Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T01:47:43.822Z Has data issue: false hasContentIssue false
  • English
  • Français

The trajectory of cognitive decline in the pre-dementia phase in memory clinic visitors: findings from the 4C-MCI study

Published online by Cambridge University Press:  19 November 2014

R. Hamel ,
S. Köhler ,
N. Sistermans ,
T. Koene ,
Y. Pijnenburg ,
W. van der Flier ,
P. Scheltens ,
P. Aalten ,
F. Verhey  and
P. J. Visser
...Show all authors
R. Hamel*
Affiliation:
Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, Maastricht, The Netherlands
S. Köhler
Affiliation:
Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, Maastricht, The Netherlands
N. Sistermans
Affiliation:
Department of Neurology and Neuroscience Campus Amsterdam, VUmc Alzheimer Centre, VUmc Medical Centre, Amsterdam, The Netherlands
T. Koene
Affiliation:
Department of Medical Psychology and Neuroscience Campus Amsterdam, VUmc Alzheimer Centre, VUmc Medical Centre, Amsterdam, The Netherlands
Y. Pijnenburg
Affiliation:
Department of Neurology and Neuroscience Campus Amsterdam, VUmc Alzheimer Centre, VUmc Medical Centre, Amsterdam, The Netherlands
W. van der Flier
Affiliation:
Department of Neurology and Neuroscience Campus Amsterdam, VUmc Alzheimer Centre, VUmc Medical Centre, Amsterdam, The Netherlands Department of Epidemiology & Biostatistics, VUmc Medical Centre, Amsterdam, The Netherlands
P. Scheltens
Affiliation:
Department of Neurology and Neuroscience Campus Amsterdam, VUmc Alzheimer Centre, VUmc Medical Centre, Amsterdam, The Netherlands
P. Aalten
Affiliation:
Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, Maastricht, The Netherlands
F. Verhey
Affiliation:
Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, Maastricht, The Netherlands
P. J. Visser
Affiliation:
Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, Maastricht, The Netherlands Department of Neurology and Neuroscience Campus Amsterdam, VUmc Alzheimer Centre, VUmc Medical Centre, Amsterdam, The Netherlands
I. Ramakers
Affiliation:
Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, Maastricht, The Netherlands
*
* Address for correspondence: R. Hamel, M.Sc., Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University Medical Centre, PO Box 616 (DRT 12), 6200 MD Maastricht, The Netherlands. (Email: r.hamel@maastrichtuniversity.nl)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

We investigated the course of decline in multiple cognitive domains in non-demented subjects from a memory clinic setting, and compared pattern, onset and magnitude of decline between subjects who progressed to Alzheimer's disease (AD) dementia at follow-up and subjects who did not progress.

Method

In this retrospective cohort study 819 consecutive non-demented patients who visited the memory clinics in Maastricht or Amsterdam between 1987 and 2010 were followed until they became demented or for a maximum of 10 years (range 0.5–10 years). Differences in trajectories of episodic memory, executive functioning, verbal fluency, and information processing speed/attention between converters to AD dementia and subjects remaining non-demented were compared by means of random effects modelling.

Results

The cognitive performance of converters and non-converters could already be differentiated seven (episodic memory) to three (verbal fluency and executive functioning) years prior to dementia diagnosis. Converters declined in these three domains, while non-converters remained stable on episodic memory and executive functioning and showed modest decline in verbal fluency. There was no evidence of decline in information processing speed/attention in either group.

Conclusions

Differences in cognitive performance between converters to AD dementia and subjects remaining non-demented could be established 7 years prior to diagnosis for episodic memory, with verbal fluency and executive functioning following several years later. Therefore, in addition to early episodic memory decline, decline in executive functions may also flag incident AD dementia. By contrast, change in information processing speed/attention seems less informative.

