Deformation-based morphometry of prospective neurodevelopmental changes in new onset paediatric epilepsy

Brain

Volumn 134, Issue 4, 2011, Pages 1003-1014

  Tosun, Duygu ^a   Dabbs, Kevin ^b   Caplan, Rochelle ^c   Siddarth, Prabha ^c   Toga, Arthur ^d   Seidenberg, Michael ^e   Hermann, Bruce ^b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

deformation based morphometry; idiopathic generalized epilepsy; localization related epilepsy; MRI; new and recent onset epilepsy; prospective neurodevelopment changes

Indexed keywords

ANTICONVULSIVE AGENT;

ADOLESCENT; ADULT; ATTENTION DEFICIT DISORDER; BENIGN CHILDHOOD EPILEPSY; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MAPPING; BRAIN STEM; CEREBELLUM; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DEFORMATION BASED MORPHOMETRY; ELECTROENCEPHALOGRAM; FEMALE; GRAY MATTER; HUMAN; INTELLIGENCE QUOTIENT; MALE; MORPHOMETRICS; NERVE CELL DIFFERENTIATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PONS; PRIORITY JOURNAL; REVIEW; THALAMUS; WHITE MATTER;

ADOLESCENT; BRAIN; BRAIN MAPPING; CHILD; EPILEPSY; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE;

EID: 79953652242     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr027     Document Type: Review

References (98)

