Different patterns of gray matter atrophy in early- and late-onset Alzheimer's disease

Neurobiology of Aging

Volumn 34, Issue 8, 2013, Pages 2014-2022

  Möller, Christiane ^a   Vrenken, Hugo ^b   Jiskoot, Lize ^a   Versteeg, Adriaan ^b   Barkhof, Frederik ^b   Scheltens, Philip ^a   van der Flier, Wiesje M ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Alzheimer's disease; Early onset; EOAD; Gray matter atrophy; Late onset; LOAD; MRI; Voxel based morphometry

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; CEREBELLUM; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GRAY MATTER ATROPHY; HIPPOCAMPUS; HUMAN; INFERIOR FRONTAL GYRUS; LUMBAR PUNCTURE; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PRECUNEUS; PRIORITY JOURNAL; TEMPORAL LOBE; THREE DIMENSIONAL IMAGING; VOXEL BASED MORPHOMETRY;

AGE OF ONSET; AGED; ALZHEIMER DISEASE; APOLIPOPROTEINS E; ATROPHY; CEREBRAL CORTEX; FEMALE; GENOTYPE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PARIETAL LOBE;

EID: 84877594365     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.02.013     Document Type: Article

References (76)

1. Alemán-Gómez, Y., Melie-García, L., Valdés-Hernandez, P., 2012. IBASPM: toolbox for automatic parcellation of brain structures. Presented at: 12th Annual Meeting of the Organization for Human Brain Mapping. June 11-15, 2006; Florence, Italy.
2. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
3. Ashburner J., Friston K.J. Voxel-based morphometry--the methods. Neuroimage 2000, 11:805-821.
4. Balasa M., Gelpi E., Antonell A., Rey M.J., Sanchez-Valle R., Molinuevo J.L., Lladó A. Clinical features and APOE genotype of pathologically proven early-onset Alzheimer disease. Neurology 2011, 76:1720-1725. Neurological Tissue Bank/University of Barcelona/Hospital Clínic NTB/UB/HC Collaborative Group.
5. Bouwman F.H., van der Flier W.M., Schoonenboom N.S., van Elk E.J., Kok A., Rijmen F., Blankenstein M.A., Scheltens P. Longitudinal changes of CSF biomarkers in memory clinic patients. Neurology 2007, 69:1006-1011.
6. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
7. Bruandet A., Richard F., Bombois S., Maurage C.A., Masse I., Amouyel P., Pasquier F. Cognitive decline and survival in Alzheimer's disease according to education level. Dement. Geriatr. Cogn. Disord. 2008, 25:74-80.
8. Canu E., Frisoni G.B., Agosta F., Pievani M., Bonetti M., Filippi M. Early and late onset Alzheimer's disease patients have distinct patterns of white matter damage. Neurobiol. Aging 2012, 33:1023-1033.
9. Cervos-Navarro J., Diemer N.H. Selective vulnerability in brain hypoxia. Crit. Rev. Neurobiol. 1991, 6:149-182.
10. Crutch S.J., Lehmann M., Schott J.M., Rabinovici G.D., Rossor M.N., Fox N.C. Posterior cortical atrophy. Lancet Neurol. 2012, 11:170-178.
11. Crutch S.J., Schott J.M., Rabinovici G.D., Boeve B.F., Cappa S.F., Dickerson B.C., Dubois B., Graff-Radford N.R., Krolak-Salmon P., Lehmann M., Mendez M.F., Pijnenburg Y., Ryan N.S., Scheltens P., Shakespeare T., Tang-Wai D.F., van der Flier W.M., Bain L., Carrillo M.C., Fox N.C. Shining a light on posterior cortical atrophy. Alzheimers Dement 2012, [e-pub ahead of print]. 10.1016/j.jalz.2012.11.004.
12. de Waal H., Stam C.J., Blankenstein M.A., Pijnenburg Y.A., Scheltens P., van der Flier W.M. EEG abnormalities in early and late onset Alzheimer's disease: understanding heterogeneity. J. Neurol. Neurosurg. Psychiatry 2011, 82:67-71.
13. Dos S.V., Thomann P.A., Wustenberg T., Seidl U., Essig M., Schroder J. Morphological cerebral correlates of CERAD test performance in mild cognitive impairment and Alzheimer's disease. J. Alzheimers Dis. 2011, 23:411-420.
14. Fazekas F., Chawluk J.B., Alavi A., Hurtig H.I., Zimmerman R.A. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am. J. Roentgenol. 1987, 149:351-356.
