Unbiased tensor-based morphometry: Improved robustness and sample size estimates for Alzheimer's disease clinical trials

NeuroImage

Volumn 66, Issue , 2013, Pages 648-661

  Hua, Xue ^a   Hibar, Derrek P ^a   Ching, Christopher R K ^a   Boyle, Christina P ^a   Rajagopalan, Priya ^a   Gutman, Boris A ^a   Leow, Alex D ^b,c   Toga, Arthur W ^a   Jack, Clifford R ^d   Harvey, Danielle ^e   Weiner, Michael W ^f,g   Thompson, Paul M ^a,h  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c University of Illinois at Chicago   (United States)

^d MAYO CLINIC   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ADNI; Aging; Alzheimer's disease; Drug trial; Mild cognitive impairment; Tensor based morphometry

Indexed keywords

APOLIPOPROTEIN E;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; BRAIN SCINTISCANNING; CONTROLLED STUDY; DIAGNOSTIC IMAGING; DISEASE COURSE; FEMALE; FUNCTIONAL NEUROIMAGING; HIGH THROUGHPUT SCREENING; HUMAN; IMAGE ANALYSIS; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; MORPHOMETRICS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SAMPLE SIZE; THREE DIMENSIONAL IMAGING; UNBIASED TENSOR-BASED MORPHOMETRY;

AGED; ALZHEIMER DISEASE; APOLIPOPROTEINS E; ATROPHY; BRAIN; CLINICAL TRIALS AS TOPIC; DATA INTERPRETATION, STATISTICAL; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; MILD COGNITIVE IMPAIRMENT; PROSPECTIVE STUDIES; RESEARCH DESIGN;

EID: 84872244006     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.10.086     Document Type: Article

References (88)

1. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821.
2. Ashburner J., Friston K.J. Morphometry. Human Brain Function 2003, Academic Press.
3. Baron J.C., Chetelat G., Desgranges B., Perchey G., Landeau B., de la Sayette V., Eustache F. In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. NeuroImage 2001, 14:298-309.
4. Bartzokis G. Alzheimer's disease as homeostatic responses to age-related myelin breakdown. Neurobiol. Aging 2011, 32:1341-1371.
5. Bartzokis G., Lu P.H., Geschwind D.H., Edwards N., Mintz J., Cummings J.L. Apolipoprotein E genotype and age-related myelin breakdown in healthy individuals: implications for cognitive decline and dementia. Arch. Gen. Psychiatry 2006, 63:63-72.
6. Bartzokis G., Lu P.H., Geschwind D.H., Tingus K., Huang D., Mendez M.F., Edwards N., Mintz J. Apolipoprotein E affects both myelin breakdown and cognition: implications for age-related trajectories of decline into dementia. Biol. Psychiatry 2007, 62:1380-1387.
7. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 2009, 29:1860-1873.
8. Carmichael O.T., Thompson P.M., Dutton R.A., Lu A., Lee S.E., Lee J.Y., Kuller L.H., Lopez O.L., Aizenstein H.J., Meltzer C.C., Liu Y., Toga A.W., Becker J.T. Mapping ventricular changes related to dementia and mild cognitive impairment in a large community-based cohort. IEEE ISBI 2006, 315-318.
9. Chen K., Reschke C., Lee W., Napatkamon A., Liu X., Bandy D., Langbaum J., Alexander G.E., Foster N.L., Koeppe R.A., Jagust W.J., Weiner M.W., Reiman E.M. Cross-sectional and longitudinal analyses of fluorodeoxyglucose positron emission tomography images from the Alzheimer's disease neuroimaging initiative. ADNI Data Presentations Meeting, Seattle, WA 2009.
10. Chen K., Langbaum J.B., Fleisher A.S., Ayutyanont N., Reschke C., Lee W., Liu X., Bandy D., Alexander G.E., Thompson P.M., Foster N.L., Harvey D.J., de Leon M.J., Koeppe R.A., Jagust W.J., Weiner M.W., Reiman E.M. Twelve-month metabolic declines in probable Alzheimer's disease and amnestic mild cognitive impairment assessed using an empirically pre-defined statistical region-of-interest: findings from the Alzheimer's Disease Neuroimaging Initiative. NeuroImage 2010, 51:654-664.