1. Abreu L, Issler C, Lafer B. Valproate-induced reversible pseudoatrophy of the brain and hyperammonemic encephalopathy in a bipolar patient. Aust N Z J Psychiatry 2009; 43: 484-5.
2. Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR, et al. Diffusion tensor imaging of the corpus callosum in Autism. Neuroimage 2007; 34: 61-73. (Pubitemid 44765248)
3. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B 1995; 57: 289-300.
4. Berg AT, Shinnar S, Levy SR, Testa FM, Smith-Rapaport S, Beckerman B. Early development of intractable epilepsy in children: a prospective study. Neurology 2001; 56: 1445-52. (Pubitemid 32532255)
5. Bernhardt BC, Rozen DA, Worsley KJ, Evans AC, Bernasconi N, Bernasconi A. Thalamo-cortical network pathology in idiopathic generalized epilepsy: insights from MRI-based morphometric correlation analysis. Neuroimage 2009; 46: 373-81.
6. Betting LE, Mory SB, Li LM, Lopes-Cendes I, Guerreiro MM, Guerreiro CA, et al. Voxel-based morphometry in patients with idio-pathic generalized epilepsies. Neuroimage 2006a; 32: 498-502. (Pubitemid 44164624)
7. Betting LE, Mory SB, Lopes-Cendes I, Li LM, Guerreiro MM, Guerreiro CA, et al. MRI reveals structural abnormalities in patients with idiopathic generalized epilepsy. Neurology 2006b; 67: 848-52. (Pubitemid 44394201)
8. Betting LE, Mory SB, Lopes-Cendes I, Li LM, Guerreiro MM, Guerreiro CA, et al. MRI volumetry shows increased anterior thalamic volumes in patients with absence seizures. Epilepsy Behav 2006c; 8: 575-80.
9. Budde MD, Kim JH, Liang HF, Schmidt RE, Russell JH, Cross AH, et al. Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn Reson Med 2007; 57: 688-95. (Pubitemid 46731794)
10. Caplan R, Levitt J, Siddarth P, Wu KN, Gurbani S, Sankar R, et al. Frontal and temporal volumes in Childhood Absence Epilepsy. Epilepsia 2009a; 50: 2466-72.
11. Caplan R, Siddarth P, Levitt J. Language and fronto-temporal volumes in pediatric epilepsy. Epilepsia 2009b; 50: 2466-72.
12. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS, et al. Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 2002; 288: 1740-8.
13. Cormack F, Gadian DG, Vargha-Khadem F, Cross JH, Connelly A, Baldeweg T. Extra-hippocampal grey matter density abnormalities in paediatric mesial temporal sclerosis. Neuroimage 2005; 27: 635-43. (Pubitemid 41139935)
14. Daley M, Ott D, Blanton R, Siddarth P, Levitt J, Mormino E, et al. Hippocampal volume in childhood complex partial seizures. Epilepsy Res 2006; 72: 57-66. (Pubitemid 44637211)
15. Daley M, Siddarth P, Levitt J, Gurbani S, Shields WD, Sankar R, et al. Amygdala volume and psychopathology in childhood complex partial seizures. Epilepsy Behav 2008; 13: 212-7.
16. Dam M. Organic changes in phenytoin-intoxicated pigs. Acta Neurol Scand 1966; 42: 491-4.
17. Dam M. Number of Purkinje cells in patients with grand mal epilepsy treated with diphenylhydantoin. Epilepsia 1970; 11: 313-20.
18. Dam M, Bolwig T, Hertz M, Bajorec J, Lomax P, Dam AM. Does seizure activity produce Purkinje cell loss? Epilepsia 1984; 25: 747-51. (Pubitemid 15196268)
19. Dam M, Nielsen M. Purkinje's cell density after diphenylhydantoin intoxication in rats. Arch Neurol 1970; 23: 555-7.
20. De Araújo Filho GM, Jackowski AP, Lin K, Guaranha MSB, Guilhoto LMFF, da Silva HH, et al. Personality traits related to juvenile myoclonic epilepsy: MRI reveals prefrontal abnormalities through a voxel-based morphometry study. Epilepsy Behav 2009; 15: 202-7.
21. del Cerro M, Snider RS. Studies on dilantin intoxication. Neurology 1967; 17: 452-66.
22. Engel J Jr. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 2001; 42: 796-803. (Pubitemid 32605946)
23. Finkleman I, Arieff AJ. Untoward effects of phenytoin sodium in epilepsy. JAMA 1942; 118: 1209-12.
24. Galimberti CA, Diegoli M, Sartori I, Uggetti C, Brega A, Tartara A, et al. Brain pseudoatrophy and mental regression on valproate and a mito-chondrial DNA mutation. Neurology 2006; 67: 1715-7. (Pubitemid 44747961)
25. Gessaga EC, Urich H. The cerebellum of epileptics. Clin Neuropathol 1985; 4: 238-45. (Pubitemid 16201953)
26. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999; 2: 861-3. (Pubitemid 30602596)
