Accelerated corpus callosum development in prematurity predicts improved outcome

Human Brain Mapping

Volumn 36, Issue 10, 2015, Pages 3733-3748

  Thompson, Deanne K ^a,b,c   Lee, Katherine J ^a,c   van Bijnen, Loeka ^a   Leemans, Alexander ^d   Pascoe, Leona ^a   Scratch, Shannon E ^a   Cheong, Jeanie ^c,e   Egan, Gary F ^b,f   Inder, Terrie E ^g,h   Doyle, Lex W ^a,c,e   Anderson, Peter J ^a,c,h  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^e ROYAL WOMEN'S HOSPITAL   (Australia)

^f MONASH UNIVERSITY   (Australia)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

diffusion weighted imaging; MRI; Neurodevelopment; Preterm; White matter

Indexed keywords

ACADEMIC ACHIEVEMENT; ARTICLE; ATTENTION; BIRTH WEIGHT; BODY GROWTH; BRAIN DEVELOPMENT; BRAIN SIZE; CHILD; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; FEMALE; FRACTIONAL ANISOTROPY; GESTATIONAL AGE; HUMAN; INFANT; INTELLIGENCE; MAJOR CLINICAL STUDY; MALE; MATHEMATICS; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NUCLEAR MAGNETIC RESONANCE SCANNER; OUTCOME ASSESSMENT; POSTERIOR COMMISSURE; PREMATURITY; PRIORITY JOURNAL; SCHOOL CHILD; SEX DIFFERENCE; VISION; WORKING MEMORY; ANISOTROPY; BRAIN; CHILD DEVELOPMENT; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREDICTIVE VALUE; PRESCHOOL CHILD;

ANISOTROPY; BRAIN; CHILD; CHILD DEVELOPMENT; CHILD, PRESCHOOL; CORPUS CALLOSUM; FEMALE; GESTATIONAL AGE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT; INFANT, EXTREMELY PREMATURE; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; MALE; PREDICTIVE VALUE OF TESTS;

EID: 84942254049     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22874     Document Type: Article

References (75)

1. Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992): Individual differences in brain asymmetries and fiber composition in the human corpus callosum. Brain Res 598:154-161.
2. Allin MPG, Kontis D, Walshe M, Wyatt J, Barker GJ, Kanaan RAA, McGuire P, Rifkin L, Murray RM, Nosarti C (2011): White matter and cognition in adults who were born preterm. PLoS One 6:e24525.
3. Anderson PJ, Doyle LW (2008): Cognitive and educational deficits in children born extremely preterm. Semin Perinatol 32:51-58.
4. Anjari M, Srinivasan L, Allsop JM, Hajnal JV, Rutherford MA, Edwards AD, Counsell SJ (2007): Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. NeuroImage 35:1021-1027.
5. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC (2001): Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21:1302-1312.
6. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003): Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077-1088.
7. Bloom JS, Hynd GW (2005): The role of the corpus callosum in interhemispheric transfer of information: Excitation or inhibition? Neuropsychol Rev 15:59-71.
8. Caldu X, Narberhaus A, Junque C, Gimenez M, Vendrell P, Bargallo N, Segarra D, Botet F (2006): Corpus callosum size and neuropsychologic impairment in adolescents who were born preterm. J Child Neurol 21:406-410.
9. Chiarello C, Welcome SE, Leonard CM (2012): Individual differences in reading skill and language lateralisation: A cluster analysis. Laterality 17:225-251.
10. Cole TJ, Freeman JV, Preece MA (1998): British 1990 growth reference centiles for weight, height, body mass index and head circumference fitted by maximum penalized likelihood. Stat Med 17:407-429.
11. Constable RT, Ment LR, Vohr BR, Kesler SR, Fulbright RK, Lacadie C, Delancy S, Katz KH, Schneider KC, Schafer RJ, Makuch RW, Reiss AR (2008): Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: An investigation of group and gender effects. Pediatrics 121:306-316.
12. Counsell SJ, Shen Y, Boardman JP, Larkman DJ, Kapellou O, Ward P, Allsop JM, Cowan FM, Hajnal JV, Edwards AD, Rutherford MA (2006): Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 117:376-386.
13. Doron KW, Gazzaniga MS (2008): Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 44:1023-1029.
14. Eikenes L, Lohaugen GC, Brubakk AM, Skranes J, Haberg AK (2011): Young adults born preterm with very low birth weight demonstrate widespread white matter alterations on brain DTI. NeuroImage 54:1774-1785.
15. Feldman HM, Lee ES, Loe IM, Yeom KW, Grill-Spector K, Luna B (2012): White matter microstructure on diffusion tensor imaging is associated with conventional magnetic resonance imaging findings and cognitive function in adolescents born preterm. Dev Med Child Neurol 54:809-814.
16. Fine JG, Semrud-Clikeman M, Keith TZ, Stapleton LM, Hynd GW (2007): Reading and the corpus callosum: An MRI family study of volume and area. Neuropsychology 21:235-241.
17. Fischl B (2012): FreeSurfer. NeuroImage 62:774-781.
18. Funnell MG, Corballis PM, Gazzaniga MS (2000): Insights into the functional specificity of the human corpus callosum. Brain 123:920-926.
19. Giedd JN, Blumenthal J, Jeffries NO, Rajapakse JC, Vaituzis AC, Liu H, Berry YC, Tobin M, Nelson J, Castellanos FX (1999): Development of the human corpus callosum during childhood and adolescence: A longitudinal MRI study. Prog Neuropsychopharmacol Biol Psychiatry 23:571-588.
20. Hasegawa T, Yamada K, Morimoto M, Morioka S, Tozawa T, Isoda K, Murakami A, Chiyonobu T, Tokuda S, Nishimura A, Nishimura T, Hosoi H (2011): Development of Corpus callosum in preterm infants is affected by the prematurity: In vivo assessment of diffusion tensor imaging at term-equivalent age. Pediatr Res 69:249-254.
21. Henderson SE, Sugden DA, Barnett AL (2007): Movement Assessment Battery for Children-second edition (Movement ABC-2). London, UK: The Psychological Corporation.
22. Hofer S, Frahm J (2006): Topography of the human corpus callosum revisited-Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. NeuroImage 32:989-994.
23. Jenkinson M, Smith S (2001): A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143-156.
24. Jones DK (2004): The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: A Monte Carlo study. Magn Reson Med 51:807-815.
25. Jones DK, Knosche TR, Turner R (2013): White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI. NeuroImage 73:239-254.
26. Kerr-Wilson CO, Mackay DF, Smith GC, Pell JP (2012): Meta-analysis of the association between preterm delivery and intelligence. J Public Health (Oxf) 34:209-216.
