Tract-based analysis of white matter degeneration in Alzheimer's disease

Neuroscience

Volumn 301, Issue , 2015, Pages 79-89

  Lee, S H ^a,b   Coutu, J P ^a,c   Wilkens, P ^a   Yendiki, A ^a   Rosas, H D ^a   Salat, D H ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Kangwon National University   (South Korea)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

Alzheimer's disease; Cingulum and angular bundle; Hippocampus; Mild cognitive impairment; White matter

Indexed keywords

AGED; ALZHEIMER DISEASE; ARTICLE; AUTOANALYSIS; BRAIN SIZE; CINGULATE GYRUS; CINGULUM (BRAIN); CONTROLLED STUDY; DATA ANALYSIS SOFTWARE; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HIPPOCAMPUS; HUMAN; IMAGE PROCESSING; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; NERVE DEGENERATION; NERVE FIBER; NERVE TRACT; NEUROANATOMY; NEUROPATHOLOGY; PRIORITY JOURNAL; WHITE MATTER DEGENERATION; WHITE MATTER LESION; BRAIN; COGNITIVE DEFECT; DIFFUSION WEIGHTED IMAGING; PATHOLOGY; WHITE MATTER;

AGED; ALZHEIMER DISEASE; BRAIN; COGNITIVE DYSFUNCTION; DIFFUSION MAGNETIC RESONANCE IMAGING; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; WHITE MATTER;

EID: 84931265617     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.05.049     Document Type: Article

References (80)