Keywords

Alzheimer's diseasecognitioncohort studyneuropsychology
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 7 , May 2015 , pp. 1509 - 1519
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albert, M, Blacker, D, Moss, MB, Tanzi, R, McArdle, JJ (2007). Longitudinal change in cognitive performance among individuals with mild cognitive impairment. Neuropsychology 21, 158–169.CrossRefGoogle ScholarPubMed
Albert, MS, Moss, MB, Tanzi, R, Jones, K (2001). Preclinical prediction of AD using neuropsychological tests. Journal of the International Neuropsychological Society 7, 631–639.CrossRefGoogle ScholarPubMed
Amieva, H, Jacqmin-Gadda, H, Orgogozo, JM, Le Carret, N, Helmer, C, Letenneur, L, Barberger-Gateau, P, Fabrigoule, C, Dartigues, JF (2005). The 9 year cognitive decline before dementia of the Alzheimer type: a prospective population-based study. Brain 128, 1093–1101.CrossRefGoogle ScholarPubMed
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association: Washington, DC.Google Scholar
Auriacombe, S, Fabrigoule, C, Lafont, S, Jacqmin-Gadda, H, Dartigues, JF (2001). Letter and cateogry fluency in normal elderly participants: a population-based study. Aging, Neuropsychology and Cognition 8, 98–108.CrossRefGoogle Scholar
Backman, L, Small, BJ (1998). Influences of cognitive support on episodic remembering: tracing the process of loss from normal aging to Alzheimer's disease. Psychology and Aging 13, 267–276.CrossRefGoogle ScholarPubMed
Backman, L, Small, BJ, Fratiglioni, L (2001). Stability of the preclinical episodic memory deficit in Alzheimer's disease. Brain 124, 96–102.CrossRefGoogle ScholarPubMed
Bunce, D, Batterham, PJ, Mackinnon, AJ, Christensen, H (2012). Depression, anxiety and cognition in community-dwelling adults aged 70 years and over. Journal of Psychiatric Research 46, 1662–1666.CrossRefGoogle ScholarPubMed
Burgmans, S, van Boxtel, MP, Smeets, F, Vuurman, EF, Gronenschild, EH, Verhey, FR, Uylings, HB, Jolles, J (2009). Prefrontal cortex atrophy predicts dementia over a six-year period. Neurobiology of Aging 30, 1413–1419.CrossRefGoogle Scholar
Cerhan, JH, Ivnik, RJ, Smith, GE, Machulda, MM, Boeve, BF, Knopman, DS, Petersen, RC, Tangalos, EG (2007). Alzheimer's disease patients’ cognitive status and course years prior to symptom recognition. Aging, Neuropsychology, and Cognition 14, 227–235.CrossRefGoogle ScholarPubMed
Chen, P, Ratcliff, G, Belle, SH, Cauley, JA, DeKosky, ST, Ganguli, M (2000). Cognitive tests that best discriminate between presymptomatic AD and those who remain nondemented. Neurology 55, 1847–1853.CrossRefGoogle ScholarPubMed
Chen, P, Ratcliff, G, Belle, SH, Cauley, JA, DeKosky, ST, Ganguli, M (2001). Patterns of cognitive decline in presymptomatic Alzheimer disease: a prospective community study. Archives of General Psychiatry 58, 853–858.CrossRefGoogle ScholarPubMed
Clark, LJ, Gatz, M, Zheng, L, Chen, YL, McCleary, C, Mack, WJ (2009). Longitudinal verbal fluency in normal aging, preclinical, and prevalent Alzheimer's disease. American Journal of Alzheimer's Disease and Other Dementias 24, 461–468.CrossRefGoogle ScholarPubMed
Crossley, M, D'Arcy, C, Rawson, NS (1997). Letter and category fluency in community-dwelling Canadian seniors: a comparison of normal participants to those with dementia of the Alzheimer or vascular type. Journal of Clinical and Experimental Neuropsychology 19, 52–62.CrossRefGoogle ScholarPubMed
Fabrigoule, C, Rouch, I, Taberly, A, Letenneur, L, Commenges, D, Mazaux, JM, Orgogozo, JM, Dartigues, JF (1998). Cognitive process in preclinical phase of dementia. Brain 121(Pt 1), 135–141.CrossRefGoogle ScholarPubMed