15. Filippini N., Rao A., Wetten S., Gibson R.A., Borrie M., Guzman D., Kertesz A., Loy-English I., Williams J., Nichols T., Whitcher B., Matthews P.M. Anatomically-distinct genetic associations of APOE epsilon4 allele load with regional cortical atrophy in Alzheimer's disease. Neuroimage 2009, 44:724-728.
16. Frisoni G.B., Pievani M., Testa C., Sabattoli F., Bresciani L., Bonetti M., Beltramello A., Hayashi K.M., Toga A.W., Thompson P.M. The topography of grey matter involvement in early and late onset Alzheimer's disease. Brain 2007, 130:720-730.
17. Frisoni G.B., Testa C., Sabattoli F., Beltramello A., Soininen H., Laakso M.P. Structural correlates of early and late onset Alzheimer's disease: voxel based morphometric study. J. Neurol. Neurosurg. Psychiatry 2005, 76:112-114.
18. Galton C.J., Patterson K., Xuereb J.H., Hodges J.R. Atypical and typical presentations of Alzheimer's disease: a clinical, neuropsychological, neuroimaging and pathological study of 13 cases. Brain 2000, 123:484-498.
19. Ginestroni A., Battaglini M., Della N.R., Moretti M., Tessa C., Giannelli M., Caffarra P., Nacmias B., Bessi V., Sorbi S., Bracco L., De Stefano N., Mascalchi M. Early structural changes in individuals at risk of familial Alzheimer's disease: a volumetry and magnetization transfer MR imaging study. J. Neurol. 2009, 256:925-932.
20. Glodzik L., Mosconi L., Tsui W., de Santi S., Zinkowski R., Pirraglia E., Rich K.E., McHugh P., Li Y., Williams S., Ali F., Zetterberg H., Blennow K., Mehta P., de Leon M.J. Alzheimer's disease markers, hypertension, and gray matter damage in normal elderly. Neurobiol. Aging 2012, 33:1215-1227.
21. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
22. Gorno-Tempini M.L., Brambati S.M., Ginex V., Ogar J., Dronkers N.F., Marcone A., Perani D., Garibotto V., Cappa S.F., Miller B.L. The logopenic/phonological variant of primary progressive aphasia. Neurology 2008, 71:1227-1234.
23. Gorno-Tempini M.L., Hillis A.E., Weintraub S., Kertesz A., Mendez M., Cappa S.F., Ogar J.M., Rohrer J.D., Black S., Boeve B.F., Manes F., Dronkers N.F., Vandenberghe R., Rascovsky K., Patterson K., Miller B.L., Knopman D.S., Hodges J.R., Mesulam M.M., Grossman M. Classification of primary progressive aphasia and its variants. Neurology 2011, 76:1006-1014.
24. Grau-Olivares M., Bartres-Faz D., Arboix A., Soliva J.C., Rovira M., Targa C., Junqué C. Mild cognitive impairment after lacunar infarction: voxel-based morphometry and neuropsychological assessment. Cerebrovasc. Dis. 2007, 23:353-361.
25. Greicius M.D., Geschwind M.D., Miller B.L. Presenile dementia syndromes: an update on taxonomy and diagnosis. J. Neurol. Neurosurg. Psychiatry 2002, 72:691-700.
26. Guerreiro R., Wojtas A., Bras J., Carrasquillo M., Rogaeva E., Majounie E., Cruchaga C., Sassi C., Kauwe J.S., Younkin S., Hazrati L., Collinge J., Pocock J., Lashley T., Williams J., Lambert J.C., Amouyel P., Goate A., Rademakers R., Morgan K., Powell J., St George-Hyslop P., Singleton A., Hardy J. TREM2 variants in Alzheimer's disease. N. Engl. J. Med. 2013, 368:117-127. Alzheimer Genetic Analysis Group.
27. Gutierrez-Galve L., Lehmann M., Hobbs N.Z., Clarkson M.J., Ridgway G.R., Crutch S., Ourselin S., Schott J.M., Fox N.C., Barnes J. Patterns of cortical thickness according to APOE genotype in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 2009, 28:476-485.
28. Hashimoto M., Yasuda M., Tanimukai S., Matsui M., Hirono N., Kazui H., Mori E. Apolipoprotein E epsilon 4 and the pattern of regional brain atrophy in Alzheimer's disease. Neurology 2001, 57:1461-1466.
29. Henley S.M., Ridgway G.R., Scahill R.I., Kloppel S., Tabrizi S.J., Fox N.C., Kassubek J. Pitfalls in the use of voxel-based morphometry as a biomarker: examples from huntington disease. AJNR Am. J. Neuroradiol. 2010, 31:711-719. EHDN Imaging Working Group.
