Improved DTI registration allows voxel-based analysis that outperforms Tract-Based Spatial Statistics

NeuroImage

Volumn 94, Issue , 2014, Pages 65-78

  Schwarz, Christopher G ^a   Reid, Robert I ^a   Gunter, Jeffrey L ^a   Senjem, Matthew L ^a   Przybelski, Scott A ^a   Zuk, Samantha M ^a   Whitwell, Jennifer L ^a   Vemuri, Prashanthi ^a   Josephs, Keith A ^a   Kantarci, Kejal ^a   Thompson, Paul M ^b   Petersen, Ronald C ^a   Jack, Clifford R ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

DTI; Fractional Anisotropy; Registration; TBSS; VBM; Voxel based analysis

Indexed keywords

ACCURACY; AGED; ALGORITHM; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FALSE POSITIVE RESULT; HUMAN; IMAGE ANALYSIS; INTERMETHOD COMPARISON; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; SENSITIVITY AND SPECIFICITY; TRACT BASED SPATIAL STATISTICS; VALIDATION PROCESS; VERY ELDERLY; VOXEL BASED ANALYSIS; BRAIN; COMPARATIVE STUDY; COMPUTER ASSISTED DIAGNOSIS; COMPUTER PROGRAM; EVALUATION STUDY; IMAGE ENHANCEMENT; IMAGE SUBTRACTION; MYELINATED NERVE; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; STATISTICAL ANALYSIS; THREE DIMENSIONAL IMAGING;

AGED; AGED, 80 AND OVER; ALGORITHMS; ALZHEIMER DISEASE; BRAIN; DATA INTERPRETATION, STATISTICAL; DIFFUSION TENSOR IMAGING; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; NERVE FIBERS, MYELINATED; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SOFTWARE; SUBTRACTION TECHNIQUE; SUPRANUCLEAR PALSY, PROGRESSIVE;

EID: 84898603661     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.026     Document Type: Article

References (49)

