Smaller medial temporal lobe volumes in individuals with subjective cognitive decline and biomarker evidence of Alzheimer's disease-Data from three memory clinic studies.
Hu, Xiaochen; Teunissen, Charlotte E; Spottke, Annikaet al.
2019 • In Alzheimer's and Dementia: the Journal of the Alzheimer's Association, 15 (2), p. 185 - 193
AD biomarkers; Alzheimer's disease; Medial temporal lobe; Subjective cognitive decline; Amyloid beta-Peptides; Biomarkers; tau Proteins; Aged; Aged, 80 and over; Alzheimer Disease/pathology; Amyloid beta-Peptides/cerebrospinal fluid; Biomarkers/cerebrospinal fluid; Cognitive Dysfunction/pathology; Female; Germany; Humans; Male; Middle Aged; Netherlands; Neuropsychological Tests; Spain; Temporal Lobe/pathology; tau Proteins/cerebrospinal fluid; Cognitive Dysfunction; Temporal Lobe; Epidemiology; Health Policy; Developmental Neuroscience; Neurology (clinical); Geriatrics and Gerontology; Cellular and Molecular Neuroscience; Psychiatry and Mental Health
Abstract :
[en] INTRODUCTION: Previous studies showed associations of brain volume differences and biomarker evidence for Alzheimer's disease (AD) in subjective cognitive decline (SCD). The consistency of this finding across SCD studies has not been investigated.
METHODS: We studied gray matter volume differences between SCD subjects with and without cerebrospinal fluid biomarker evidence for AD across three European memory clinic samples (German Center for Neurodegenerative Diseases Longitudinal Cognitive Impairment and Dementia study, Amsterdam, Barcelona). Analysis of covariance models with samples and cerebrospinal fluid biomarkers as between-subject factors were calculated.
RESULTS: A significant main effect for AD biomarker (Aβ42- > Aβ42+) in the left medial temporal lobe (MTL) was found, with the absence of main effects for sample or interaction effects between AD biomarker and sample. This indicates consistent lower left MTL volume across three samples in SCD subjects with abnormal Aβ42 levels.
DISCUSSION: Our results support the model that in the presence of AD pathology, SCD corresponds to the late preclinical stage (stage 2 of AD) with smaller MTL volumes.
Disciplines :
Neurology
Author, co-author :
Hu, Xiaochen; Department of Psychiatry and Psychotherapy, Medical Faculty, University of Cologne, Cologne, Germany. Electronic address: xiaochen.hu@uk-koeln.de
Teunissen, Charlotte E; Neurochemistry lab and Biobank, Department of Clinical Chemistry, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands
Spottke, Annika; German Center for Neurodegenerative Disorder (DZNE), Bonn, Germany, Department of Neurology, University Hospital of Bonn, Bonn, Germany
HENEKA, Michael ; German Center for Neurodegenerative Disorder (DZNE), Bonn, Germany, Department of Neurodegeneration Diseases and Geriatric Psychiatry, University Hospital of Bonn, Bonn, Germany
Düzel, Emrah; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany, Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, Magdeburg, Germany
Peters, Oliver; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany, Department of Psychiatry, Charité Berlin, Berlin, Germany
Li, Siyao; Department of Psychiatry, Charité Berlin, Berlin, Germany
Priller, Josef; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany, Department of Neuropsychiatry, Charité Berlin & Berlin Institute of Health, Berlin, Germany
Buerger, Katharina; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany, Institute for Stroke and Dementia Research, Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich, Germany
Teipel, Stefan; German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany, Department of Psychosomatic Medicine, University Hospital of Rostock, Rostock, Germany
Laske, Christoph; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany
Verfaillie, Sander C J; Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands, Department of Radiology and Nuclear Medicine, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands
Barkhof, Frederik; Department of Radiology and Nuclear Medicine, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands, Institutes of Neurology and Healthcare Engineering, University College London, London, United Kingdom
Coll-Padrós, Nina; Alzheimer's disease and other cognitive disorder Unit, Institut d'Investigacions Biomediques August Pi l Sunyer (IDIBAPS), Hospital Clinic, Barcelona, Spain
Rami, Lorena; Alzheimer's disease and other cognitive disorder Unit, Institut d'Investigacions Biomediques August Pi l Sunyer (IDIBAPS), Hospital Clinic, Barcelona, Spain
Molinuevo, Jose Luis; Alzheimer's disease and other cognitive disorder Unit, Institut d'Investigacions Biomediques August Pi l Sunyer (IDIBAPS), Hospital Clinic, Barcelona, Spain, BarcelonaBeta Brain Research Center, Fundació Pasqual Maragall, Barcelona, Spain
van der Flier, Wiesje M; Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands
Jessen, Frank; Department of Psychiatry and Psychotherapy, Medical Faculty, University of Cologne, Cologne, Germany, German Center for Neurodegenerative Disorder (DZNE), Bonn, Germany
Smaller medial temporal lobe volumes in individuals with subjective cognitive decline and biomarker evidence of Alzheimer's disease-Data from three memory clinic studies.