30. Ishii K., Kawachi T., Sasaki H., Kono A.K., Fukuda T., Kojima Y., Mori E. Voxel-based morphometric comparison between early- and late-onset mild Alzheimer's disease and assessment of diagnostic performance of z score images. AJNR Am. J. Neuroradiol. 2005, 26:333-340.
31. Jack C.R., Knopman D.S., Jagust W.J., Shaw L.M., Aisen P.S., Weiner M.W., Petersen R.C., Trojanowski J.Q. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 2010, 9:119-128.
32. Jacobs D., Sano M., Marder K., Bell K., Bylsma F., Lafleche G., Albert M., Brandt J., Stern Y. Age at onset of Alzheimer's disease: relation to pattern of cognitive dysfunction and rate of decline. Neurology 1994, 44:1215-1220.
33. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 2001, 5:143-156.
34. Karas G., Scheltens P., Rombouts S., van Schijndel R., Klein M., Jones B., van der Flier W., Vrenken H., Barkhof F. Precuneus atrophy in early-onset Alzheimer's disease: a morphometric structural MRI study. Neuroradiology 2007, 49:967-976.
35. Kester M.I., Scheffer P.G., Koel-Simmelink M.J., Twaalfhoven H., Verwey N.A., Veerhuis R., Twisk J.W., Bouwman F.H., Blankenstein M.A., Scheltens P., Teunissen C., van der Flier W.M. Serial CSF sampling in Alzheimer's disease: specific versus non-specific markers. Neurobiol. Aging 2012, 33:1591-1598.
36. Kim E.J., Cho S.S., Jeong Y., Park K.C., Kang S.J., Kang E., Kim S.E., Lee K.H., Na D.L. Glucose metabolism in early onset versus late onset Alzheimer's disease: an SPM analysis of 120 patients. Brain 2005, 128:1790-1801.
37. Koedam E.L., Lauffer V., van der Vlies A.E., van der Flier W.M., Scheltens P., Pijnenburg Y.A. Early-versus late-onset Alzheimer's disease: more than age alone. J. Alzheimers Dis. 2010, 19:1401-1408.
38. Koedam E.L., Lehmann M., van der Flier W.M., Scheltens P., Pijnenburg Y.A., Fox N., Barkhof F., Wattjes M.P. Visual assessment of posterior atrophy development of a MRI rating scale. Eur. Radiol. 2011, 21:2618-2625.
39. Koss E., Edland S., Fillenbaum G., Mohs R., Clark C., Galasko D., Morris J.C. Clinical and neuropsychological differences between patients with earlier and later onset of Alzheimer's disease: a CERAD analysis, Part XII. Neurology 1996, 46:136-141.
40. Lehmann M., Barnes J., Ridgway G.R., Ryan N.S., Warrington E.K., Crutch S.J., Fox N.C. Global gray matter changes in posterior cortical atrophy: a serial imaging study. Alzheimers Dement. 2012, 8:502-512.
41. Mahncke H.W., Bronstone A., Merzenich M.M. Brain plasticity and functional losses in the aged: scientific bases for a novel intervention. Prog. Brain Res. 2006, 157:81-109.
42. Marshall G.A., Fairbanks L.A., Tekin S., Vinters H.V., Cummings J.L. Early-onset Alzheimer's disease is associated with greater pathologic burden. J. Geriatr. Psychiatry Neurol. 2007, 20:29-33.
43. McKhann G.M., Knopman D.S., Chertkow H., Hyman B.T., Jack C.R., Kawas C.H., Klunk W.E., Koroshetz W.J., Manly J.J., Mayeux R., Mohs R.C., Morris J.C., Rossor M.N., Scheltens P., Carrillo M.C., Thies B., Weintraub S., Phelps C.H. 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. 2011, 7:263-269.
44. Mesulam M., Wicklund A., Johnson N., Rogalski E., Leger G.C., Rademaker A., Weintraub S., Bigio E.H. Alzheimer and frontotemporal pathology in subsets of primary progressive aphasia. Ann. Neurol. 2008, 63:709-719.
45. Migliaccio R., Agosta F., Rascovsky K., Karydas A., Bonasera S., Rabinovici G.D., Miller B.L., Gorno-Tempini M.L. Clinical syndromes associated with posterior atrophy: early age at onset AD spectrum. Neurology 2009, 73:1571-1578.
46. Moghekar A., Kraut M., Elkins W., Troncoso J., Zonderman A.B., Resnick S.M., O'Brien R.J. Cerebral white matter disease is associated with Alzheimer pathology in a prospective cohort. Alzheimers Dement. 2012, 8(5 suppl):S71-S77.
