Multidimensional morphometric 3D MRI analyses for detecting brain abnormalities in children: Impact of control population

Human Brain Mapping

Volumn 35, Issue 7, 2014, Pages 3199-3215

  Wilke, Marko ^a,b   Rose, Douglas F ^b   Holland, Scott K ^b   Leach, James L ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Automated morphometry; Brain lesion detection; Control group size; High resolution structural MRI; Muiltidimensional analyses

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN DAMAGE; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN REGION; CEREBROSPINAL FLUID; CHILD; CONTROLLED STUDY; CORTICAL DYSPLASIA; FEMALE; GRAY MATTER; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MICROGYRIA; MORPHOMETRICS; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PERIVENTRICULAR HETEROTOPIA; PRIORITY JOURNAL; SCHIZENCEPHALY; SUBCORTICAL HETEROTOPIA; THREE DIMENSIONAL IMAGING; WHITE MATTER; AGE; AGE DISTRIBUTION; ALGORITHM; BRAIN; BRAIN INJURY; NONPARAMETRIC TEST; PATHOLOGY; PATHOPHYSIOLOGY; PRESCHOOL CHILD; SEX RATIO; YOUNG ADULT;

ADOLESCENT; AGE DISTRIBUTION; AGE FACTORS; ALGORITHMS; BRAIN; BRAIN INJURIES; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MALE; SEX DISTRIBUTION; STATISTICS, NONPARAMETRIC; YOUNG ADULT;

EID: 84902174655     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22395     Document Type: Article

References (78)