27. Keshavan MS, Diwadkar VA, DeBellis M, Dick E, Kotwal R, Rosenberg DR, Sweeney JA, Minshew N, Pettegrew JW (2002): Development of the corpus callosum in childhood, adolescence and early adulthood. Life Sci 70:1909-1922.
28. Kidokoro H, Neil JJ, Inder TE (2013): New MR imaging assessment tool to define brain abnormalities in very preterm infants at term. AJNR Am J Neuroradiol 34:2208-2214.
29. Kikinis R, Shenton ME, Gerig G, Martin J, Anderson M, Metcalf D, Guttmann CR, McCarley RW, Lorensen, W, Cline H, et al. (1992): Routine quantitative analysis of brain and cerebrospinal fluid spaces with MR imaging. J Magn Reson Imaging 2:619-629.
30. Kontis D, Catani M, Cuddy M, Walshe M, Nosarti C, Jones D, Wyatt J, Rifkin L, Murray R, Allin M (2009): Diffusion tensor MRI of the corpus callosum and cognitive function in adults born preterm. Neuroreport 20:424-428.
31. LaMantia AS, Rakic P (1990): Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. J Neurosci 10:2156-2175.
32. Lawrence EJ, Allen GM, Walshe M, Allin M, Murray R, Rifkin L, McGuire PK, Nosarti C (2010): The corpus callosum and empathy in adults with a history of preterm birth. J Int Neuropsychol Soc 16:716-720.
33. Leemans A, Jones DK (2009): The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:1336-1349.
34. Leemans A, Jeurissen B, Sijbers J, Jones DK (2009): ExploreDTI: A graphical toolbox for processing, analyzing, and visualizing diffusion MR data. Hawaii. p. 3537.
35. Lubsen J, Vohr B, Myers E, Hampson M, Lacadie C, Schneider KC, Katz KH, Constable RT, Ment LR (2011): Microstructural and functional connectivity in the developing preterm brain. Semin Perinatol 35:34-43.
36. Malinger G, Zakut H (1993): The corpus callosum: Normal fetal development as shown by transvaginal sonography. AJR Am J Roentgenol 161:1041-1043.
37. Manly T, Robertson IH, Anderson V, Nimmo-Smith I (1999): TEA-Ch: The Test of Everyday Attention for Children. Bury St. Edmunds, England: Thames Valley Test Company.
38. Martin N (2006): Test of Visual Perceptual Skills, Third Edition (TVPS-3). Novato, CA: Academic Therapy Publications.
39. Mathew P, Pannek K, Snow P, D'Acunto MG, Guzzetta A, Rose SE, Colditz PB, Finnigan S (2013): Maturation of corpus callosum anterior midbody is associated with neonatal motor function in eight preterm-born infants. Neural Plast 2013:359532
40. Mathur AM, Neil JJ, Inder TE (2010): Understanding brain injury and neurodevelopmental disabilities in the preterm infant: The evolving role of advanced magnetic resonance imaging. Semin Perinatol 34:57-66.
41. Melhem ER, Itoh R, Jones L, Barker PB (2000): Diffusion tensor MR imaging of the brain: Effect of diffusion weighting on trace and anisotropy measurements. AJNR Am J Neuroradiol 21:1813-1820.
42. Molloy CS, Wilson-Ching M, Anderson VA, Roberts G, Anderson PJ, Doyle LW; Victorian Infant Collaborative Study Group (2013): Visual processing in adolescents born extremely low birth weight and/or extremely preterm. Pediatrics 132:e704-12.
43. Mukherjee P, McKinstry RC (2006): Diffusion tensor imaging and tractography of human brain development. Neuroimaging Clin N Am 16:19-43, vii.
44. Mullen KM, Vohr BR, Katz KH, Schneider KC, Lacadie C, Hampson M, Makuch RW, Reiss AL, Constable RT, Ment LR (2011): Preterm birth results in alterations in neural connectivity at age 16 years. NeuroImage 54:2563-2570.
45. Murray AL, Scratch SE, Thompson DK, Inder TE, Doyle LW, Anderson JF, Anderson PJ (2014): Neonatal brain pathology predicts adverse attention and processing speed outcomes in very preterm and/or very low birth weight children. Neuropsychology 28:552-532.
46. Nagy Z, Westerberg H, Skare S, Andersson JL, Lilja A, Flodmark O, Fernell E, Holmberg K, Bohm B, Forssberg H, Lagercrantz H, Klingberg T (2003): Preterm children have disturbances of white matter at 11 years of age as shown by diffusion tensor imaging. Pediatr Res 54:672-679.
47. Narberhaus A, Segarra D, Caldu X, Gimenez M, Junque C, Pueyo R, Botet F (2007): Gestational age at preterm birth in relation to corpus callosum and general cognitive outcome in adolescents. J Child Neurol 22:761-765.
48. Ng WHA, Chan YL, Au KSA, Yeung KWD, Kwan TF, To CY (2005): Morphometry of the corpus callosum in Chinese children: Relationship with gender and academic performance. Pediatr Radiol 35:565-571.
49. Nosarti C, Rushe TM, Woodruff PW, Stewart AL, Rifkin L, Murray RM (2004): Corpus callosum size and very preterm birth: Relationship to neuropsychological outcome. Brain 127:2080-2089.