Ferrer, E, Salthouse, TA, Stewart, WF, Schwartz, BS (2004). Modeling age and retest processes in longitudinal studies of cognitive abilities. Psychology and Aging 19, 243–259.CrossRefGoogle ScholarPubMed
Fox, NC, Warrington, EK, Seiffer, AL, Agnew, SK, Rossor, MN (1998). Presymptomatic cognitive deficits in individuals at risk of familial Alzheimer's disease. A longitudinal prospective study. Brain 121(Pt 9), 1631–1639.CrossRefGoogle ScholarPubMed
Galvin, JE, Powlishta, KK, Wilkins, K, McKeel, DW Jr., Xiong, C, Grant, E, Storandt, M, Morris, JC (2005). Predictors of preclinical Alzheimer disease and dementia: a clinicopathologic study. Archives of Neurology 62, 758–765.CrossRefGoogle ScholarPubMed
Grober, E, Hall, CB, Lipton, RB, Zonderman, AB, Resnick, SM, Kawas, C (2008). Memory impairment, executive dysfunction, and intellectual decline in preclinical Alzheimer's disease. Journal of the International Neuropsychological Society 14, 266–278.CrossRefGoogle ScholarPubMed
Hammes, J (1973). De Stroop Kleur-Woord Test: Handleiding [The Stroop Color-Word Test: Manual]. Swets & Zeitlinger: Amsterdam.Google Scholar
Hanninen, T, Hallikainen, M, Koivisto, K, Helkala, EL, Reinikainen, KJ, Soininen, H, Mykkanen, L, Laakso, M, Pyorala, K, Riekkinen, PJ Sr. (1995). A follow-up study of age-associated memory impairment: neuropsychological predictors of dementia. Journal of the American Geriatrics Society 43, 1007–1015.CrossRefGoogle ScholarPubMed
Jack, CR Jr., Knopman, DS, Jagust, WJ, Shaw, LM, Aisen, PS, Weiner, MW, Petersen, RC, Trojanowski, JQ (2010). Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurology 9, 119–128.CrossRefGoogle ScholarPubMed
Jacobs, HI, Van Boxtel, MP, Uylings, HB, Gronenschild, EH, Verhey, FR, Jolles, J (2011). Atrophy of the parietal lobe in preclinical dementia. Brain and Cognition 75, 154–163.CrossRefGoogle ScholarPubMed
Johnson, DK, Storandt, M, Morris, JC, Galvin, JE (2009). Longitudinal study of the transition from healthy aging to Alzheimer disease. Archives of Neurology 66, 1254–1259.CrossRefGoogle ScholarPubMed
Laukka, EJ, Jones, S, Small, BJ, Fratiglioni, L, Backman, L (2004). Similar patterns of cognitive deficits in the preclinical phases of vascular dementia and Alzheimer's disease. Journal of the International Neuropsychological Society 10, 382–391.CrossRefGoogle ScholarPubMed
Laukka, EJ, Macdonald, SW, Fratiglioni, L, Backman, L (2012). Preclinical cognitive trajectories differ for Alzheimer's disease and vascular dementia. Journal of the International Neuropsychological Society 18, 191–199.CrossRefGoogle ScholarPubMed
Lezak, MD, Howieson, DB, Loring, DW (2004). Neuropsychological Assessment, 4th edn. Oxford University Press: Oxford, UK.Google Scholar
Linn, RT, Wolf, PA, Bachman, DL, Knoefel, JE, Cobb, JL, Belanger, AJ, Kaplan, EF, D'Agostino, RB (1995). The ‘preclinical phase’ of probable Alzheimer's disease. A 13-year prospective study of the Framingham cohort. Archives of Neurology 52, 485–490.CrossRefGoogle ScholarPubMed
Luteijn, F, Barelds, DPH (2004). Groninger Intelligentie Test 2 Handleiding [Groninger Intelligence Test 2 Manual]. Harcourt Assessment BV: Amsterdam.Google Scholar
Machulda, MM, Pankratz, VS, Christianson, TJ, Ivnik, RJ, Mielke, MM, Roberts, RO, Knopman, DS, Boeve, BF, Petersen, RC (2013). Practice effects and longitudinal cognitive change in normal aging vs. incident mild cognitive impairment and dementia in the Mayo Clinic Study of Aging. The Clinical Neuropsychologist 27, 1247–1264.CrossRefGoogle ScholarPubMed