Publication date :
February 2019
Journal title :
Alzheimer's and Dementia: the Journal of the Alzheimer's Association
EU Joint Programme – Neurodegenerative Disease Research
Funding text :
This work was supported by an EU Joint Program—Neurodegenerative Disease Research (JPND) project. The project is supported through the following funding organizations under the aegis of JPND (www.jpnd.eu): Germany, Bundesministerium für Bildung und Forschung (BMBF grant number: 01ED1508); the Netherlands, The Netherlands Organisation for Health Research and Development; Spain, Instituto De Salud Carlos III. This research was also supported by the German Research Council (DFG; grant number: JE 2707/7-1) and the German Center for Neurodegenerative Diseases (Deutsches Zentrum für Neurodegenerative Erkrankungen, DZNE), reference number BN012 (DELCODE). W.v.d.F. is a recipient of a research grant on subjective cognitive decline (SCIENCe project: Gieskes Strijbis fonds). F.B. is supported by the NIHR UCLH Biomedical Research Centre.This work was supported by an EU Joint Program?Neurodegenerative Disease Research (JPND) project. The project is supported through the following funding organizations under the aegis of JPND (www.jpnd.eu): Germany, Bundesministerium f?r Bildung und Forschung (BMBF grant number: 01ED1508); the Netherlands, The Netherlands Organisation for Health Research and Development; Spain, Instituto De Salud Carlos III. This research was also supported by the German Research Council (DFG; grant number: JE 2707/7-1) and the German Center for Neurodegenerative Diseases (Deutsches Zentrum f?r Neurodegenerative Erkrankungen, DZNE), reference number BN012 (DELCODE). W.v.d.F. is a recipient of a research grant on subjective cognitive decline (SCIENCe project: Gieskes Strijbis fonds). F.B. is supported by the NIHR UCLH Biomedical Research Centre.This work was supported by an EU Joint Program—Neurodegenerative Disease Research (JPND) project. The project is supported through the following funding organizations under the aegis of JPND ( www.jpnd.eu ): Germany, Bundesministerium für Bildung und Forschung (BMBF grant number: 01ED1508 ); the Netherlands, The Netherlands Organisation for Health Research and Development ; Spain, Instituto De Salud Carlos III . This research was also supported by the German Research Council ( DFG ; grant number: JE 2707/7-1 ) and the German Center for Neurodegenerative Diseases ( Deutsches Zentrum für Neurodegenerative Erkrankungen , DZNE), reference number BN012 (DELCODE). W.v.d.F. is a recipient of a research grant on subjective cognitive decline (SCIENCe project: Gieskes Strijbis fonds). F.B. is supported by the NIHR UCLH Biomedical Research Centre.
Doody, R.S., Thomas, R.G., Farlow, M., Iwatsubo, T., Vellas, B., Joffe, S., et al. Phase 3 trials of solanezumab for mild-to-moderate Alzheimer's disease. N Engl J Med 370 (2014), 311–321.