27. Giedd JN, Lalonde FM, Celano MJ, White SL, Wallace GL, Lee NR, et al. Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J Am Acad Child Adolesc Psychiatry 2009; 48: 465-70.
28. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 2004; 101: 8174-9. (Pubitemid 38698073)
29. Gogtay N, Lu A, Leow AD, Klunder AD, Lee AD, Chavez A, et al. Three-dimensional brain growth abnormalities in childhood-onset schizophrenia visualized by using tensor-based morphometry. Proc Natl Acad Sci USA 2008; 105: 15979-84.
30. Gogtay N, Ordonez A, Herman DH, Hayashi KM, Greenstein D, Vaituzis C, et al. Dynamic mapping of cortical development before and after the onset of pediatric bipolar illness. J Child Psychol Psychiatry 2007; 48: 852-62. (Pubitemid 47244898)
31. Govindan RM, Makki MI, Sundaram SK, Juhasz C, Chugani HT. Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy. Epilepsy Res 2008; 80: 30-41.
32. Greenstein D, Lerch J, Shaw P, Clasen L, Giedd J, Gochman P, et al. Childhood onset schizophrenia: cortical brain abnormalities as young adults. J Child Psychol Psychiatry 2006; 47: 1003-12. (Pubitemid 44642429)
33. Guerrini R, Belmonte A, Canapicchi R, Casalini C, Perucca E. Reversible pseudoatrophy of the brain and mental deterioration associated with valproate treatment. Epilepsia 1998; 39: 27-32. (Pubitemid 28116838)
34. Guimaraes CA, Bonilha L, Franzon RC, Li LM, Cendes F, Guerreiro MM. Distribution of regional gray matter abnormalities in a pediatric population with temporal lobe epilepsy and correlation with neuropsycho-logical performance. Epilepsy Behav 2007; 11: 558-66. (Pubitemid 350177380)
35. Hasan KM, Kamali A, Iftikhar A, Kramer LA, Papanicolaou AC, Fletcher JM, et al. Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan. Brain Res 2009; 1249: 91-100.
36. Hermann BP, Lin JJ, Jones JE, Seidenberg M. The emerging architecture of neuropsychological impairment in epilepsy. Neurologic Clinics 2009; 27: 881-907.
37. Hermann B, Hansen R, Seidenberg M, Magnotta V, O'Leary D. Neurodevelopmental vulnerability of the corpus callosum to childhood onset localization-related epilepsy. Neuroimage 2003; 18: 284-92. (Pubitemid 36269140)
38. Hermann B, Jones J, Sheth R, Dow C, Koehn M, Seidenberg M. Children with new-onset epilepsy: neuropsychological status and brain structure. Brain 2006; 129 (Pt 10): 2609-19. (Pubitemid 44522094)
39. Hermann B, Seidenberg M, Bell B, Rutecki P, Sheth R, Ruggles K, et al. The neurodevelopmental impact of childhood-onset temporal lobe epilepsy on brain structure and function. Epilepsia 2002; 43: 1062-71. (Pubitemid 35006482)
40. Hermann BP, Dabbs K, Becker T, Jones JE, Myers Y Gutierrez A, Wendt G, et al. Brain development in children with new onset epilepsy: A prospective controlled cohort investigation. Epilepsia 2010; 51: 2038-46.
41. Holmes MD, Quiring J, Tucker DM. Evidence that juvenile myoclonic epilepsy is a disorder of frontotemporal corticothalamic networks. Neuroimage 2010; 49: 80-93.
42. Honavar M, Meldrum B. Epilepsy. In: Graham DI, Lantos PL, editors. Greenfield's neuropathology. London: Edward Arnold; 2002. p. 899-941.
43. Hua X, Leow AD, Levitt JG, Caplan R, Thompson PM, Toga AW. Detecting brain growth patterns in normal children using tensor-based morphometry. Hum Brain Mapp 2009; 30: 209-19.
44. Hutchinson E, Pulsipher D, Dabbs K, Gutierrez AMy, Sheth R, Jones J, et al. Children with new-onset epilepsy exhibit diffusion abnormalities in cerebral white matter in the absence of volumetric differences. Epilepsy Res 2010; 88: 208-14.
45. Ikonomidou C, Turski L. Antiepileptic drugs and brain development. Epilepsy Res 2010; 88: 11-22.
46. Joshi S, Davis B, Jomier M, Gerig G. Unbiased diffeomorphic atlas construction for computational anatomy. Neuroimage 2004; 23 (Suppl 1): S151-60. (Pubitemid 39421714)
47. Kim JH, Lee JK, Koh SB, Lee SA, Lee JM, Kim SI, et al. Regional grey matter abnormalities in juvenile myoclonic epilepsy: a voxel-based morphometry study. Neuroimage 2007; 37: 1132-7. (Pubitemid 47385285)
48. Kochunov P, Lancaster J, Thompson P, Toga AW, Brewer P, Hardies J, et al. An optimized individual target brain in the Talairach coordinate system. Neuroimage 2002; 17: 922-7. (Pubitemid 35317025)
49. Kokenge R, Kutt H, McDowell F. Neurological sequelae following Dilantin overdose in a patient and in experimental animals. Neurology 1965; 15: 823-9.