1. Acosta-Cabronero J., Williams G.B., Pengas G., Nestor P.J. Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. Brain 2010, 133:529-539.
2. Basser P.J., Pajevic S., Pierpaoli C., Duda J., Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med 2000, 44:625-632.
3. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - A technical review. NMR Biomed 2002, 15:435-455.
4. Behrens T.E., Berg H.J., Jbabdi S., Rushworth M.F., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. Neuroimage 2007, 34:144-155.
5. Bernal-Rusiel J.L., Greve D.N., Reuter M., Fischl B., Sabuncu M.R. Statistical analysis of longitudinal neuroimage data with Linear Mixed Effects models. Neuroimage 2012, 66C:249-260.
6. Bernal-Rusiel J.L., Reuter M., Greve D.N., Fischl B., Sabuncu M.R. Spatiotemporal linear mixed effects modeling for the mass-univariate analysis of longitudinal neuroimage data. Neuroimage 2013, 81:358-370.
7. Bobinski M., de Leon M.J., Wegiel J., Desanti S., Convit A., Saint Louis L.A., Rusinek H., Wisniewski H.M. The histological validation of post mortem magnetic resonance imaging-determined hippocampal volume in Alzheimer's disease. Neuroscience 2000, 95:721-725.
8. Bouras C., Hof P.R., Giannakopoulos P., Michel J.P., Morrison J.H. Regional distribution of neurofibrillary tangles and senile plaques in the cerebral cortex of elderly patients: a quantitative evaluation of a one-year autopsy population from a geriatric hospital. Cereb Cortex 1991, 4:138-150.
9. Bozzali M., Falini A., Franceschi M., Cercignani M., Zuffi M., Scotti G., Comi G., Filippi M. White matter damage in Alzheimer's disease assessed in vivo using diffusion tensor magnetic resonance imaging. J Neurol Neurosurg Psychiatry 2002, 72:742-746.
10. Brun A., Englund E. A white matter disorder in dementia of the Alzheimer type: a pathoanatomical study. Ann Neurol 1986, 19:253-262.
11. Bucur B., Madden D.J., Spaniol J., Provenzale J.M., Cabeza R., White L.E., Huettel S.A. Age-related slowing of memory retrieval: contributions of perceptual speed and cerebral white matter integrity. Neurobiol Aging 2008, 29:1070-1079.
12. Chenevert T.L., Stegman L.D., Taylor J.M., Robertson P.L., Greenberg H.S., Rehemtulla A., Ross B.D. Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. J Natl Cancer Inst 2000, 92:2029-2036.
13. Cherbuin N., Anstey K.J., Reglade-Meslin C., Sachdev P.S. In vivo hippocampal measurement and memory: a comparison of manual tracing and automated segmentation in a large community-based sample. PLoS One 2009, 4:e5265.
14. Choi S.J., Lim K.O., Monteiro I., Reisberg B. Diffusion tensor imaging of frontal white matter microstructure in early Alzheimer's disease: a preliminary study. J Geriatr Psychiatry Neurol 2005, 18:12-19.
15. Convit A., De Leon M.J., Tarshish C., De Santi S., Tsui W., Rusinek H., George A. Specific hippocampal volume reductions in individuals at risk for Alzheimer's disease. Neurobiol Aging 1997, 18:131-138.
16. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194.
17. Desikan R.S., Segonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Buckner R.L., Dale A.M., Maguire R.P., Hyman B.T., Albert M.S., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
18. Destrieux C., Fischl B., Dale A., Halgren E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 2010, 53:1-15.
19. Douaud G., Jbabdi S., Behrens T.E., Menke R.A., Gass A., Monsch A.U., Rao A., Whitcher B., Kindlmann G., Matthews P.M., Smith S. DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. NeuroImage 2011, 55:880-890.
20. 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.
21. Fischl B., Liu A., Dale A.M. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 2001, 20:70-80.
22. Fischl B., Rajendran N., Busa E., Augustinack J., Hinds O., Yeo B.T., Mohlberg H., Amunts K., Zilles K. Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 2005, 8(18):1973-1980.
23. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., van der Kouwe A., Killiany R., Kennedy D., Klaveness S., Montillo A., Makris N., Rosen B., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
24. Fischl B., Salat D.H., van der Kouwe A.J., Makris N., Segonne F., Quinn B.T., Dale A.M. Sequence-independent segmentation of magnetic resonance images. Neuroimage 2004, 23(Suppl. 1):S69-84.
25. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 1999, 9:195-207.
26. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D.H., Busa E., Seidman L.J., Goldstein J., Kennedy D., Caviness V., Makris N., Rosen B., Dale A.M. Automatically parcellating the human cerebral cortex. Cereb Cortex 2004, 14:11-22.
27. Galasko D., Klauber M.R., Hofstetter C.R., Salmon D.P., Lasker B., Thal L.J. The Mini-Mental State Examination in the early diagnosis of Alzheimer's disease. Arch Neurol 1990, 47:49-52.
28. Gold B.T., Powell D.K., Xuan L., Jicha G.A., Smith C.D. Age-related slowing of task switching is associated with decreased integrity of frontoparietal white matter. Neurobiol Aging 2010, 31:512-522.