1. Altaye M, Holland SK, Wilke M, Gaser C (2008): Infant brain probability templates for MRI segmentation and normalization. NeuroImage 43:721-730.
2. Ashburner J (2007): A fast diffeomorphic image registration algorithm. NeuroImage 38:95-113.
3. Ashburner J, Friston KJ (2000): Voxel-based morphometry - the methods. NeuroImage 11:805-821.
4. Ashburner J, Friston KJ (2005): Unified segmentation. NeuroImage 26:839-851.
5. Barkovich AJ, Guerrini R, Kuzniecky RI, Jackson GD, Dobyns WB (2012): A developmental and genetic classification for malformations of cortical development: Update 2012. Brain 135:1348-1369.
6. Bernasconi A, Antel SB, Collins DL, Bernasconi N, Olivier A, Dubeau F, Pike GB, Andermann F, Arnold DL (2001): Texture analysis and morphological processing of magnetic resonance imaging assist detection of focal cortical dysplasia in extra-temporal partial epilepsy. Ann Neurol 49:770-775.
7. Bernasconi A, Bernasconi N, Bernhardt BC, Schrader D (2011): Advances in MRI for 'cryptogenic' epilepsies. Nat Rev Neurol 7:99-108.
8. Blumcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Kahane P, Mathern G, Najm I, Ozkara C, Raybaud C, Represa A, Roper SN, Salamon N, Schulze-Bonhage A, Tassi L, Vezzani A, Spreafico R (2011): The clinicopathologic spectrum of focal cortical dysplasias: A consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52:158-174.
9. Brain Development Cooperative Group (2012): Total and regional brain volumes in a population-based normative sample from 4 to 18 years: The NIH MRI Study of Normal Brain Development. Cereb Cortex 22:1-12.
10. Bruggemann JM, Wilke M, Som SS, Bye AM, Bleasel A, Lawson JA (2007): Voxel-based morphometry in the detection of dysplasia and neoplasia in childhood epilepsy: Combined grey/white matter analysis augments detection. Epilepsy Res 77:93-101.
11. Bruggemann JM, Wilke M, Som SS, Bye AM, Bleasel A, Lawson JA (2009): Voxel-based morphometry in the detection of dysplasia and neoplasia in childhood epilepsy: Limitations of grey matter analysis. J Clin Neurosci 16:780-785.
12. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS, Blumenthal JD, James RS, Ebens CL, Walter JM, Zijdenbos A, Evans AC, Giedd JN, Rapoport JL (2002): Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 288:1740-1748.
13. Colombo N, Salamon N, Raybaud C, Ozkara C, Barkovich AJ (2009): Imaging of malformations of cortical development. Epileptic Disord 11:194-205.
14. Courchesne E, Plante E (1996): Measurement and analysis issues in neurodevelopmental magnetic resonance imaging. In: Thatcher RW, Lyon GR, Rumsey J, Krasnegor N, editors. Developmental Neuroimaging: Mapping the Development of Brain and Behavior, ed 1. San Diego: Academic Press. p 43.
15. Cuadra MB, Cammoun L, Butz T, Cuisenaire O, Thiran JP (2005): Comparison and validation of tissue modelization and statistical classification methods in T1-weighted MR brain images. IEEE Trans Med Imaging 24:1548-1565.
16. de Zwart JA, van Gelderen P, Duyn JH (2006): Receive coil arrays and parallel imaging for functional magnetic resonance imaging of the human brain. Conf Proc IEEE Eng Med Biol Soc 1:17-20.
17. Evans AC, Brain Development Cooperative Group (2006): The NIH MRI study of normal brain development. NeuroImage 30:184-202.
18. Fischl B, Dale AM (2000): Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050-11055.
19. Frederix G, Pauwels EJ (1999): Automatic interpretation based on robust segmentation and shape-extraction. Lect Notes Comp Sci 1614:773-780.
20. Friston K (2012): Ten ironic rules for non-statistical reviewers. NeuroImage 61:1300-1310.
21. Friston KJ, Holmes AP, Worsley KJ (1999): How many subjects constitute a study? NeuroImage 10:1-5.
22. Gaser C, Altaye M, Wilke M, Holland SK (2007): Unified Segmentation Without Tissue Priors. NeuroImage 36(Suppl 1):S68; see also http://dbm.neuro.uni-jena.de/vbm/vbm5-for-spm5/use-of-tissue-priors-experimental/ (retrieved August 28, 2012).
23. Gaser (2012): VBM8 Toolbox. Available online at http://dbm.neuro.uni-jena.de.
24. Gerig G, Kikinis R, Kubler O, Jolesz FA (1992): Nonlinear anisotropic filtering of MRI data. IEEE Trans Med Imaging 11:221-232.
25. Giedd JN, Snell JW, Lange N, Rajapakse JC, Casey BJ, Kozuch PL, Vaituzis AC, Vauss YC, Hamburger SD, Kaysen D, Rapoport JL (1996): Quantitative magnetic resonance imaging of human brain development: Ages 4-18. Cereb Cortex 6:551-560.