Salloway, S., Sperling, R., Fox, N.C., Blennow, K., Klunk, W., Raskind, M., et al. Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N Engl J Med 370 (2014), 322–333.
Mitchell, A.J., Beaumont, H., Ferguson, D., Yadegarfar, M., Stubbs, B., Risk of dementia and mild cognitive impairment in older people with subjective memory complaints: meta-analysis. Acta Psychiatr Scand 130 (2014), 439–451.
Jessen, F., Wiese, B., Bachmann, C., Eifflaender-Gorfer, S., Haller, F., Kölsch, H., et al. Prediction of dementia by subjective memory impairment. Arch Gen Psychiatry 67 (2010), 414–422.
Reisberg, B., Shulman, M.B., Torossian, C., Leng, L., Zhu, W., Outcome over seven years of healthy adults with and without subjective cognitive impairment. Alzheimers Dement 6 (2010), 11–24.
Rodda, J., Okello, A., Edison, P., Dannhauser, T., Brooks, D.J., Walker, Z., (11)C-PIB PET in subjective cognitive impairment. Eur Psychiatry 25 (2010), 123–125.
Perrotin, A., Mormino, E., Madison, C.M., Hayenga, A.O., Jagust, W.J., Subjective cognition and amyloid deposition imaging. Arch Neurol 69 (2012), 223–229.
Snitz, B.E., Lopez, O.L., McDade, E., Becker, J.T., Cohen, A.D., Price, J.C., et al. Amyloid-beta Imaging in Older Adults Presenting to a Memory Clinic with Subjective Cognitive Decline: A Pilot Study. J Alzheimers Dis 48 (2015), S151–S159.
Vogel, J.W., Varga Dolezalova, M., La Joie, R., Marks, S.M., Schwimmer, H.D., Landau, S.M., et al. Subjective cognitive decline and β-amyloid burden predict cognitive change in healthy elderly. Neurology 89 (2017), 2002–2009.
Buckley, R.F., Hanseeuw, B., Schultz, A.P., Vannini, P., Aghjayan, S.L., Properzi, M.J., et al. Region-Specific Association of Subjective Cognitive Decline With Tauopathy Independent of Global beta-Amyloid Burden. JAMA Neurol 74 (2017), 1455–1463.
Mosconi, L., De Santi, S., Brys, M., Tsui, W.H., Pirraglia, E., Glodzik-Sobanska, L., et al. Hypometabolism and altered cerebrospinal fluid markers in normal Apolipoprotein E E4 carriers with subjective memory complaints. Biol Psychiatry 63 (2008), 609–618.
Scheef, L., Spottke, A., Daerr, M., Joe, A., Striepens, N., Kölsch, H., et al. Glucose metabolism, gray matter structure, and memory decline in subjective memory impairment. Neurology 79 (2012), 1332–1339.
Jessen, F., Feyen, L., Freymann, K., Tepest, R., Maier, W., Heun, R., et al. Volume reduction of the entorhinal cortex in subjective memory impairment. Neurobiol Aging 27 (2006), 1751–1756.
Perrotin, A., de Flores, R., Lamberton, F., Poisnel, G., La Joie, R., de la Sayette, V., et al. Hippocampal Subfield Volumetry and 3D Surface Mapping in Subjective Cognitive Decline. J Alzheimers Dis 48 (2015), S141–S150.
Saykin, A.J., Wishart, H.A., Rabin, L.A., Santulli, R.B., Flashman, L.A., West, J.D., et al. Older adults with cognitive complaints show brain atrophy similar to that of amnestic MCI. Neurology 67 (2006), 834–842.
Erk, S., Spottke, A., Meisen, A., Wagner, M., Walter, H., Jessen, F., Evidence of neuronal compensation during episodic memory in subjective memory impairment. Arch Gen Psychiatry 68 (2011), 845–852.