50. Lawson JA, Cook MJ, Bleasel AF, Nayanar V, Morris KF, Bye AM. Quantitative MRI in outpatient childhood epilepsy. Epilepsia 1997; 38: 1289-93. (Pubitemid 28007518)
51. Lawson JA, Nguyen W, Bleasel AF, Pereira JK, Vogrin S, Cook MJ, et al. ILAE-defined epilepsy syndromes in children: correlation with quantitative MRI. Epilepsia 1998; 39: 1345-9. (Pubitemid 29005636)
52. Lawson JA, Vogrin S, Bleasel AF, Cook MJ, Burns L, McAnally L, et al. Predictors of hippocampal, cerebral, and cerebellar volume reduction in childhood epilepsy. Epilepsia 2000a; 41: 1540-5. (Pubitemid 32002726)
53. Lawson JA, Vogrin S, Bleasel AF, Cook MJ, Bye AM. Cerebral and cere-bellar volume reduction in children with intractable epilepsy. Epilepsia 2000b; 41: 1456-62.
54. Lazaro L, Bargallo N, Castro-Fornieles J, Falcon C, Andres S, Calvo R, et al. Brain changes in children and adolescents with obsessive-compulsive disorder before and after treatment: a voxel-based morphometric MRI study. Psychiatry Res 2009; 172: 140-6.
55. Lenroot RK, Giedd JN. Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev 2006; 30: 718-29. (Pubitemid 44292283)
56. Leow AD, Klunder AD, Jack CR Jr, Toga AW, Dale AM, Bernstein MA, et al. Longitudinal stability of MRI for mapping brain change using tensor-based morphometry. Neuroimage 2006; 31: 627-40. (Pubitemid 44218807)
57. Lindvall O, Nilsson B. Cerebellar atrophy following phenytoin intoxication. Ann Neurol 1984; 16: 258-60. (Pubitemid 14062677)
58. Marsh R, Gerber AJ, Peterson BS. Neuroimaging studies of normal brain development and their relevance for understanding childhood neuro-psychiatric disorders. J Am Acad Child Adolesc Psychiatry 2008; 47: 1233-51.
59. McLachlan R. Pseudoatrophy of the brain with valproic acid monother-apy. Can J Neurol Sci 1987.
60. McLain LW, Martin JT, Allen JH. Cerebellar degeneration due to chronic phenytoin therapy. Ann Neurol 1980; 7: 18-23. (Pubitemid 10129565)
61. Ment LR, Kesler S, Vohr B, Katz KH, Baumgartner H, Schneider KC, et al. Longitudinal brain volume changes in preterm and term control subjects during late childhood and adolescence. Pediatrics 2009; 123: 503-11.
62. Ney GC, Lantos G, Barr WB, Schaul N. Cerebellar atrophy in patients with long-term phenytoin exposure and epilepsy. Arch Neurol 1994; 51: 767-71. (Pubitemid 24242600)
63. Nielsen MH, Dam M, Klinken L. The ultrastructure of Purkinje cells in diphenylhydantoin intoxicated rats. Exp Brain Res 1971; 12: 447-56.
64. Nilsson D, Go C, Rutka JT, Rydenhag B, Mabbott DJ, Snead OC 3rd, et al. Bilateral diffusion tensor abnormalities of temporal lobe and cin-gulate gyrus white matter in children with temporal lobe epilepsy. Epilepsy Res 2008; 81: 128-35.
65. Pardoe H, Pell GS, Abbott DF, Berg AT, Jackson GD. Multi-site voxel-based morphometry: methods and a feasibility demonstration with childhood absence epilepsy. Neuroimage 2008; 42: 611-6.
66. Paus T, Keshavan M, Giedd JN. Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 2008; 9: 947-57.
67. Paus T, Zijdenbos A, Worsley K, Collins DL, Blumenthal J, Giedd JN, et al. Structural maturation of neural pathways in children and adolescents: in vivo study. Science 1999; 283: 1908-11.
68. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000; 284: 1939-47.
69. Pulsipher DT, Dabbs K, Tuchsherer V, Sheth R, Koehn MA, Hermann BP, et al. Thalamofrontal neurodevelopment in new-onset pediatric idio-pathic generalized epilepsy. Neurology 2011; 76: 28-33.
70. Pulsipher DT, Seidenberg M, Guidotti L, Tuchscherer VN, Morton J, Sheth RD, et al. Thalamofrontal circuitry and executive dysfunction in recent-onset juvenile myoclonic epilepsy. Epilepsia 2009; 50: 1210-19.
71. Rapoport JL, Giedd JN, Blumenthal J, Hamburger S, Jeffries N, Fernandez T, et al. Progressive cortical change during adolescence in childhood-onset schizophrenia. A longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 1999; 56: 649-54. (Pubitemid 29315637)
72. Riley JD, Franklin DL, Choi V, Kim RC, Binder DK, Cramer SC, et al. Altered white matter integrity in temporal lobe epilepsy: Association with cognitive and clinical profiles. Epilepsia 2010; 51 (4): 536-45.