50. Omizzolo C, Scratch SE, Stargatt R, Kidokoro H, Thompson DK, Lee KJ, Cheong J, Neil J, Inder TE, Doyle LW, Anderson PJ (2014): Neonatal brain abnormalities and memory and learning outcomes at 7 years in children born very preterm. Memory 22:605-615.
51. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, Katz KH, Westerveld M, Sparrow S, Anderson AW, Duncan CC, Makuch RW, Gore JC, Ment LR (2000): Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 284:1939-1947.
52. Pickering S, Gathercole S (2001): Working Memory Test Battery for Children-Manual. London. The Psychological Corporation.
53. Rademaker KJ, Lam JN, Van Haastert IC, Uiterwaal CS, Lieftink AF, Groenendaal F, Grobbee DE, de Vries LS (2004): Larger corpus callosum size with better motor performance in prematurely born children. Semin Perinatol 28:279-287.
54. Reidy N, Morgan A, Thompson DK, Inder TE, Doyle LW, Anderson PJ (2013): Impaired language abilities and white matter abnormalities in children born very preterm and/or very low birth weight. J Pediatr 162:719-724.
55. Ren T, Anderson A, Shen WB, Huang H, Plachez C, Zhang J, Mori S, Kinsman SL, Richards LJ (2006): Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. Anat Rec A Discov Mol Cell Evol Biol 288:191-204.
56. Rose J, Butler EE, Lamont LE, Barnes PD, Atlas SW, Stevenson DK (2009): Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev Med Child Neurol 51:526-535.
57. Semel E, Wiig E, Secord W (2006): Clinical Evaluation of Language Fundamentals-4th Edition, Australian Standardised Edition (CELF-4 Australian). London: Harcourt.
58. Shin YW, Kim DJ, Ha TH, Park HJ, Moon WJ, Chung EC, Lee JM, Kim IY, Kim SI, Kwon JS (2005): Sex differences in the human corpus callosum: Diffusion tensor imaging study. Neuroreport 16:795-798.
59. Skiold B, Horsch S, Hallberg B, Engstrom M, Nagy Z, Mosskin M, Blennow M, Aden U (2010): White matter changes in extremely preterm infants, a population-based diffusion tensor imaging study. Acta Paediatrica 99:842-849.
60. Stewart AL, Rifkin L, Amess PN, Kirkbride V, Townsend JP, Miller DH, Lewis SW, Kingsley DP, Moseley IF, Foster O, Murray RM (1999): Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm. Lancet 353:1653-1657.
61. Thompson DK, Inder TE, Faggian N, Johnston L, Warfield SK, Anderson PJ, Doyle LW, Egan GF (2011): Characterization of the corpus callosum in very preterm and full-term infants utilizing MRI. NeuroImage 55:479-490.
62. Thompson DK, Inder TE, Faggian N, Warfield SK, Anderson PJ, Doyle LW, Egan GF (2012): Corpus callosum alterations in very preterm infants: Perinatal correlates and 2 year neurodevelopmental outcomes. NeuroImage 59:3571-3581.
63. Tournier JD, Calamante F, Connelly A (2012): MRtrix: Diffusion tractography in crossing fiber regions. Int J Imag Syst Tech 22:53-66.
64. van der Knaap MS, Valk J (1995): Magnetic Resonance of Myelination and Myelin Disorders. Berlin: Springer-Verlag.
65. van Kooij BJ, de Vries LS, Ball G, van Haastert IC, Benders MJ, Groenendaal F, Counsell SJ (2012): Neonatal tract-based spatial statistics findings and outcome in preterm infants. AJNR Am J Neuroradiol 33:188-194.
66. van Pul C, van Kooij BJ, de Vries LS, Benders MJ, Vilanova A, Groenendaal F (2012): Quantitative fiber tracking in the corpus callosum and internal capsule reveals microstructural abnormalities in preterm infants at term-equivalent age. AJNR Am J Neuroradiol 33:678-684.
67. Vangberg TR, Skranes J, Dale AM, Martinussen M, Brubakk AM, Haraldseth O (2006): Changes in white matter diffusion anisotropy in adolescents born prematurely. NeuroImage 32:1538-1548.
68. Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B (2013): Weighted linear least squares estimation of diffusion MRI parameters: Strengths, limitations, and pitfalls. NeuroImage 81:335-346.
69. Volpe JJ (2009): Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110-124.
70. Wechsler D (1999): Wechsler Abbreviated Scale of Intelligence (WASI). The Psychological Corporation.
71. Westerhausen R, Kreuder F, Woerner W, Huster RJ, Smit CM, Schweiger E, Wittling W (2006): Interhemispheric transfer time and structural properties of the corpus callosum. Neurosci Lett 409:140-145.
72. Wilkinson GS, Robertson GJ (2005): Wide Range Achievement Test, 4th ed. Wilmington: Delaware.
73. Williams J, Lee KJ, Anderson PJ (2010): Prevalence of motor-skill impairment in preterm children who do not develop cerebral palsy: A systematic review. Dev Med Child Neurol 52:232-237.
74. Witelson SF (1985): The brain connection: The corpus callosum is larger in left-handers. Science 229:665-668.
75. Witelson SF (1989): Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. Brain 112:799-835.