11. Chetelat G., Landeau B., Eustache F., Mezenge F., Viader F., de la Sayette V., Desgranges B., Baron J.C. Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. NeuroImage 2005, 27:934-946.
12. Ching C.R.K., Hua X., Ward C., Gunter J., Bernstein M., Jack C.R., Weiner M.W., Thompson P.M. Phantom-based MRI corrections and power to track brain change. IEEE International Symposium on Biomedical Imaging 2012, 1172-1175.
13. Chou Y.Y., Lepore N., de Zubicaray G.I., Carmichael O.T., Becker J.T., Toga A.W., Thompson P.M. Automated ventricular mapping with multi-atlas fluid image alignment reveals genetic effects in Alzheimer's disease. NeuroImage 2008, 40:615-630.
14. Chou Y.Y., Lepore N., Avedissian C., Madsen S.K., Parikshak N., Hua X., Shaw L.M., Trojanowski J.Q., Weiner M.W., Toga A.W., Thompson P.M. Mapping correlations between ventricular expansion and CSF amyloid and tau biomarkers in 240 subjects with Alzheimer's disease, mild cognitive impairment and elderly controls. NeuroImage 2009, 46:394-410.
15. Christensen G.E., Johnson H.J. Consistent image registration. IEEE Trans. Med. Imaging 2001, 20:568-582.
16. Chung M.K., Worsley K.J., Paus T., Cherif C., Collins D.L., Giedd J.N., Rapoport J.L., Evans A.C. A unified statistical approach to deformation-based morphometry. NeuroImage 2001, 14:595-606.
17. Clarkson M.J., Ourselin S., Nielsen C., Leung K.K., Barnes J., Whitwell J.L., Gunter J.L., Hill D.L., Weiner M.W., Jack C.R., Fox N.C. Comparison of phantom and registration scaling corrections using the ADNI cohort. NeuroImage 2009, 47:1506-1513.
18. Collins D.L., Neelin P., Peters T.M., Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994, 18:192-205.
19. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
20. Corder E.H., Saunders A.M., Risch N.J., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Rimmler J.B., Locke P.A., Conneally P.M., Schmader K.E., et al. Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat. Genet. 1994, 7:180-184.
21. Cummings J.L. Integrating ADNI results into Alzheimer's disease drug development programs. Neurobiol. Aging 2010, 31:1481-1492.
22. Davatzikos C., Resnick S.M., Wu X., Parmpi P., Clark C.M. Individual patient diagnosis of AD and FTD via high-dimensional pattern classification of MRI. NeuroImage 2008, 41:1220-1227.
23. Davison A.C., Hinkley D.V. Bootstrap methods and their application 1997, Cambridge University Press.
24. Eastman P. Plans under way for Alzheimer's prevention trial. Neurology Today 2012, 1-14.
25. Efron B., Tibshirani R.J. An introduction to the bootstrap 1993, Chapman & Hall, New York.
26. Ferri C.P., Prince M., Brayne C., Brodaty H., Fratiglioni L., Ganguli M., Hall K., Hasegawa K., Hendrie H., Huang Y., Jorm A., Mathers C., Menezes P.R., Rimmer E., Scazufca M. Global prevalence of dementia: a Delphi consensus study. Lancet 2005, 366:2112-2117.
27. Fox N.C., Cousens S., Scahill R., Harvey R.J., Rossor M.N. Using serial registered brain magnetic resonance imaging to measure disease progression in Alzheimer disease: power calculations and estimates of sample size to detect treatment effects. Arch. Neurol. 2000, 57:339-344.
28. Fox N.C., Ridgway G.R., Schott J.M. Algorithms, atrophy and Alzheimer's disease: cautionary tales for clinical trials. NeuroImage 2011, 57:15-18.
29. Freeborough P.A., Fox N.C. The boundary shift integral: an accurate and robust measure of cerebral volume changes from registered repeat MRI. IEEE Trans. Med. Imaging 1997, 16:623-629.
30. Freeborough P.A., Fox N.C. Modeling brain deformations in Alzheimer disease by fluid registration of serial 3D MR images. J. Comput. Assist. Tomogr. 1998, 22:838-843.
31. Frisoni G.B., Weiner M.W. Alzheimer's Disease Neuroimaging Initiative special issue. Neurobiol. Aging 2010, 31:1259-1262.