1. Andersson J., Smith S., Jenkinson M. FNIRT-FMRIB's non-linear image registration tool. Annual Meeting of the Organization for Human Brain Mapping (OHBM) 2008, Wiley, Melbourne, Australia.
2. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821.
3. Avants B., Gee J.C. Geodesic estimation for large deformation anatomical shape averaging and interpolation. NeuroImage 2004, 23(Suppl. 1):S139-S150.
4. Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008, 12:26-41.
5. Avants B.B., Tustison N.J., Song G., Cook P.A., Klein A., Gee J.C. A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 2011, 54:2033-2044.
6. Bastin M.E. Correction of eddy current-induced artefacts in diffusion tensor imaging using iterative cross-correlation. Magn. Reson. Imaging 1999, 17:1011-1024.
7. Bookstein F.L. "Voxel-based morphometry" should not be used with imperfectly registered images. NeuroImage 2001, 14:1454-1462.
8. Braskie M.N., Jahanshad N., Stein J.L., Barysheva M., McMahon K.L., de Zubicaray G.I., Martin N.G., Wright M.J., Ringman J.M., Toga A.W., Thompson P.M. Common Alzheimer's disease risk variant within the CLU gene affects white matter microstructure in young adults. J. Neurosci. 2011, 31:6764-6770.
9. Camara-Rey O., Schweiger M., Scahill R.I., Crum W.R., Schnabel J.A., Hill D.L.G., Fox N.C. Simulation of local and global atrophy in Alzheimer's disease studies. Med. Image Comput. Comput. Assist. Interv. 2006, 937-945.
10. Carmichael O., Lockhart S. The role of diffusion tensor imaging in the study of cognitive aging. Curr. Top. Behav. Neurosci. 2012, 11:289-320.
11. Chiang M.-C., Leow A.D., Klunder A.D., Dutton R.A., Barysheva M., Rose S.E., McMahon K.L., de Zubicaray G.I., Toga A.W., Thompson P.M. Fluid registration of diffusion tensor images using information theory. Trans. Med. Imaging 2008, 27:442-456.
12. Chiang M.-C., McMahon K.L., de Zubicaray G.I., Martin N.G., Hickie I., Toga A.W., Wright M.J., Thompson P.M. Genetics of white matter development: a DTI study of 705 twins and their siblings aged 12 to 29. NeuroImage 2011, 54:2308-2317.
13. De Groot M., Vernooij M.W., Klein S., Ikram M.A., Vos F.M., Smith S.M., Niessen W.J., Andersson J.L.R. Improving alignment in tract-based spatial statistics: evaluation and optimization of image registration. NeuroImage 2013, 79:400-411.
14. Douaud G., Jbabdi S., Behrens T.E.J., 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.
15. Edden R.A., Jones D.K. Spatial and orientational heterogeneity in the statistical sensitivity of skeleton-based analyses of diffusion tensor MR imaging data. J. Neurosci. Methods 2011, 201:213-219.
16. Jack C.R.J., 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.G., 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.
17. Jahanshad N., Kochunov P., Sprooten E., Mandl R.C., Nichols T.E., Almassy L., Blangero J., Brouwer R.M., Curran J.E., de Zubicaray G.I., Duggirala R., Fox P.T., Hong L.E., Landman B.A., Martin N.G., McMahon K.L., Medland S.E., Mitchell B.D., Olvera R.L., Peterson C.P., Starr J.M., Sussmann J.E., Toga A.W., Wardlaw J.M., Wright M.J., Hulshoff Pol H.E., Bastin M.E., McIntosh A.M., Deary I.J., Thompson P.M., Glahn D.C. Multi-site genetic analysis of diffusion images and voxelwise heritability analysis: a pilot project of the ENIGMA-DTI working group. NeuroImage 2013, 81:455-469.
18. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 2002, 17:825-841.
19. Jenkinson M., Beckmann C.F., Behrens T.E.J., Woolrich M.W., Smith S.M. FSL. NeuroImage 2012, 62:782-790.
20. Jones D.K., Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010, 23:803-820.
21. Josephs K.A., Xia R., Mandrekar J., Gunter J.L., Senjem M.L., Jack C.R.J., Whitwell J.L. Modeling trajectories of regional volume loss in progressive supranuclear palsy. Mov. Disord. 2013, 28:1117-1124.
22. Kantarci K., Senjem M.L., Lowe V.J., Wiste H.J., Weigand S.D., Kemp B.J., Frank A.R., Shiung M.M., Boeve B.F., Knopman D.S., Petersen R.C., Jack C.R.J. Effects of age on the glucose metabolic changes in mild cognitive impairment. Am. J. Neuroradiol. 2010, 31:1247-1253.
23. Keihaninejad S., Ryan N.S., Malone I.B., Modat M., Cash D., Ridgway G.R., Zhang H., Fox N.C., Ourselin S. The importance of group-wise registration in tract based spatial statistics study of neurodegeneration: a simulation study in Alzheimer's disease. PloS ONE 2012, 7:e45996.
24. Keihaninejad S., Zhang H., Ryan N.S., Malone I.B., Modat M., Cardoso M.J., Cash D., Fox N.C., Ourselin S. An unbiased longitudinal analysis framework for tracking white matter changes using diffusion tensor imaging with application to Alzheimer's disease. NeuroImage 2013, 72:153-163.
25. Klein A., Andersson J., Ardekani B.A., Ashburner J., Avants B., Chiang M.-C., Christensen G.E., Collins D.L., Gee J., Hellier P., Song J.H., Jenkinson M., Lepage C., Rueckert D., Thompson P., Vercauteren T., Woods R.P., Mann J.J., Parsey R.V. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. NeuroImage 2009, 46:786-802.