Hu, X., Uhle, F., Fliessbach, K., Wagner, M., Han, Y., Weber, B., et al. Reduced future-oriented decision making in individuals with subjective cognitive decline: A functional MRI study. Alzheimers Dement (Amst) 6 (2017), 222–231.
Jessen, F., Amariglio, R.E., van Boxtel, M., Breteler, M., Ceccaldi, M., Chételat, G., et al. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer's disease. Alzheimers Dement 10 (2014), 844–852.
Smart, C.M., Segalowitz, S.J., Mulligan, B.P., Koudys, J., Gawryluk, J.R., Mindfulness training for older adults with subjective cognitive decline: Results from a pilot randomized controlled trial. J Alzheimers Dis 52 (2016), 757–774.
Vellas, B., Coley, N., Ousset, P.J., Berrut, G., Dartigues, J.F., Dubois, B., et al. Long-term use of standardised ginkgo biloba extract for the prevention of Alzheimer's disease (GuidAge): a randomised placebo-controlled trial. Lancet Neurol 11 (2012), 851–859.
Gillette-Guyonnet, S., Andrieu, S., Dantoine, T., Dartigues, J.F., Touchon, J., Vellas, B., Commentary on “A roadmap for the prevention of dementia II. Leon Thal Symposium 2008.” The Multidomain Alzheimer Preventive Trial (MAPT): a new approach to the prevention of Alzheimer's disease. Alzheimers Dement 5 (2009), 114–121.
ten Brinke, L.F., Bolandzadeh, N., Nagamatsu, L.S., Hsu, C.L., Davis, J.C., Miran-Khan, K., et al. Aerobic exercise increases hippocampal volume in older women with probable mild cognitive impairment: a 6-month randomised controlled trial. Br J Sports Med 49 (2015), 248–254.
Visser, P.J., Verhey, F., Knol, D.L., Scheltens, P., Wahlund, L.O., Freund-Levi, Y., et al. Prevalence and prognostic value of CSF markers of Alzheimer's disease pathology in patients with subjective cognitive impairment or mild cognitive impairment in the DESCRIPA study: a prospective cohort study. Lancet Neurol 8 (2009), 619–627.
van Harten, A.C., Visser, P.J., Pijnenburg, Y.A., Teunissen, C.E., Blankenstein, M.A., Scheltens, P., et al. Cerebrospinal fluid Abeta42 is the best predictor of clinical progression in patients with subjective complaints. Alzheimers Dement 9 (2013), 481–487.
Molinuevo, J.L., Rabin, L.A., Amariglio, R., Teunissen, C.E., Blankenstein, M.A., Scheltens, P., et al. Implementation of subjective cognitive decline criteria in research studies. Alzheimers Dement 9 (2016), 481–487.
Jessen, F., Spottke, A., Boecker, H., Brosseron, F., Buerger, K., Catak, C., et al. Design and first baseline data of the DZNE multicenter observational study on predementia Alzheimer's disease (DELCODE). Alzheimers Res Ther, 10, 2018, 15.
Morris, J.C., Heyman, A., Mohs, R.C., Hughes, J.P., van Belle, G., Fillenbaum, G., et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 39 (1989), 1159–1165.
Gauggel, S., Birkner, B., Validity and reliability of a German version of the Geriatric Depression Scale (GDS). Z für Klinische Psychol Psychotherapie 28 (1999), 18–27 [Article German].
van der Flier, W.M., Pijnenburg, Y.A.L., Prins, N., Lemstra, A.W., Bouwman, F.H., Teunissen, C.E., et al. Optimizing patient care and research: The Amsterdam dementia cohort. J Alzheimers Dis 41 (2014), 313–327.
Sheikh, J.I., Yesavage, J.A., Geriatric Depression Scale (GDS). Recent evidence and development of a shorter version. Brink, T.L., (eds.) Clinical Gerontology: A Guide to Assessment and Intervention, 1986, The Haworth Press, Inc, NY, 165–173.