32. 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.
33. Gunter J., Bernstein M., Borowski B., Felmlee J., Blezek D., Mallozzi R., Levy J., Schuff N., Jack C.R. Validation testing of the MRI calibration phantom for the Alzheimer's Disease Neuroimaging Initiative Study. ISMRM 14th Scientific Meeting and Exhibition 2006.
34. Gutman B., Rajagopalan P., Hua X., Thompson P.M. Maximizing Power to Track Alzheimer's Disease Progression by LDA-Based Weighting of Longitudinal Ventricular Surface Features. The 15th International Conference on Medical Image Computing and Computer Assisted Intervention (MICCAI), Novel Neuroimaging Biomarkers for Alzheimer's Disease and Related Disorders Workshop, Nice, France 2012.
35. Hobbs N.Z., Henley S.M., Ridgway G.R., Wild E.J., Barker R.A., Scahill R.I., Barnes J., Fox N.C., Tabrizi S.J. The progression of regional atrophy in premanifest and early Huntington's disease: a longitudinal voxel-based morphometry study. J. Neurol. Neurosurg. Psychiatry 2010, 81:756-763.
36. Holland D., Dale A.M. Nonlinear registration of longitudinal images and measurement of change in regions of interest. Medical Image Analysis 2011, 15:489-497.
37. Holland D., Brewer J.B., Hagler D.J., Fennema-Notestine C., Dale A.M. Subregional neuroanatomical change as a biomarker for Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20954-20959.
38. Holland D., McEvoy L.K., Dale A.M. Unbiased comparison of sample size estimates from longitudinal structural measures in ADNI. Hum. Brain Mapp 2012, 33:2586-2602.
39. Hua X., Leow A.D., Parikshak N., Lee S., Chiang M.C., Toga A.W., Jack C.R., Weiner M.W., Thompson P.M. Tensor-based morphometry as a neuroimaging biomarker for Alzheimer's disease: an MRI study of 676 AD, MCI, and normal subjects. NeuroImage 2008, 43:458-469.
40. Hua X., Lee S., Yanovsky I., Leow A.D., Chou Y.Y., Ho A.J., Gutman B., Toga A.W., Jack C.R., Bernstein M.A., Reiman E.M., Harvey D.J., Kornak J., Schuff N., Alexander G.E., Weiner M.W., Thompson P.M. Optimizing power to track brain degeneration in Alzheimer's disease and mild cognitive impairment with tensor-based morphometry: an ADNI study of 515 subjects. NeuroImage 2009, 48:668-681.
41. Hua X., Lee S., Hibar D.P., Yanovsky I., Leow A.D., Toga A.W., Jack C.R., Bernstein M.A., Reiman E.M., Harvey D.J., Kornak J., Schuff N., Alexander G.E., Weiner M.W., Thompson P.M. Mapping Alzheimer's disease progression in 1309 MRI scans: power estimates for different inter-scan intervals. NeuroImage 2010, 51:63-75.
42. Hua X., Gutman B., Boyle C.P., Rajagopalan P., Leow A.D., Yanovsky I., Kumar A.R., Toga A.W., Jack C.R., Schuff N., Alexander G.E., Chen K., Reiman E.M., Weiner M.W., Thompson P.M. Accurate measurement of brain changes in longitudinal MRI scans using tensor-based morphometry. NeuroImage 2011, 57:5-14.
43. Iglesias J.E., Liu C.Y., Thompson P.M., Tu Z. Robust brain extraction across datasets and comparison with publicly available methods. IEEE Trans. Med. Imaging 2011, 30:1617-1634.
44. Jack C.R., Petersen R.C., Xu Y.C., O'Brien P.C., Smith G.E., Ivnik R.J., Boeve B.F., Waring S.C., Tangalos E.G., Kokmen E. Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 1999, 52:1397-1403.
45. Jack C.R., Dickson D.W., Parisi J.E., Xu Y.C., Cha R.H., O'Brien P.C., Edland S.D., Smith G.E., Boeve B.F., Tangalos E.G., Kokmen E., Petersen R.C. Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology 2002, 58:750-757.