73. Salcman M, Defendini R, Correll J, Gilman S. Neuropathological changes in cerebellar biopsies of epileptic patients. Ann Neurol 1978 Jan;3(1):10-9.
74. Seidenberg M, Kelly KG, Parrish J, Geary E, Dow C, Rutecki P, et al. Ipsilateral and contralateral MRI volumetric abnormalities in chronic unilateral temporal lobe epilepsy and their clinical correlates. Epilepsia 2005; 46: 420-30. (Pubitemid 40365648)
75. Shattuck DW, Leahy RM. BrainSuite: an automated cortical surface identification tool. Med Image Anal 2002; 6: 129-42. (Pubitemid 35282822)
76. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci USA 2007; 104: 19649-54.
77. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, et al. Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 2008; 28: 3586-94.
78. Shaw P, Lerch J, Greenstein D, Sharp W, Clasen L, Evans A, et al. Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 2006; 63: 540-9.
79. Shinnar S, Pellock JM. Update on the epidemiology and prognosis of pediatric epilepsy. J Child Neurol 2002; 17 (Suppl 1): S4-17.
80. Sillanpaa M, Haataja L, Shinnar S. Perceived impact of childhood-onset epilepsy on quality of life as an adult. Epilepsia 2004; 45: 971-7. (Pubitemid 39062822)
81. Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imag 1998; 17: 87-97. (Pubitemid 128742012)
82. Snook L, Paulson LA, Roy D, Phillips L, Beaulieu C. Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 2005; 26: 1164-73. (Pubitemid 40806495)
83. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26: 132-40. (Pubitemid 40602893)
84. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW. Mapping cortical change across the human life span. Nat Neurosci 2003; 6: 309-15. (Pubitemid 36278290)
85. Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW. Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 2004; 24: 8223-31. (Pubitemid 39280801)
86. Studholme C, Cardenas V, Blumenfeld R, Schuff N, Rosen HJ, Miller B, et al. Deformation tensor morphometry of semantic dementia with quantitative validation. NeuroImage 2004; 21: 1387-98. (Pubitemid 38450721)
87. Studholme C, Drapaca C, Iordanova B, Cardenas V. Deformation-based mapping of volume change from serial brain MRI in the presence of local tissue contrast change. Med Imag. IEEE Trans 2006; 25: 626-39.
88. Sullivan J, Dlugos D. Idiopathic generalized epilepsy. Curr Treat Opt Neurol 2004; 6: 231-42. (Pubitemid 38915127)
89. Tae WS, Hong SB, Joo EY, Han SJ, Cho JW, Seo DW, et al. Structural brain abnormalities in juvenile myoclonic epilepsy patients: volumetry and voxel-based morphometry. Korean J Radiol 2006; 7: 162-72. (Pubitemid 44371901)
90. Tae WS, Kim SH, Joo EY, Han SJ, Kim IY, Kim SI, et al. Cortical thickness abnormality in juvenile myoclonic epilepsy. J Neurol 2008; 255: 561-6.
91. Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, et al. Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 2005; 309: 2226-8. (Pubitemid 41396074)
92. Toga AW, Thompson PM, Sowell ER. Mapping brain maturation. Trends Neurosci 2006; 29: 148-59.
93. Utterback RA, Ojeman R, Malek J. Parenchymatous cerebellar degeneration with Dilantin intoxication. J Neuropathol Exp Neurol 1958; 17: 516-9.
94. Van't Ent D, Lehn H, Derks EM, Hudziak JJ, Van Strien NM, Veltman DJ, et al. A structural MRI study in monozygotic twins concordant or discordant for attention/hyperactivity problems: evidence for genetic and environmental heterogeneity in the developing brain. NeuroImage 2007, 35, 1004-20. (Pubitemid 46507840)
95. Wassink TH, Hazlett HC, Epping EA, Arndt S, Dager SR, Schellenberg GD, et al. Cerebral cortical gray matter overgrowth and functional variation of the serotonin transporter gene in autism. Arch Gen Psychiatry 2007; 64: 709-17. (Pubitemid 46878671)
96. Weber B, Luders E, Faber J, Richter S, Quesada CM, Urbach H, et al. Distinct regional atrophy in the corpus callosum of patients with temporal lobe epilepsy. Brain 2007; 130: 3149-54. (Pubitemid 350209063)
97. Wilke M, Krageloh-Mann I, Holland SK. Global and local development of gray and white matter volume in normal children and adolescents. Exp Brain Res 2007; 178: 296-307. (Pubitemid 46440574)
98. World Medical Association. Declaration of Helsinki. J Law Med Ethics 1991; 19: 264-5.