Rami, L., Molinuevo, J.L., Sanchez-Valle, R., Bosch, B., Villar, A., Screening for amnestic mild cognitive impairment and early Alzheimer's disease with M@T (Memory Alteration Test) in the primary care population. Int J Geriatr Psychiatry 22 (2007), 294–304.
Bjelland, I., Dahl, A.A., Haug, T.T., Neckelmann, D., The validity of the Hospital Anxiety and Depression Scale. An updated literature review. J Psychosomatic Res 52 (2002), 69–77.
Mulder, C., Verwey, N.A., van der Flier, W.M., Bouwman, F.H., Kok, A., van Elk, E.J., et al. Amyloid-beta(1-42), total tau, and phosphorylated tau as cerebrospinal fluid biomarkers for the diagnosis of Alzheimer disease. Clin Chem 56 (2010), 248–253.
Tijms, B.M., Willemse, E.A.J., Zwan, M.D., Mulder, S.D., Visser, P.J., van Berckel, B.N.M., et al. Unbiased approach to counteract upward drift in cerebrospinal fluid Amyloid-β 1-42 Analysis Results. Clin Chem 64 (2018), 576–585.
Jack, C.R. Jr., Bennett, D.A., Blennow, K., Carrillo, M.C., Dunn, B., Haeberlein, S.B., et al. NIA-AA Research Framework: Toward a biological definition of Alzheimer's disease. Alzheimers Dement 14 (2018), 535–562.
Chetelat, G., Villemagne, V.L., Bourgeat, P., Pike, K.E., Jones, G., Ames, D., et al. Relationship between atrophy and beta-amyloid deposition in Alzheimer disease. Ann Neurol 67 (2010), 317–324.
Mormino, E.C., Kluth, J.T., Madison, C.M., Rabinovici, G.D., Baker, S.L., Miller, B.L., et al. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain 132 (2009), 1310–1323.
Jack, C.R. Jr., Lowe, V.J., Senjem, M.L., Weigand, S.D., Kemp, B.J., Shiung, M.M., et al. 11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment. Brain 131 (2008), 665–680.
Storandt, M., Mintun, M.A., Head, D., Morris, J.C., Cognitive decline and brain volume loss as signatures of cerebral Amyloid-ß peptide deposition identified with Pittsburgh compound B. Arch Neurol 66 (2009), 1476–1481.
Rowe, C.C., Ellis, K.A., Rimajova, M., Bourgeat, P., Pike, K.E., Jones, G., et al. Amyloid imaging results from the Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging. Neurobiol Aging 31 (2010), 1275–1283.
Dickerson, B.C., Bakkour, A., Salat, D.H., Feczko, E., Pacheco, J., Greve, D.N., et al. The cortical signature of Alzheimer's disease: regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloid-positive individuals. Cereb Cortex 19 (2009), 497–510.
Becker, J.A., Hedden, T., Carmasin, J., Maye, J., Rentz, D.M., Putcha, D., et al. Amyloid-β associated cortical thinning in clinically normal elderly. Ann Neurol 69 (2011), 1032–1042.
Sperling, R.A., Johnson, K.A., Doraiswamy, P.M., Reiman, E.M., Fleisher, A.S., Sabbagh, M.N., et al. Amyloid deposition detected with florbetapir F 18 ((18)F-AV-45) is related to lower episodic memory performance in clinically normal older individuals. Neurobiol Aging 34 (2013), 822–831.
Amariglio, R.E., Mormino, E.C., Pietras, A.C., Marshall, G.A., Vannini, P., Johnson, K.A., et al. Subjective cognitive concerns, amyloid-ß and neurodegeneration in clinically normal elderly. Neurology 85 (2015), 56–62.
Pike, K.E., Ellis, K.A., Villemagne, V.L., Good, N., Chételat, G., Ames, D., et al. Cognition and beta-amyloid in preclinical Alzheimer's disease: data from the AIBL study. Neuropsychologia 49 (2011), 2384–2390.