46. Jack C.R., Bernstein M.A., Fox N.C., Thompson P., Alexander G., Harvey D., Borowski B., Britson P.J., Whitwell J.L., Ward C., Dale A.M., Felmlee J.P., Gunter J.L., Hill D.L., Killiany R., Schuff N., Fox-Bosetti S., Lin C., Studholme C., DeCarli C.S., Krueger G., Ward H.A., Metzger G.J., Scott K.T., Mallozzi R., Blezek D., Levy J., Debbins J.P., Fleisher A.S., Albert M., Green R., Bartzokis G., Glover G., Mugler J., Weiner M.W. The Alzheimer's Disease Neuroimaging Initiative (ADNI): MRI methods. J. Magn. Reson. Imaging 2008, 27:685-691.
47. Jovicich J., Czanner S., Greve D., Haley E., van der Kouwe A., Gollub R., Kennedy D., Schmitt F., Brown G., Macfall J., Fischl B., Dale A. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. NeuroImage 2006, 30:436-443.
48. Kochunov P., Lancaster J., Thompson P., Toga A.W., Brewer P., Hardies J., Fox P. An optimized individual target brain in the Talairach coordinate system. NeuroImage 2002, 17:922-927.
49. Kochunov P., Lancaster J., Hardies J., Thompson P.M., Woods R.P., Cody J.D., Hale D.E., Laird A., Fox P.T. Mapping structural differences of the corpus callosum in individuals with 18q deletions using targetless regional spatial normalization. Hum. Brain Mapp. 2005, 24:325-331.
50. Leow A., Huang S.C., Geng A., Becker J.T., Davis S., Toga A.W., Thompson P.M. Inverse Consistent Mapping in 3D Deformable Image Registration: Its Construction and Statistical Properties. Information Processing in Medical Imaging, Glenwood Springs, Colorado, USA 2005, 493-503.
51. Leporé N., Brun C.C., Chou Y.Y., Lee A.D., Barysheva M., de Zubicaray G.I., Meredith M., McMahon K., Wright M.J., Toga A.W., Thompson P.M. Multi-atlas Tensorbased Morphometry and its Application to a Genetic Study of 92 Twins. Med Image Comput Comput Assist Interv Workshop on Mathematical Foundations of Computational Anatomy (MFCA) 2008.
52. Marsden J., Hughes T. Mathematical foundations of elasticity 1983, Prentice-Hall.
53. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J., Zilles K., Woods R., Paus T., Simpson G., Pike B., Holmes C., Collins L., Thompson P., MacDonald D., Iacoboni M., Schormann T., Amunts K., Palomero-Gallagher N., Geyer S., Parsons L., Narr K., Kabani N., Le Goualher G., Boomsma D., Cannon T., Kawashima R., Mazoyer B. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:1293-1322.
54. Morra J.H., Tu Z., Apostolova L.G., Green A.E., Avedissian C., Madsen S.K., Parikshak N., Hua X., Toga A.W., Jack C.R., Schuff N., Weiner M.W., Thompson P.M. Automated 3D mapping of hippocampal atrophy and its clinical correlates in 400 subjects with Alzheimer's disease, mild cognitive impairment, and elderly controls. Hum. Brain Mapp. 2009, 30:2766-2788.
55. Morra J.H., Tu Z., Apostolova L.G., Green A.E., Avedissian C., Madsen S.K., Parikshak N., Toga A.W., Jack C.R., Schuff N., Weiner M.W., Thompson P.M. Automated mapping of hippocampal atrophy in 1-year repeat MRI data from 490 subjects with Alzheimer's disease, mild cognitive impairment, and elderly controls. NeuroImage 2009, 45:S3-S15.
56. Mueller S.G., Weiner M.W., Thal L.J., Petersen R.C., Jack C., Jagust W., Trojanowski J.Q., Toga A.W., Beckett L. The Alzheimer's disease neuroimaging initiative. Neuroimaging Clin. N. Am. 2005, 15:869-877. (xi-xii).
57. Mueller S.G., Weiner M.W., Thal L.J., Petersen R.C., Jack C.R., Jagust W., Trojanowski J.Q., Toga A.W., Beckett L. Ways toward an early diagnosis in Alzheimer's disease: The Alzheimer's Disease Neuroimaging Initiative (ADNI). Alzheimers Dement. 2005, 1:55-66.
