001/jamaneurol.2014.3978

    Article  PubMed  PubMed Central  Google Scholar 

  32. López ME, Turrero A, Delgado ML, Rodríguez-Rojo IC, Arrazola J, Barabash A, Maestú F, Fernández A (2017) APOE ε4 genotype and cognitive reserve effects on the cognitive functioning of healthy elders. Dement Geriatr Cogn Disord 44:328–342. https://doi.org/10.1159/000481852

    Article  CAS  PubMed  Google Scholar 

  33. Carlson MC, Helms MJ, Steffens DC, Burke JR, Potter GG, Plassman BL (2008) Midlife activity predicts risk of dementia in older male twin pairs. Alzheimers Dement J Alzheimers Assoc 4:324–331. https://doi.org/10.1016/j.jalz.2008.07.002

    Article  Google Scholar 

  34. Niti M, Yap K-B, Kua E-H, Tan C-H, Ng T-P (2008) Physical, social and productive leisure activities, cognitive decline and interaction with APOE-ε4 genotype Chinese older adults. Int Psychogeriatr 20:237–251. https://doi.org/10.1017/S1041610207006655

    Article  PubMed  Google Scholar 

  35. Wang H-X, Gustafson DR, Kivipelto M, Pedersen NL, Skoog I, Windblad B, Fratiglioni L (2012) Education halves the risk of dementia due to apolipoprotein ε4 allele: a collaborative study from the Swedish brain power initiative. Neurobiol Aging 33:1007.e1–1007.e7. https://doi.org/10.1016/j.neurobiolaging.2011.10.003

    Article  CAS  Google Scholar 

  36. Pettigrew C, Soldan A, Li S, Lu Y, Wang M-C, Selnes OA, Moghekar A, O’Brien R, Albert M, The Biocard Research Team null (2013) Relationship of cognitive reserve and APOE status to the emergence of clinical symptoms in preclinical Alzheimer’s disease. Cogn Neurosci 4:136–142. https://doi.org/10.1080/17588928.2013.831820

    Article  PubMed  Google Scholar 

  37. Ferrari C, Lombardi G, Polito C, Lucidi G, Bagnoli S, Piaceri I, Nacmias B, Berti V, Rizzuto D, Fratiglioni L, Sorbi S (2018) Alzheimer’s disease progression: factors influencing cognitive decline. J Alzheimers Dis JAD 61:785–791. https://doi.org/10.3233/JAD-170665

    Article  PubMed  Google Scholar 

  38. Arenaza-Urquijo EM, Gonneaud J, Fouquet M, Perrotin A, Mézenge F, Landeau B, Egret S, De la Sayette V, Desgranges B, Chételat G (2015) Interaction between years of education and APOE ε4 status on frontal and temporal metabolism. Neurology 85:1392–1399. https://doi.org/10.1212/WNL.0000000000002034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wirth M, Haase CM, Villeneuve S, Vogel J, Jagust WJ (2014) Neuroprotective pathways: lifestyle activity, brain pathology, and cognition in cognitively normal older adults. Neurobiol Aging 35:1873–1882. https://doi.org/10.1016/j.neurobiolaging.2014.02.015

    Article  PubMed  PubMed Central  Google Scholar 

  40. Crook TH, Feher EP, Larrabee GJ (1992) Assessment of memory complaint in age-associated memory impairment: the MAC-Q. Int Psychogeriatr 4:165–176

    Article  PubMed  Google Scholar 

  41. Lawton MP, Brody EM (1969) Assessment of Older people: self-maintaining and instrumental activities of daily living. The Gerontologist 9:179–186. https://doi.org/10.1093/geront/9.3_Part_1.179

    Article  CAS  PubMed  Google Scholar 

  42. Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund L-O, Nordberg A, Bäckman L, Albert M, Almkvist O, Arai H, Basun H, Blennow K, De Leon M, DeCarli C, Erkinjuntti T, Giacobini E, Graff C, Hardy J, Jack C, Jorm A, Ritchie K, Van Duijn C, Visser P, Petersen R c (2004) Mild cognitive impairment—beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 256:240–246. https://doi.org/10.1111/j.1365-2796.2004.01380.x