26. Kohannim O., Jahanshad N., Braskie M.N., Stein J.L., Chiang M.-C., Reese A.H., Hibar D.P., Toga A.W., McMahon K.L., de Zubicaray G.I., Medland S.E., Montgomery G.W., Martin N.G., Wright M.J., Thompson P.M. Predicting white matter integrity from multiple common genetic variants. Neuropsychopharmacology 2012, 37:2012-2019.
27. Le Bihan D., Breton E., Lallemand D., Grenier P., Cabanis E., Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986, 161:401-407.
28. Litvan I., Agid Y., Calne D., Campbell G., Dubois B., Duvoisin R.C., Goetz C.G., Golbe L.I., Grafman J., Growdon J.H., Hallett M., Jankovic J., Quinn N.P., Tolosa E., Zee D.S. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996, 47:1-9.
29. 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.
30. Oba H., Yagishita A., Terada H., Barkovich A.J., Kutomi K., Yamauchi T., Furui S., Shimizu T., Uchigata M., Matsumura K., Sonoo M., Sakai M., Takada K., Harasawa A., Takeshita K., Kohtake H., Tanaka H., Suzuki S. New and reliable MRI diagnosis for progressive supranuclear palsy. Neurology 2005, 64:2050-2055.
31. Oishi K., Faria A., Jiang H., Li X., Akhter K., Zhang J., Hsu J.T., Miller M.I., van Zijl P.C.M., Albert M., Lyketsos C.G., Woods R., Toga A.W., Pike G.B., Rosa-Neto P., Evans A., Mazziotta J., Mori S. Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: Application to normal elderly and Alzheimer's disease participants. NeuroImage 2009, 46:486-499.
32. Park H.-J., Kubicki M., Shenton M.E., Guimond A., McCarley R.W., Maier S.E., Kikinis R., Jolesz F.A., Westin C.-F. Spatial normalization of diffusion tensor MRI using multiple channels. NeuroImage 2003, 20:1995-2009.
33. Petersen R.C., Roberts R.O., Knopman D.S., Geda Y.E., Cha R.H., Pankratz V.S., Boeve B.F., Tangalos E.G., Ivnik R.J., Rocca W.A. Prevalence of mild cognitive impairment is higher in men. The Mayo Clinic Study of Aging. Neurology 2010, 75:889-897.
34. Pierpaoli C., Basser P.J. Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 1996, 36:893-906.
35. Ridgway G.R., Omar R., Ourselin S., Hill D.L.G., Warren J.D., Fox N.C. Issues with threshold masking in voxel-based morphometry of atrophied brains. NeuroImage 2009, 44:99-111.
36. Roberts R.O., Geda Y.E., Knopman D.S., Cha R.H., Pankratz V.S., Boeve B.F., Ivnik R.J., Tangalos E.G., Petersen R.C., Rocca W.A. The Mayo Clinic Study of Aging: design and sampling, participation, baseline measures and sample characteristics. Neuroepidemiology 2008, 30:58-69.
37. Savva G.M., Wharton S.B., Ince P.G., Forster G., Matthews F.E., Brayne C. Age, neuropathology, and dementia. N. Engl. J. Med. 2009, 360:2302-2309.
38. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 2009, 44:83-98.
39. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E.J. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 2006, 31:1487-1505.
40. Stebbins G.T., Murphy C.M. Diffusion tensor imaging in Alzheimer's disease and mild cognitive impairment. Behav. Neurol. 2009, 21:39-49.
41. Sullivan E.V., Adalsteinsson E., Pfefferbaum A. Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb. Cortex 2006, 16:1030-1039.
42. Tustison N.J., Avants B.B., Cook P.A., Kim J., Whyte J., Gee J.C., Stone J.R. Logical circularity in voxel-based analysis: Normalization strategy may induce statistical bias. Hum. Brain Mapp. 2014, 35(3):745-759.
43. 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.J. Alzheimer's disease diagnosis in individual subjects using structural MR images: validation studies. NeuroImage 2008, 39:1186-1197.
44. Whitwell J.L., Wiste H.J., Weigand S.D., Rocca W.A., Knopman D.S., Roberts R.O., Boeve B.F., Petersen R.C., Jack C.R.J. Comparison of imaging biomarkers in the Alzheimer Disease Neuroimaging Initiative and the Mayo Clinic Study of Aging. Arch. Neurol. 2012, 69:614-622.
45. Whitwell J.L., Xu J., Mandrekar J.N., Gunter J.L., Jack C.R.J., Josephs K.A. Rates of brain atrophy and clinical decline over 6 and 12-month intervals in PSP: determining sample size for treatment trials. Parkinsonism Relat. Disord. 2012, 18:252-256.
46. 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.
47. Zalesky A. Moderating registration misalignment in voxelwise comparisons of DTI data: a performance evaluation of skeleton projection. Magn. Reson. Imaging 2011, 29:111-125.
48. Zhan W., Zhang Y., Mueller S.G., Lorenzen P., Hadjidemetriou S., Schuff N., Weiner M.W. Characterization of white matter degeneration in elderly subjects by magnetic resonance diffusion and FLAIR imaging correlation. NeuroImage 2009, 47(Suppl. 2):T58-T65.
49. Zhang H., Yushkevich P.A., Rueckert D., Gee J.C. A computational white matter atlas for aging with surface-based representation of fasciculi. Biomedical Image Registration 2010, 6204:83-90. International Workshop on (WBIR).