29. Gouw A.A., Seewann A., Vrenken H., van der Flier W.M., Rozemuller J.M., Barkhof F., Scheltens P., Geurts J.J. Heterogeneity of white matter hyperintensities in Alzheimer's disease: post-mortem quantitative MRI and neuropathology. Brain 2008, 131:3286-3298.
30. Greve D.N., Fischl B. Accurate and robust brain image alignment using boundary-based registration. Neuroimage 2009, 48:63-72.
31. Han X., Fischl B. Atlas renormalization for improved brain MR image segmentation across scanner platforms. IEEE Trans Med Imaging 2007, 26:479-486.
32. Hasan MK, Lee W, Park B, Han K (2012) Connectivity Analysis of Hippocampus in Alzheimer's Brain Using Probabilistic Tractography. In: Bio-Inspired Computing and Applications, pp 521-529: Springer, Berlin Heidelberg.
33. Hyman B.T. The neuropathological diagnosis of Alzheimer's disease: clinical-pathological studies. Neurobiol Aging 1997, 18:S27-S32.
34. Jack C.R., Albert M.S., Knopman D.S., McKhann G.M., Sperling R.A., Carrillo M.C., Thies B., Phelps C.H. Introduction to the recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011, 7:257-262.
35. Jack CR, Jr., Bernstein MA, Fox NC, Thompson P, Alexander G, Harvey D, Borowski B, Britson PJ, J LW, Ward C, Dale AM, Felmlee JP, Gunter JL, Hill DL, Killiany R, Schuff N, Fox-Bosetti S, Lin C, Studholme C, DeCarli CS, Krueger G, Ward HA, Metzger GJ, Scott KT, Mallozzi R, Blezek D, Levy J, Debbins JP, Fleisher AS, Albert M, Green R, Bartzokis G, Glover G, Mugler J, Weiner MW (2008) The Alzheimer's Disease Neuroimaging Initiative (ADNI): MRI methods. Journal of magnetic resonance imaging : JMRI 27:685-691.
36. Jeurissen B., Leemans A., Tournier J.D., Jones D.K., Sijbers J. Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp 2013, 34:2747-2766.
37. Langa K.M., Chernew M.E., Kabeto M.U., Herzog A.R., Ofstedal M.B., Willis R.J., Wallace R.B., Mucha L.M., Straus W.L., Fendrick A.M. National estimates of the quantity and cost of informal caregiving for the elderly with dementia. J Gen Intern Med 2001, 16:770-778.
38. Lim J.S., Park Y.H., Jang J.W., Park S.Y., Kim S. Differential white matter connectivity in early mild cognitive impairment according to CSF biomarkers. PLoS One 2014, 9:e91400.
39. Liu Y., Spulber G., Lehtimaki K.K., Kononen M., Hallikainen I., Grohn H., Kivipelto M., Hallikainen M., Vanninen R., Soininen H. Diffusion tensor imaging and tract-based spatial statistics in Alzheimer's disease and mild cognitive impairment. Neurobiol Aging 2011, 32:1558-1571.
40. Madden D.J., Spaniol J., Costello M.C., Bucur B., White L.E., Cabeza R., Davis S.W., Dennis N.A., Provenzale J.M., Huettel S.A. Cerebral white matter integrity mediates adult age differences in cognitive performance. J Cogn Neurosci 2009, 21:289-302.
41. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. 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 1984, 34:939-944.
42. Morey R.A., Petty C.M., Xu Y., Hayes J.P., Wagner H.R., Lewis D.V., LaBar K.S., Styner M., McCarthy G. A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 2009, 45:855-866.
43. Moseley M. Diffusion tensor imaging and aging - a review. NMR Biomed 2002, 15:553-560.
44. Nir T, Jahanshad N, Jack CR, Weiner MW, Toga AW, Thompson PM (2012) Small world network measures predict white matter degeneration in patients with early-stage mild cognitive impairment. Proceedings / IEEE International Symposium on Biomedical Imaging: from nano to macro IEEE International Symposium on Biomedical Imaging 1405-1408.
45. Nir T.M., Jahanshad N., Villalon-Reina J.E., Toga A.W., Jack C.R., Weiner M.W., Thompson P.M. Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging. Neuroimage Clin 2013, 3:180-195.
46. Pardoe H.R., Pell G.S., Abbott D.F., Jackson G.D. Hippocampal volume assessment in temporal lobe epilepsy: How good is automated segmentation?. Epilepsia 2009, 50:2586-2592.
47. Peters A. The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 2002, 31:581-593.
48. Pievani M., Agosta F., Pagani E., Canu E., Sala S., Absinta M., Geroldi C., Ganzola R., Frisoni G.B., Filippi M. Assessment of white matter tract damage in mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 2010, 31:1862-1875.
49. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012, 59:2142-2154.
50. Reuter M., Fischl B. Avoiding asymmetry-induced bias in longitudinal image processing. Neuroimage 2011, 57:19-21.
51. Reuter M., Rosas H.D., Fischl B. Highly accurate inverse consistent registration: a robust approach. Neuroimage 2010, 53:1181-1196.
52. Reuter M., Schmansky N.J., Rosas H.D., Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 2012, 61:1402-1418.
53. Rice D.P., Fox P.J., Max W., Webber P.A., Lindeman D.A., Hauck W.W., Segura E. The economic burden of Alzheimer's disease care. Health Aff (Millwood) 1993, 12:164-176.