    Article  CAS  Google Scholar 

  43. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (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. Alzheimers Dement J Alzheimers Assoc 7:263–269. https://doi.org/10.1016/j.jalz.2011.03.005

    Article  Google Scholar 

  44. Román GC, Tatemichi TK, Erkinjuntti T, Cummings JL, Masdeu JC, Garcia JH, Amaducci L, Orgogozo JM, Brun A, Hofman A (1993) Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology 43:250–260

    Google Scholar 

  45. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller BL, Cummings J, Benson DF (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51:1546–1554

    Article  CAS  Google Scholar 

  46. Colombo L, Sartori G, Brivio C (2002) Stima del quoziente intellettivo tramite l’applicazione del TIB (test breve di intelligenza). G Ital Psicol. https://doi.org/10.1421/1256

    Article  Google Scholar 

  47. Nelson H (1982) National adult reading test (NART): for the assessment of premorbid intelligence in patients with dementia: test manual. NFER-Nelson, Windsor

    Google Scholar 

  48. Sorbi S, Nacmias B, Forleo P, Latorraca S, Gobbini I, Bracco L, Piacentini S, Amaducci L (1994) ApoE allele frequencies in Italian sporadic and familial Alzheimer’s disease. Neurosci Lett 177:100–102

    Article  CAS  PubMed  Google Scholar 

  49. Jorm AF, Mather KA, Butterworth P, Anstey KJ, Christensen H, Easteal S (2007) APOE genotype and cognitive functioning in a large age-stratified population sample. Neuropsychology 21:1–8. https://doi.org/10.1037/0894-4105.21.1.1

    Article  PubMed  Google Scholar 

  50. Casaletto KB, Cattie J, Franklin DR, Moore DJ, Woods SP, Grant I, Heaton RK (2014) The wide range achievement test-4 reading subtest “Holds” in HIV-infected individuals. J Clin Exp Neuropsychol 36:992–1001. https://doi.org/10.1080/13803395.2014.960370

    Article  PubMed  PubMed Central  Google Scholar 

  51. Green REA, Melo B, Christensen B, Ngo L-A, Monette G, Bradbury C (2008) Measuring premorbid IQ in traumatic brain injury: an examination of the validity of the Wechsler Test of Adult Reading (WTAR). J Clin Exp Neuropsychol 30:163–172. https://doi.org/10.1080/13803390701300524

    Article  PubMed  Google Scholar 

  52. Oliveira MO de, Nitrini R, Yassuda MS, Brucki SMD (2014) Vocabulary is an appropriate measure of premorbid intelligence in a sample with heterogeneous educational level in Brazil. In: Behav. Neurol. https://www.hindawi.com/journals/bn/2014/875960/. Accessed 29 May 2018

  53. Crawford JR, Deary IJ, Starr J, Whalley LJ (2001) The NART as an index of prior intellectual functioning: a retrospective validity study covering a 66-year interval. Psychol Med 31:451–458

    Article  CAS  PubMed  Google Scholar 

  54. McGurn B, Starr JM, Topfer JA, Pattie A, Whiteman MC, Lemmon HA, Whalley LJ, Deary IJ (2004) Pronunciation of irregular words is preserved in dementia, validating premorbid IQ estimation. Neurology 62:1184–1186

    Article  CAS  PubMed  Google Scholar 

  55. Stewart R, Godin O, Crivello F, Maillard P, Mazoyer B, Tzourio C, Dufouil C (2011) Longitudinal neuroimaging correlates of subjective memory impairment: 4-year prospective community study. Br J Psychiatry J Ment Sci 198:199–205. https://doi.org/10.1192/bjp.bp.110.078683