58. Nestor S.M., Rupsingh R., Borrie M., Smith M., Accomazzi V., Wells J.L., Fogarty J., Bartha R. Ventricular enlargement as a possible measure of Alzheimer's disease progression validated using the Alzheimer's disease neuroimaging initiative database. Brain 2008, 131:2443-2454.
59. Pericak-Vance M.A., Bebout J.L., Gaskell P.C., Yamaoka L.H., Hung W.Y., Alberts M.J., Walker A.P., Bartlett R.J., Haynes C.A., Welsh K.A., et al. Linkage studies in familial Alzheimer disease: evidence for chromosome 19 linkage. Am. J. Hum. Genet. 1991, 48:1034-1050.
60. Petersen R.C. Aging, mild cognitive impairment, and Alzheimer's disease. Neurol. Clin. 2000, 18:789-806.
61. Petersen R.C. Mild cognitive impairment clinical trials. Nat. Rev. Drug Discov. 2003, 2:646-653.
62. Petersen R.C. Mild Cognitive Impairment: Aging to Alzheimer's Disease 2003, Oxford University Press, New York.
63. Reiman E.M., Chen K., Ayutyanont N., Lee W., Bandy D., Reschke C., Alexander G.E., Weiner M.W., Koeppe R.A., Foster N.L., Jagust W.J. Twelve-month cerebral metabolic declines in probable Alzheimer's disease and amnestic mild cognitive impairment: Preliminary findings from the Alzheimer's disease neuroimaging initiative (ADNI). Alzheimers Dement. 2008, 4:T110-T111.
64. Reuter M., Schmansky N.J., Rosas H.D., Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 2012, 61:1402-1418.
65. Riddle W.R., Li R., Fitzpatrick J.M., DonLevy S.C., Dawant B.M., Price R.R. Characterizing changes in MR images with color-coded Jacobians. Magn. Reson. Imaging 2004, 22:769-777.
66. Rosner B. Fundamentals of Biostatistics 1990, PWS-Kent Publishing Company, Boston.
67. Ross J., Thompson P.M., Tariot P., Reiman E.M., Schneider L., Frigerio E., Fiorentini F., Giardino L., Calzà L., Norris D., Cicirello H., Casula D., Imbimbo B.P. Primary and Secondary Prevention Trials in Subjects at Risk of Developing Alzheimer's Disease: the GEPARD-AD (Genetically Enriched Population At Risk of Developing Alzheimer's Disease) Studies. CTAD conference, Monte Carlo, Monaco 2012.
68. Saunders A.M., Schmader K., Breitner J.C., Benson M.D., Brown W.T., Goldfarb L., Goldgaber D., Manwaring M.G., Szymanski M.H., McCown N., et al. Apolipoprotein E epsilon 4 allele distributions in late-onset Alzheimer's disease and in other amyloid-forming diseases. Lancet 1993, 342:710-711.
69. Saunders A.M., Strittmatter W.J., Schmechel D., George-Hyslop P.H., Pericak-Vance M.A., Joo S.H., Rosi B.L., Gusella J.F., Crapper-MacLachlan D.R., Alberts M.J., et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 1993, 43:1467-1472.
70. Schachter F., Faure-Delanef L., Guenot F., Rouger H., Froguel P., Lesueur-Ginot L., Cohen D. Genetic associations with human longevity at the APOE and ACE loci. Nat. Genet. 1994, 6:29-32.
71. Schuff N., Woerner N., Boreta L., Kornfield T., Shaw L.M., Trojanowski J.Q., Thompson P.M., Jack C.R., Weiner M.W. MRI of hippocampal volume loss in early Alzheimer's disease in relation to ApoE genotype and biomarkers. Brain 2009, 132(4):1067-1077.
72. Sled J.G., Zijdenbos A.P., Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 1998, 17:87-97.
73. Smith S.M., Rao A., De Stefano N., Jenkinson M., Schott J.M., Matthews P.M., Fox N.C. Longitudinal and cross-sectional analysis of atrophy in Alzheimer's disease: cross-validation of BSI, SIENA and SIENAX. NeuroImage 2007, 36:1200-1206.
74. Spires-Jones T.L., Stoothoff W.H., de Calignon A., Jones P.B., Hyman B.T. Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci. 2009, 32:150-159.