47. Mulder C., Verwey N.A., van der Flier W.M., Bouwman F.H., Kok A., van Elk E.J., Scheltens P., Blankenstein M.A. Amyloid-beta(1-42), total tau, and phosphorylated tau as cerebrospinal fluid biomarkers for the diagnosis of Alzheimer disease. Clin. Chem. 2010, 56:248-253.
48. Murray M.E., Graff-Radford N.R., Ross O.A., Petersen R.C., Duara R., Dickson D.W. Neuropathologically defined subtypes of Alzheimer's disease with distinct clinical characteristics: a retrospective study. Lancet Neurol. 2011, 10:785-796.
49. Ossenkoppele R., Tolboom N., Foster-Dingley J.C., Adriaanse S.F., Boellaard R., Yaqub M., Windhorst A.D., Barkhof F., Lammertsma A.A., Scheltens P., van der Flier W.M., van Berckel B.N. Longitudinal imaging of Alzheimer pathology using [11C]PIB, [18F]FDDNP and [18F]FDG PET. Eur. J. Nucl. Med. Mol. Imaging 2012, 39:990-1000.
50. Ossenkoppele R., Zwan M.D., Tolboom N., van Assema D.M., Adriaanse S.F., Kloet R.W., Boellaard R., Windhorst A.D., Barkhof F., Lammertsma A.A., Scheltens P., van der Flier W.M., van Berckel B.N. Amyloid burden and metabolic function in early-onset Alzheimer's disease: parietal lobe involvement. Brain 2012, 135:2115-2125.
51. Pievani M., Rasser P.E., Galluzzi S., Benussi L., Ghidoni R., Sabattoli F., Bonetti M., Binetti G., Thompson P.M., Frisoni G.B. Mapping the effect of APOE epsilon4 on gray matter loss in Alzheimer's disease in vivo. Neuroimage 2009, 45:1090-1098.
52. Potkin S.G., Guffanti G., Lakatos A., Turner J.A., Kruggel F., Fallon J.H., Saykin A.J., Orro A., Lupoli S., Salvi E., Weiner M., Macciardi F., Alzheimer's Disease Neuroimaging Initiative Hippocampal atrophy as a quantitative trait in a genome-wide association study identifying novel susceptibility genes for Alzheimer's disease. PLoS One 2009, 4:e6501.
53. Raji C.A., Lopez O.L., Kuller L.H., Carmichael O.T., Becker J.T. Age, Alzheimer disease, and brain structure. Neurology 2009, 73:1899-1905.
54. Reiman E.M., Quiroz Y.T., Fleisher A.S., Chen K., Velez-Pardo C., Jimenez-Del-Rio M., Fagan A.M., Shah A.R., Alvarez S., Arbelaez A., Giraldo M., Acosta-Baena N., Sperling R.A., Dickerson B., Stern C.E., Tirado V., Munoz C., Reiman R.A., Huentelman M.J., Alexander G.E., Langbaum J.B., Kosik K.S., Tariot P.N., Lopera F. Brain imaging and fluid biomarker analysis in young adults at genetic risk for autosomal dominant Alzheimer's disease in the presenilin 1 E280A kindred: a case-control study. Lancet Neurol. 2012, 11:1048-1056.
55. Ridgway G.R., Lehmann M., Barnes J., Rohrer J.D., Warren J.D., Crutch S.J., Fox N.C. Early-onset Alzheimer disease clinical variants: multivariate analyses of cortical thickness. Neurology 2012, 79:80-84.
56. Ridgway G.R., Omar R., Ourselin S., Hill D.L., Warren J.D., Fox N.C. Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage 2009, 44:99-111.
57. Roe C.M., Mintun M.A., D'Angelo G., Xiong C., Grant E.A., Morris J.C. Alzheimer disease and cognitive reserve: variation of education effect with carbon 11-labeled Pittsburgh Compound B uptake. Arch. Neurol. 2008, 65:1467-1471.
58. Rosano C., Brach J., Studenski S., Longstreth W.T., Newman A.B. Gait variability is associated with subclinical brain vascular abnormalities in high-functioning older adults. Neuroepidemiology 2007, 29:193-200.
59. Roselli F., Tartaglione B., Federico F., Lepore V., Defazio G., Livrea P. Rate of MMSE score change in Alzheimer's disease: influence of education and vascular risk factors. Clin. Neurol. Neurosurg. 2009, 111:327-330.