26. Gispert JD, Reig S, Pascau J, Vaquero JJ, García-Barreno P, Desco M (2004): Method for bias field correction of brain T1-weighted magnetic resonance images minimizing segmentation error. Hum Brain Mapp 22:133-144.
27. Gogta y N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM (2004): Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101:8174-8149.
28. Good CD, Johnsrude I, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001): Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage 14:685-700.
29. Gothelf D, Penniman L, Gu E, Eliez S, Reiss AL (2007): Developmental trajectories of brain structure in adolescents with 22q11.2 deletion syndrome: A longitudinal study. Schizophr Res 96:72-81.
30. Hoeksma MR, Kenemans JL, Kemner C, van Engeland H (2005): Variability in spatial normalization of pediatric and adult brain images. Clin Neurophysiol 116:1188-1194.
31. Hui C, Zhou YX, Narayana P (2010): Fast algorithm for calculation of inhomogeneity gradient in magnetic resonance imaging data. J Magn Reson Imaging 32:1197-1208.
32. Huppertz HJ, Grimm C, Fauser S, Kassubek J, Mader I, Hochmuth A, Spreer J, Schulze-Bonhage A (2005): Enhanced visualization of blurred gray-white matter junctions in focal cortical dysplasia by voxel-based 3D MRI analysis. Epilepsy Res 67:35-50.
33. Huppertz HJ, Wellmer J, Staack AM, Altenmüller DM, Urbach H, Kröll J (2008): Voxel-based 3D MRI analysis helps to detect subtle forms of subcortical band heterotopia. Epilepsia 49:772-785.
34. Ioannidis JPA (2005): Why most published research findings are false. PLoS Med 2:696-701.
35. Jones DK, Symms MR, Cercignani M, Howard RJ (2005): The effect of filter size on VBM analyses of DT-MRI data. NeuroImage 26:546-554.
36. Kassubek J, Huppertz HJ, Spreer J, Schulze-Bonhage A (2002): Detection and localization of focal cortical dysplasia by voxel-based 3-D MRI analysis. Epilepsia 43:596-602.
37. Lenroot RK, Gogtay N, Greenstein DK, Wells EM, Wallace GL, Clasen LS, Blumenthal JD, Lerch J, Zijdenbos AP, Evans AC, Thompson PM, Giedd JN (2007): Sexual dimorphism of brain developmental trajectories during childhood and adolescence. NeuroImage 36:1065-1073.
38. Machilsen B, d'Agostino E, Maes F, Vandermeulen D, Hahn HK, Lagae L, Stiers P (2007): Linear normalization of MR brain images in pediatric patients with periventricular leukomalacia. NeuroImage 35:686-697.
39. Manjón JV, Coupé P, Martí-Bonmatí L, Collins DL, Robles M (2010): Adaptive non-local means denoising of MR images with spatially varying noise levels. J Magn Reson Imaging 31:192-203.
40. Mehta S, Grabowski TJ, Trivedi Y, Damasio H (2003): Evaluation of voxel-based morphometry for focal lesion detection in individuals. NeuroImage 20:1438-1454.
41. Moser E, Stahlberg F, Ladd ME, Trattnig S, 2012 7-T MR-From research to clinical applications? NMR Biomed 25:695-716.
42. Muzik O, Chugani DC, Juhász C, Shen C, Chugani HT (2000): Statistical parametric mapping: Assessment of application in children. NeuroImage 12:538-549.
43. Nichols TE (2012): Multiple testing corrections, nonparametric methods, and random field theory. NeuroImage 62:811-815.
44. Nichols TE, Holmes AP (2002): Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum Brain Mapp 15:1-25.
45. Nugent AC, Luckenbaugh DA, Wood SE, Bogers W, Zarate CA Jr, Drevets WC (2013): Automated subcortical segmentation using FIRST: Test-retest reliability, interscanner reliability, and comparison to manual segmentation. Hum Brain Mapp 34:2313-2329.
46. Ogg RJ, Laningham FH, Clarke D, Einhaus S, Zou P, Tobias ME, Boop FA (2009): Passive range of motion functional magnetic resonance imaging localizing sensorimotor cortex in sedated children. J Neurosurg Pediatr 4:317-322.
47. Paus T (2010): Population neuroscience: Why and how. Hum Brain Mapp 31:891-903.
48. Perona P, Malik J (1990): Scale-space and edge detection using anisotropic diffusion. IEEE Trans Pattern Anal Mach Intell 12:629-639.
49. Peterson BS, Anderson AW, Ehrenkranz R, Staib LH, Tageldin M, Colson E, Gore JC, Duncan CC, Makuch R, Ment LR (2003): Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics 111:939-948.
50. Rademacher J, Caviness VS Jr, Steinmetz H, Galaburda AM (1993): Topographical variation of the human primary cortices: Implications for neuroimaging, brain mapping, and neurobiology. Cereb Cortex 3:313-329.
51. Rademacher J, Bürgel U, Zilles K (2002): Stereotaxic localization, intersubject variability, and interhemispheric differences of the human auditory thalamocortical system. NeuroImage 17:142-160.