McKeith, IG, Dickson, DW, Lowe, J, Emre, M, O'Brien, JT, Feldman, H, Cummings, J, Duda, JE, Lippa, C, Perry, EK, Aarsland, D, Arai, H, Ballard, CG, Boeve, B, Burn, DJ, Costa, D, Del Ser, T, Dubois, B, Galasko, D, Gauthier, S, Goetz, CG, Gomez-Tortosa, E, Halliday, G, Hansen, LA, Hardy, J, Iwatsubo, T, Kalaria, RN, Kaufer, D, Kenny, RA, Korczyn, A, Kosaka, K, Lee, VM, Lees, A, Litvan, I, Londos, E, Lopez, OL, Minoshima, S, Mizuno, Y, Molina, JA, Mukaetova-Ladinska, EB, Pasquier, F, Perry, RH, Schulz, JB, Trojanowski, JQ, Yamada, M (2005). Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65, 1863–1872.CrossRefGoogle ScholarPubMed
McKhann, G, Drachman, D, Folstein, M, Katzman, R, Price, D, Stadlan, EM (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, 939–944.CrossRefGoogle ScholarPubMed
Mitchell, AJ, Shiri-Feshki, M (2009). Rate of progression of mild cognitive impairment to dementia – meta-analysis of 41 robust inception cohort studies. Acta Psychiatrica Scandinavica 119, 252–265.CrossRefGoogle ScholarPubMed
Mitrushina, M, Satz, P (1991). Effect of repeated administration of a neuropsychological battery in the elderly. Journal of Clinical Psychology 47, 790–801.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Mungas, D, Beckett, L, Harvey, D, Farias, ST, Reed, B, Carmichael, O, Olichney, J, Miller, J, DeCarli, C (2010). Heterogeneity of cognitive trajectories in diverse older persons. Psychology and Aging 25, 606–619.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nielsen, H, Lolk, A, Andersen, K, Andersen, J, Kragh-Sorensen, P (1999). Characteristics of elderly who develop Alzheimer's disease during the next two years-a neuropsychological study using CAMCOG. The Odense Study. International Journal of Geriatric Psychiatry 14, 957–963.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
O'Brien, JT, Erkinjuntti, T, Reisberg, B, Roman, G, Sawada, T, Pantoni, L, Bowler, JV, Ballard, C, DeCarli, C, Gorelick, PB, Rockwood, K, Burns, A, Gauthier, S, DeKosky, ST (2003). Vascular cognitive impairment. Lancet Neurology 2, 89–98.CrossRefGoogle ScholarPubMed
Petersen, RC, Smith, GE, Waring, SC, Ivnik, RJ, Tangalos, EG, Kokmen, E (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology 56, 303–308.CrossRefGoogle ScholarPubMed
Raoux, N, Amieva, H, Le Goff, M, Auriacombe, S, Carcaillon, L, Letenneur, L, Dartigues, JF (2008). Clustering and switching processes in semantic verbal fluency in the course of Alzheimer's disease subjects: results from the PAQUID longitudinal study. Cortex 44, 1188–1196.CrossRefGoogle ScholarPubMed
Rapp, MA, Reischies, FM (2005). Attention and executive control predict Alzheimer disease in late life: results from the Berlin Aging Study (BASE). American Journal of Geriatric Psychiatry 13, 134–141.CrossRefGoogle ScholarPubMed
Ridha, BH, Barnes, J, Bartlett, JW, Godbolt, A, Pepple, T, Rossor, MN, Fox, NC (2006). Tracking atrophy progression in familial Alzheimer's disease: a serial MRI study. Lancet Neurology 5, 828–834.CrossRefGoogle ScholarPubMed
Roman, GC, Tatemichi, TK, Erkinjuntti, T, Cummings, JL, Masdeu, JC, Garcia, JH, Amaducci, L, Orgogozo, JM, Brun, A, Hofman, A, Moody, DM, O’Brien, MD, Yamaguchi, T, Grafman, J, Drayer, BP, Bennett, DA, Fisher, M, Ogata, J, Kokmen, E, Bermejo, F, Wolf, PA, Gorelick, PB, Bick, KL, Pajeau, AK, Bell, MA, DeCarli, C, Culebras, A, Korczyn, AD, Bogousslavsky, J, Hartmann, A, Scheinberg, P (1993). Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology 43, 250–260.CrossRefGoogle ScholarPubMed
Rubin, EH, Storandt, M, Miller, JP, Kinscherf, DA, Grant, EA, Morris, JC, Berg, L (1998). A prospective study of cognitive function and onset of dementia in cognitively healthy elders. Archives of Neurology 55, 395–401.CrossRefGoogle ScholarPubMed