54. Rose S.E., Chen F., Chalk J.B., Zelaya F.O., Strugnell W.E., Benson M., Semple J., Doddrell D.M. Loss of connectivity in Alzheimer's disease: an evaluation of white matter tract integrity with colour coded MR diffusion tensor imaging. J Neurol Neurosurg Psychiatry 2000, 69:528-530.
55. Rowley J., Fonov V., Wu O., Eskildsen S.F., Schoemaker D., Wu L., Mohades S., Shin M., Sziklas V., Cheewakriengkrai L., Shmuel A., Dagher A., Gauthier S., Rosa-Neto P. White matter abnormalities and structural hippocampal disconnections in amnestic mild cognitive impairment and Alzheimer's disease. PLoS One 2013, 8:e74776.
56. Sabuncu M.R., Bernal-Rusiel J.L., Reuter M., Greve D.N., Fischl B. For the Alzheimer's disease neuroimaging I. Event time analysis of longitudinal neuroimage data. Neuroimage 2014, 97C:9-18.
57. Salat D.H., Greve D.N., Pacheco J.L., Quinn B.T., Helmer K.G., Buckner R.L., Fischl B. Regional white matter volume differences in nondemented aging and Alzheimer's disease. Neuroimage 2009, 44:1247-1258.
58. Salat D.H., Kaye J.A., Janowsky J.S. Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease. Arch Neurol 1999, 56:338-344.
59. Salat D.H., Stangl P.A., Kaye J.A., Janowsky J.S. Sex differences in prefrontal volume with aging and Alzheimer's disease. Neurobiol Aging 1999, 20:591-596.
60. Salat D.H., Tuch D.S., van der Kouwe A.J., Greve D.N., Pappu V., Lee S.Y., Hevelone N.D., Zaleta A.K., Growdon J.H., Corkin S., Fischl B., Rosas H.D. White matter pathology isolates the hippocampal formation in Alzheimer's disease. Neurobiol Aging 2010, 31:244-256.
61. Seab J.P., Jagust W.J., Wong S.T., Roos M.S., Reed B.R., Budinger T.F. Quantitative NMR measurements of hippocampal atrophy in Alzheimer's disease. Magn Reson Med 1988, 8:200-208.
62. Segonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., Fischl B. A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004, 22:1060-1075.
63. Segonne F., Grimson E., Fischl B. A genetic algorithm for the topology correction of cortical surfaces. Inf Process Med Imaging 2005, 19:393-405.
64. Sjobeck M., Haglund M., Englund E. Decreasing myelin density reflected increasing white matter pathology in Alzheimer's disease - A neuropathological study. Int J Geriatr Psychiatry 2005, 20:919-926.
65. Sjobeck M., Haglund M., Englund E. White matter mapping in Alzheimer's disease: a neuropathological study. Neurobiol Aging 2006, 27:673-680.
66. Smith C.D., Chebrolu H., Andersen A.H., Powell D.A., Lovell M.A., Xiong S., Gold B.T. White matter diffusion alterations in normal women at risk of Alzheimer's disease. Neurobiol Aging 2010, 31:1122-1131.
67. Song S.K., Sun S.W., Ju W.K., Lin S.J., Cross A.H., Neufeld A.H. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003, 20:1714-1722.
68. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002, 17:1429-1436.
69. Sotak C.H. The role of diffusion tensor imaging in the evaluation of ischemic brain injury - A review. NMR Biomed 2002, 15:561-569.
70. Stebbins G.T., Murphy C.M. Diffusion tensor imaging in Alzheimer's disease and mild cognitive impairment. Behav Neurol 2009, 21:39-49.
71. Sun X., Salat D., Upchurch K., Deason R., Kowall N., Budson A. Destruction of white matter integrity in patients with mild cognitive impairment and Alzheimer disease. J Investig Med 2014.
72. Talairach J., Tournoux P. Co-planar stereotaxic atlas of the human brain 1988, Thieme Medical Publishers, New York.
73. Tiraboschi P., Hansen L.A., Thal L.J., Corey-Bloom J. The importance of neuritic plaques and tangles to the development and evolution of AD. Neurology 2004, 62:1984-1989.
74. Wedeen V.J., Rosene D.L., Wang R., Dai G., Mortazavi F., Hagmann P., Kaas J.H., Tseng W.Y. The geometric structure of the brain fiber pathways. Science 2012, 335:1628-1634.
75. Wenger E., Martensson J., Noack H., Bodammer N.C., Kuhn S., Schaefer S., Heinze H.J., Duzel E., Backman L., Lindenberger U., Lovden M. Comparing manual and automatic segmentation of hippocampal volumes: reliability and validity issues in younger and older brains. Hum Brain Mapp 2014, 35:4236-4248.
76. Werring D.J., Clark C.A., Barker G.J., Thompson A.J., Miller D.H. Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology 1999, 52:1626-1632.
77. Yendiki A., Koldewyn K., Kakunoori S., Kanwisher N., Fischl B. Spurious group differences due to head motion in a diffusion MRI study. Neuroimage 2013, 88C:79-90.
78. Yendiki A., Panneck P., Srinivasan P., Stevens A., Zollei L., Augustinack J., Wang R., Salat D., Ehrlich S., Behrens T., Jbabdi S., Gollub R., Fischl B. Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front Neuroinformatics 2011, 5:23.
79. Yeo B.T., Sabuncu M.R., Desikan R., Fischl B., Golland P. Effects of registration regularization and atlas sharpness on segmentation accuracy. Med Image Anal 2008, 12:603-615.
80. Yoshita M., Fletcher E., Harvey D., Ortega M., Martinez O., Mungas D.M., Reed B.R., DeCarli C.S. Extent and distribution of white matter hyperintensities in normal aging, MCI, and AD. Neurology 2006, 67:2192-2198.