75. Thirion J.P. Image matching as a diffusion process: an analogy with Maxwell's demons. Medical Image Analysis 1998, 2:243-260.
76. Thompson P.M., Giedd J.N., Woods R.P., MacDonald D., Evans A.C., Toga A.W. Growth patterns in the developing brain detected by using continuum mechanical tensor maps. Nature 2000, 404:190-193.
77. Thompson P.M., Hayashi K.M., De Zubicaray G.I., Janke A.L., Rose S.E., Semple J., Hong M.S., Herman D.H., Gravano D., Doddrell D.M., Toga A.W. Mapping hippocampal and ventricular change in Alzheimer disease. NeuroImage 2004, 22:1754-1766.
78. Toga A.W. Brain Warping 1999, Academic Press, San Diego. 1 ed.
79. Trojanowski J.Q., Vandeerstichele H., Korecka M., Clark C.M., Aisen P.S., Petersen R.C., Blennow K., Soares H., Simon A., Lewczuk P., Dean R., Siemers E., Potter W.Z., Weiner M.W., Jack C.R., Jagust W., Toga A.W., Lee V.M., Shaw L.M. Update on the biomarker core of the Alzheimer's Disease Neuroimaging Initiative subjects. Alzheimer's & Dementia : the Journal of the Alzheimer's Association 2010, 6:230-238.
80. Vemuri P., Gunter J.L., Senjem M.L., Whitwell J.L., Kantarci K., Knopman D.S., Boeve B.F., Petersen R.C., Jack C.R. Alzheimer's disease diagnosis in individual subjects using structural MR images: validation studies. NeuroImage 2008, 39:1186-1197.
81. Weiner M.W., Aisen P.S., Jack C.R., Jagust W.J., Trojanowski J.Q., Shaw L., Saykin A.J., Morris J.C., Cairns N., Beckett L.A., Toga A., Green R., Walter S., Soares H., Snyder P., Siemers E., Potter W., Cole P.E., Schmidt M. The Alzheimer's disease neuroimaging initiative: progress report and future plans. Alzheimer's & Dementia : the Journal of the Alzheimer's Association 2010, 6(202-211):e207.
82. Weiner M.W., Veitch D.P., Aisen P.S., Beckett L.A., Cairns N.J., Green R.C., Harvey D., Jack C.R., Jagust W., Liu E., Morris J.C., Petersen R.C., Saykin A.J., Schmidt M.E., Shaw L., Siuciak J.A., Soares H., Toga A.W., Trojanowski J.Q. The Alzheimer's Disease Neuroimaging Initiative: A review of papers published since its inception. Alzheimer's & Dementia : the Journal of the Alzheimer's Association 2012, 8:S1-68.
83. Woods R.P., Grafton S.T., Watson J.D., Sicotte N.L., Mazziotta J.C. Automated image registration: II. Intersubject validation of linear and nonlinear models. J. Comput. Assist. Tomogr. 1998, 22:153-165.
84. Wozniak J.R., Lim K.O. Advances in white matter imaging: a review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging. Neurosci. Biobehav. Rev. 2006, 30:762-774.
85. Wyman B.T., Harvey D.J., Crawford F., Bernstein M.A., Cole P.E., DeCarli C., Fox N.C., Gunter J.L., Hill D., Killiany R.J., Pachai C., Shchwarz A.J., Schuff N., Suhy J., Thompson P.M., Weiner M., Jack C.R. Standardization of Analysis Sets for Reporting Results from ADNI MRI data 2012.
86. Yanovsky I., Thompson P., Osher S., Leow A.D. Asymmetric and symmetric unbiased image registration: statistical assessment of performance. IEEE Computer Society Workshop on Mathematical Methods in Biomedical Image Analysis 2008, 1:1-8.
87. Yanovsky I., Leow A.D., Lee S., Osher S.J., Thompson P.M. Comparing registration methods for mapping brain change using tensor-based morphometry. Medical Image Analysis 2009, 13:679-700.
88. Yushkevich P.A., Avants B.B., Das S.R., Pluta J., Altinay M., Craige C. Bias in estimation of hippocampal atrophy using deformation-based morphometry arises from asymmetric global normalization: an illustration in ADNI 3 T MRI data. NeuroImage 2010, 50:434-445.