Schmand, B, Houx, P, de Koning, I (2003). Normen voor Stroop kleur-woord tests, Trail Making test en Story Recall van de Rivermead Behavioural Memory Test. [Norms for Stroop color-word tests, Trail Making Test and Story Recall of the Rivermead Behavioural Memory Test]. Nederlands Instituut van Psychologen, Sectie Neuropsychologie: Amsterdam.Google Scholar
Silva, D, Guerreiro, M, Santana, I, Rodrigues, A, Cardoso, S, Maroco, J, de Mendonca, A (2013). Prediction of long-term (5 years) conversion to dementia using neuropsychological tests in a memory clinic setting. Journal of Alzheimer's Disease 34, 681–689.CrossRefGoogle Scholar
Sluimer, JD, van der Flier, WM, Karas, GB, van Schijndel, R, Barnes, J, Boyes, RG, Cover, KS, Olabarriaga, SD, Fox, NC, Scheltens, P, Vrenken, H, Barkhof, F (2009). Accelerating regional atrophy rates in the progression from normal aging to Alzheimer's disease. European Radiology 19, 2826–2833.CrossRefGoogle ScholarPubMed
Tabert, MH, Manly, JJ, Liu, X, Pelton, GH, Rosenblum, S, Jacobs, M, Zamora, D, Goodkind, M, Bell, K, Stern, Y, Devanand, DP (2006). Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Archives of General Psychiatry 63, 916–924.CrossRefGoogle ScholarPubMed
Thorvaldsson, V, Macdonald, SW, Fratiglioni, L, Winblad, B, Kivipelto, M, Laukka, EJ, Skoog, I, Sacuiu, S, Guo, X, Ostling, S, Borjesson-Hanson, A, Gustafson, D, Johansson, B, Backman, L (2011). Onset and rate of cognitive change before dementia diagnosis: findings from two Swedish population-based longitudinal studies. Journal of the International Neuropsychological Society 17, 154–162.CrossRefGoogle ScholarPubMed
Van der Elst, W, van Boxtel, MP, van Breukelen, GJ, Jolles, J (2005). Rey's verbal learning test: normative data for 1855 healthy participants aged 24–81 years and the influence of age, sex, education, and mode of presentation. Journal of the International Neuropsychological Society 11, 290–302.CrossRefGoogle ScholarPubMed
Van der Elst, W, Van Boxtel, MP, Van Breukelen, GJ, Jolles, J (2006 a). Normative data for the Animal, Profession and Letter M Naming verbal fluency tests for Dutch speaking participants and the effects of age, education, and sex. Journal of the International Neuropsychological Society 12, 80–89.CrossRefGoogle Scholar
Van der Elst, W, Van Boxtel, MP, Van Breukelen, GJ, Jolles, J (2006 b). The Stroop color-word test: influence of age, sex, and education; and normative data for a large sample across the adult age range. Assessment 13, 62–79.CrossRefGoogle ScholarPubMed
van der Flier, WM, Pijnenburg, YA, Prins, N, Lemstra, AW, Bouwman, FH, Teunissen, CE, van Berckel, BN, Stam, CJ, Barkhof, F, Visser, PJ, van Egmond, E, Scheltens, P (2014). Optimizing patient care and research: the amsterdam dementia cohort. Journal of Alzheimer's Disease 41, 313–327.CrossRefGoogle ScholarPubMed
van Harten, AC, Smits, LL, Teunissen, CE, Visser, PJ, Koene, T, Blankenstein, MA, Scheltens, P, van der Flier, WM (2013). Preclinical AD predicts decline in memory and executive functions in subjective complaints. Neurology 81, 1409–1416.CrossRefGoogle ScholarPubMed
Wilson, RS, Beckett, LA, Bennett, DA, Albert, MS, Evans, DA (1999). Change in cognitive function in older persons from a community population: relation to age and Alzheimer disease. Archives of Neurology 56, 1274–1279.CrossRefGoogle ScholarPubMed
Wilson, RS, Leurgans, SE, Boyle, PA, Bennett, DA (2011). Cognitive decline in prodromal Alzheimer disease and mild cognitive impairment. Archives of Neurology 68, 351–356.CrossRefGoogle ScholarPubMed