52. Raschle N, Zuk J, Ortiz-Mantilla S, Sliva DD, Franceschi A, Grant PE, Benasich AA, Gaab N (2012): Pediatric neuroimaging in early childhood and infancy: Challenges and practical guidelines. Ann N Y Acad Sci 1252:43-50.
53. Reiss AL, Abrams MT, Singer HS, Ross JL, Denckla MB (1996): Brain development, gender and IQ in children. A volumetric imaging study. Brain 119:1763-1774.
54. Rivkin MJ (2000): Developmental neuroimaging of children using magnetic resonance techniques. Ment Retard Dev Disabil Res Rev 6:68-80.
55. Salmond CH, Ashburner J, Vargha-Khadem F, Connelly A, Gadian DG, Friston KJ (2002): Distributional assumptions in voxel-based morphometry. NeuroImage 17:1027-1030.
56. Scarpazza C, Sartori G, De Simone MS, Mechelli A (2013): When the single matters more than the group: Very high false positive rates in single case Voxel Based Morphometry. NeuroImage 70:175-188.
57. Schaer M, Eliez S (2007): From genes to brain: Understanding brain development in neurogenetic disorders using neuroimaging techniques. Child Adolesc Psychiatr Clin N Am 16:557-579.
58. Schmithorst VJ, Wilke M, Dardzinski BJ, Holland SK (2005): Cognitive functions correlate with white matter architecture in a normal pediatric population: A diffusion tensor MRI study. Hum Brain Mapp 26:139-147.
59. Seghier ML, Ramlackhansingh A, Crinion J, Leff AP, Price CJ (2008): Lesion identification using unified segmentation-normalisation models and fuzzy clustering. NeuroImage 41:1253-1566.
60. Sled JG, Zijdenbos AP, Evans AC (1998): A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87-97.
61. Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Markesbery WR (2007): Age and gender effects on human brain anatomy: A voxel-based morphometric study in healthy elderly. Neurobiol Aging 28:1075-87.
62. Thirion B, Pinel P, Me'riaux S, Roche A, Dehaene S, Poline JB (2007): Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses. NeuroImage 35:105-120.
63. Tohka J, Zijdenbos A, Evans A (2004): Fast and robust parameter estimation for statistical partial volume models in brain MRI. NeuroImage 23:84-97.
64. Unser M (1999): Splines: A perfect fit for signal and image processing. IEEE Sign Proc Mag 16:22-38.
65. White SH (2000): Conceptual foundations of IQ testing. Psychol Pub Pol Law 6:33-43.
66. Wilke M (2012a): An alternative approach towards assessing and accounting for individual motion in fMRI timeseries. NeuroImage 59:2062-2072.
67. Wilke M (2012b): An iterative jackknife approach for assessing reliability and power of FMRI group analyses. PLoS One 7: E35578.
68. Wilke M, Holland SK (2003): Variability of gray and white matter during normal development: A voxel-based MRI analysis. Neuroreport 14:1887-1890.
69. Wilke M, Holland SK (2008): Structural MR-Imaging studies of the brain in children: Issues and opportunities. Neuroembryol Aging 5:6-13.
70. Wilke M, Schmithorst VJ, Holland SK (2003a): Normative pediatric brain data for spatial normalization and segmentation differs from standard adult data. Magn Reson Med 50:749-757.
71. Wilke M, Kassubek J, Ziyeh S, Schulze-Bonhage A, Huppertz HJ (2003b): Automated detection of gray matter malformations using optimized voxel-based morphometry: A systematic approach. NeuroImage 20:330-343.
72. Wilke M, Schmithorst VJ (2006): A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data. NeuroImage 33:522-530.
73. Wilke M, Krägeloh-Mann I, Holland SK (2007): Global and local development of gray and white matter volume in normal children and adolescents. Exp Brain Res 178:296-307.
74. Wilke M, Schmithorst VJ, Holland SK (2002): Assessment of spatial normalization of whole-brain magnetic resonance images in children. Hum Brain Mapp 17:48-60.
75. Wilke M, de Haan B, Juenger H, Karnath HO (2011): Manual, semi-automated, and automated delineation of chronic brain lesions: A comparison of methods. NeuroImage 56:2038-2046.
76. Woermann FG, Free SL, Koepp MJ, Ashburner J, Duncan JS (1999): Voxel-by-voxel comparison of automatically segmented cerebral gray matter-A rater-independent comparison of structural MRI in patients with epilepsy. NeuroImage 10:373-384.
77. Yoon U, Fonov VS, Perusse D, Evans AC; Brain Development Cooperative Group (2009): The effect of template choice on morphometric analysis of pediatric brain data. NeuroImage 45:769-777.
78. Yuan W, Mangano FT, Air EL, Holland SK, Jones BV, Altaye M, Bierbrauer K (2009): Anisotropic diffusion properties in infants with hydrocephalus: A diffusion tensor imaging study. Am J Neuroradiol 30:1792-1798.