    Article  Google Scholar 

  56. Derouesné C, Dealberto MJ, Boyer P, Lubin S, Sauron B, Piette F, Kohler F, Alpérovitch A (1993) Empirical evaluation of the “Cognitive Difficulties Scale” for assessment of memory complaints in general practice: a study of 1628 cognitively normal subjects aged 45–75 years. Int J Geriatr Psychiatry 8:599–607. https://doi.org/10.1002/gps.930080712

    Article  Google Scholar 

  57. Vemuri P, Lesnick TG, Przybelski SA, Machulda M, Knopman DS, Mielke MM, Roberts RO, Geda YE, Rocca WA, Petersen RC, Jack CR (2014) Association of lifetime intellectual enrichment with cognitive decline in the older population. JAMA Neurol 71:1017–1024. https://doi.org/10.1001/jamaneurol.2014.963

    Article  PubMed  PubMed Central  Google Scholar 

  58. Guerreiro R, Bras J (2015) The age factor in Alzheimer’s disease. Genome Med. https://doi.org/10.1186/s13073-015-0232-5

    Article  PubMed  PubMed Central  Google Scholar 

  59. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science 261:921–923

    Article  CAS  PubMed  Google Scholar 

  60. Soldan A, Pettigrew C, Wang M-C, Li S, Lu Y, Albert M, Selnes O (2013) Relationship of cognitive reserve and APOE status to clinical symptom onset of mild cognitive impairment: the BIOCARD Cohort. Alzheimers Dement J Alzheimers Assoc 9:P134. https://doi.org/10.1016/j.jalz.2013.04.072

    Article  Google Scholar 

  61. Arenaza-Urquijo EM, Wirth M, Chételat G (2015) Cognitive reserve and lifestyle: moving towards preclinical Alzheimer’s disease. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2015.00134

    Article  PubMed  PubMed Central  Google Scholar 

  62. Wu L, Zhao L (2016) ApoE2 and Alzheimer’s disease: time to take a closer look. Neural Regen Res 11:412–413. https://doi.org/10.4103/1673-5374.179044

    Article  PubMed  PubMed Central  Google Scholar 

  63. Roselli F, Tartaglione B, Federico F, Lepore V, Defazio G, Livrea P (2009) Rate of MMSE score change in Alzheimer’s disease: influence of education and vascular risk factors. Clin Neurol Neurosurg 111:327–330. https://doi.org/10.1016/j.clineuro.2008.10.006

    Article  PubMed  Google Scholar 

  64. Scarmeas N, Albert SM, Manly JJ, Stern Y (2006) Education and rates of cognitive decline in incident Alzheimer’s disease. J Neurol Neurosurg Psychiatry 77:308–316. https://doi.org/10.1136/jnnp.2005.072306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. de Oliveira IR, Seixas C, Osório FL, Crippa JAS, de Abreu JN, Menezes IG, Pidgeon A, Sudak D, Wenzel A (2015) Evaluation of the psychometric properties of the cognitive distortions Questionnaire (CD-Quest) in a sample of undergraduate students. Innov Clin Neurosci 12:20–27

    PubMed  PubMed Central  Google Scholar 

  66. Bracco L, Piccini C, Baccini M, Bessi V, Biancucci F, Nacmias B, Bagnoli S, Sorbi S (2007) Pattern and progression of cognitive decline in Alzheimer’s disease: role of premorbid intelligence and ApoE genotype. Dement Geriatr Cogn Disord 24:483–491. https://doi.org/10.1159/000111081

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was funded by Ministero della Salute and Regione Toscana (Grants n° GR-2010-2316359—Longitudinal clinical–neuropsychological study of subjective memory complaints).

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Correspondence to Valentina Bessi.

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All procedures involving experiments on human subjects have been done in accordance with the ethical standards of the Committee on Human Experimentation of the institution in which the experiments were done or in accordance with the Helsinki Declaration of 1975. Specific national laws have been observed.

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Mazzeo, S., Padiglioni, S., Bagnoli, S. et al. The dual role of cognitive reserve in subjective cognitive decline and mild cognitive impairment: a 7-year follow-up study. J Neurol 266, 487–497 (2019). https://doi.org/10.1007/s00415-018-9164-5

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