60. Rossor M.N., Iversen L.L., Reynolds G.P., Mountjoy C.Q., Roth M. Neurochemical characteristics of early and late onset types of Alzheimer's disease. Br. Med. J. [Clin. Res. Ed.] 1984, 288:961-964.
61. Scheltens P., Fox N., Barkhof F., DeCarli C.D. Structural magnetic resonance imaging in the practical assessment of dementia: beyond exclusion. Lancet Neurol. 2002, 1:13-21.
62. Scheltens P., Leys D., Barkhof F., Huglo D., Weinstein H.C., Vermersch P., Kuiper M., Steinling M., Wolters E.C., Valk J. Atrophy of medial temporal lobes on MRI in " probable" Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates. J. Neurol. Neurosurg. Psychiatry 1992, 55:967-972.
63. Shiino A., Watanabe T., Kitagawa T., Kotani E., Takahashi J., Morikawa S., Akiguchi I. Different atrophic patterns in early- and late-onset Alzheimer's disease and evaluation of clinical utility of a method of regional z-score analysis using voxel-based morphometry. Dement. Geriatr. Cogn. Disord. 2008, 26:175-186.
64. Shiino A., Watanabe T., Maeda K., Kotani E., Akiguchi I., Matsuda M. Four subgroups of Alzheimer's disease based on patterns of atrophy using VBM and a unique pattern for early onset disease. Neuroimage 2006, 33:17-26.
65. Smith C.D., Chebrolu H., Wekstein D.R., Schmitt F.A., Markesbery W.R. Age and gender effects on human brain anatomy: a voxel-based morphometric study in healthy elderly. Neurobiol. Aging 2007, 28:1075-1087.
66. Smits L.L., Pijnenburg Y.A., Koedam E.L., van der Vlies A.E., Reuling I.E., Koene T., Teunissen C.E., Scheltens P., van der Flier W.M. Early onset Alzheimer's disease is associated with a distinct neuropsychological profile. J. Alzheimers Dis. 2012, 30:101-108.
67. Spulber G., Niskanen E., Macdonald S., Kivipelto M., Padilla D.F., Julkunen V., Hallikainen M., Vanninen R., Wahlund L.O., Soininen H. Evolution of global and local grey matter atrophy on serial MRI scans during the progression from MCI to AD. Curr. Alzheimer Res. 2012, 9:516-524.
68. Stern Y., Albert S., Tang M.X., Tsai W.Y. Rate of memory decline in AD is related to education and occupation: cognitive reserve?. Neurology 1999, 53:1942-1947.
69. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
70. van de Pol L.A., Hensel A., Barkhof F., Gertz H.J., Scheltens P., van der Flier W.M. Hippocampal atrophy in Alzheimer disease: age matters. Neurology 2006, 66:236-238.
71. van der Flier W.M., Pijnenburg Y.A., Fox N.C., Scheltens P. Early-onset versus late-onset Alzheimer's disease: the case of the missing APOE epsilon 4 allele. Lancet Neurol. 2011, 10:280-288.
72. van der Vlies A.E., Koedam E.L., Pijnenburg Y.A., Twisk J.W., Scheltens P., van der Flier W.M. Most rapid cognitive decline in APOE epsilon4 negative Alzheimer's disease with early onset. Psychol. Med. 2009, 39:1907-1911.
73. Whitwell J.L., Dickson D.W., Murray M.E., Weigand S.D., Tosakulwong N., Senjem M.L., Knopman D.S., Boeve B.F., Parisi J.E., Petersen R.C., Jack C.R., Josephs K.A. Neuroimaging correlates of pathologically defined subtypes of Alzheimer's disease: a case-control study. Lancet Neurol. 2012, 11:868-877.
74. Whitwell J.L., Jack C.R., Kantarci K., Weigand S.D., Boeve B.F., Knopman D.S., Drubach D.A., Tang-Wai D.F., Petersen R.C., Josephs K.A. Imaging correlates of posterior cortical atrophy. Neurobiol. Aging 2007, 28:1051-1061.
75. Whitwell J.L., Weigand S.D., Boeve B.F., Senjem M.L., Gunter J.L., DeJesus-Hernandez M., Rutherford N.J., Baker M., Knopman D.S., Wszolek Z.K., Parisi J.E., Dickson D.W., Petersen R.C., Rademakers R., Jack C.R., Josephs K.A. Neuroimaging signatures of frontotemporal dementia genetics: C9ORF72, tau, progranulin and sporadics. Brain 2012, 135:794-806.
76. Zakzanis K.K., Boulos M.I. Posterior cortical atrophy. Neurologist 2001, 7:341-349.