Hindbrain regional growth in preterm newborns and its impairment in relation to brain injury

Human Brain Mapping

Volumn 37, Issue 2, 2016, Pages 678-688

  Kim, Hosung ^a   Gano, Dawn ^a   Ho, Mai Lan ^b   Guo, Xiaoyue M ^a   Unzueta, Alisa ^a   Hess, Christopher ^a   Ferriero, Donna M ^a   Xu, Duan ^a   Barkovich, A James ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Hindbrain regional growth; Neonatal brain MRI; Preterm newborns; Surface based morphometry

Indexed keywords

ARTICLE; BRAIN DEVELOPMENT; BRAIN FOURTH VENTRICLE; BRAIN GROWTH; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN MAPPING; BRAIN STEM; CEREBELLUM; CEREBELLUM HEMORRHAGE; DISEASE SEVERITY; FEMALE; HUMAN; IMAGE PROCESSING; INFERIOR COLLICULUS; MAJOR CLINICAL STUDY; MALE; MORPHOGENESIS; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PERINATAL DEVELOPMENT; PONS; PONS ANGLE; PREMATURITY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SUPERIOR COLLICULUS; ADULT; BRAIN DISEASES; GROWTH, DEVELOPMENT AND AGING; INFANT; NEWBORN INTENSIVE CARE; ORGAN SIZE; PATHOLOGY; RHOMBENCEPHALON; SEVERITY OF ILLNESS INDEX; THREE DIMENSIONAL IMAGING;

ADULT; BRAIN DISEASES; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; INFANT; INFANT, PREMATURE; INTENSIVE CARE, NEONATAL; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; RHOMBENCEPHALON; SEVERITY OF ILLNESS INDEX;

EID: 84955211404     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23058     Document Type: Article

References (51)

1. Almli CR, Rivkin MJ, McKinstry RC (2007): The NIH MRI study of normal brain development (Objective-2): Newborns, infants, toddlers, and preschoolers. Neuroimage 35:308-325.
2. Anderson P, Doyle LW, Victorian Infant Collaborative Study G (2003): Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. JAMA 289:3264-3272.
3. Apps R, Hawkes R (2009): Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10:670-681.
4. Argyropoulou MI, Xydis V, Drougia A, Argyropoulou PI, Tzoufi M, Bassounas A, Andronikou S, Efremidis SC (2003): MRI measurements of the pons and cerebellum in children born preterm; associations with the severity of periventricular leukomalacia and perinatal risk factors. Neuroradiology 45:730-734.
5. Barkovich AJ, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns WB (2001): Classification system for malformations of cortical development: Update 2001. Neurology 57:2168-2178.
6. Benjamini Y, Hochberg Y (1995): Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Royal Stat Soc 57:289-300.
7. Bhutta AT, Cleves MA, Casey PH, Cradock MM, Anand KJS (2002): Cognitive and behavioral outcomes of school-aged children who were born preterm - A meta-analysis. JAMA 288:728-737.
8. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, Adler A, Garcia CV, Rohde S, Say L, Lawn JE (2012): National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: A systematic analysis and implications. Lancet 379:2162-2172.
9. Chung MK, Worsley KJ, Nacewicz BM, Dalton KM, Davidson RJ (2010): General multivariate linear modeling of surface shapes using SurfStat. Neuroimage 53:491-505.
10. Dastjerdi FV, Consalez GG, Hawkes R (2012): Pattern formation during development of the embryonic cerebellum. Front Neuroanat 6:10.
11. Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL, Brain Development Cooperative G (2011): Unbiased average age-appropriate atlases for pediatric studies. Neuroimage 54:313-327.
12. Gerig G, Styner M, Jones D, Weinberg DR, Lieberman J (2001): Shape analysis of brain ventricles using SPHARM. MMBIA 171-178.
13. Geva R, Schreiber J, Segal-Caspi L, Markus-Shiffman M (2014): Neonatal brainstem dysfunction after preterm birth predicts behavioral inhibition. J Child Psychol Psychol 55:802-810.
14. Gilthorpe JD, Papantoniou EK, Chedotal A, Lumsden A, Wingate RJ (2002): The migration of cerebellar rhombic lip derivatives. Development 129:4719-4728.
15. Grojean S, Koziel V, Vert P, Daval JL (2000): Bilirubin induces apoptosis via activation of NMDA receptors in developing rat brain neurons. Exp Neurol 166:334-341.
16. Haldipur P, Gillies GS, Janson OK, Chizhikov VV, Mithal DS, Miller RJ, Millen KJ (2014): Foxc1 dependent mesenchymal signalling drives embryonic cerebellar growth. eLife 3:e03962.
17. Hoekstra RE, Ferrara TB, Couser RJ, Payne NR, Connett JE (2004): Survival and long-term neurodevelopmental outcome of extremely premature infants born at 23-26 weeks' gestational age at a tertiary center. Pediatrics 113:E1-E6.
18. Holland D, Chang LD, Ernst TM, Curran M, Buchthal SD, Alicata D, Skranes J, Johansen H, Hernandez A, Yamakawa R, Kuperman JM, Dale AM (2014): Structural growth trajectories and rates of change in the first 3 months of infant brain development. JAMA Neurol 71:1266-1274.
19. Imamura T, Ariga H, Kaneko M, Watanabe M, Shibukawa Y, Fukuda Y, Nagasawa K, Goto A, Fujiki T (2013): Neurodevelopmental outcomes of children with periventricular leukomalacia. Pediatr Neonatol 54:367-372.
20. Joo EY, Kim H, Suh S, Hong SB (2014): Hippocampal substructural vulnerability to sleep disturbance and cognitive impairment in patients with chronic primary insomnia: Magnetic resonance imaging morphometry. Sleep 37:1189-1198.
21. Kliegman RM, Hack M, Jones P, Fanaroff AA (1982): Epidemiologic-study of necrotizing enterocolitis among low-birth-weight infants - Absence of identifiable risk-factors. J Pediatr 100:440-444.
22. Kim H, Besson P, Colliot O, Bernasconi A, Bernasconi N (2008): Surface-based vector analysis using heat equation interpolation: A new approach to quantify local hippocampal volume changes. Med Image Comput Assist Interv 5241:1008-1015.
23. Kim H, Mansi T, Bernasconi N (2013): Disentangling hippocampal shape anomalies in epilepsy. Front Neurol 4:131.
24. Kiss JZ, Vasung L, Petrenko V (2014): Process of cortical network formation and impact of early brain damage. Curr Opin Neurol 27:133-141.
25. Knickmeyer RC, Gouttard S, Kang C, Evans D, Wilber K, Smith JK, Hamer RM, Lin W, Gerig G, Gilmore JH (2008): A structural MRI study of human brain development from birth to 2 years. J Neurosci 28:12176-12182.
26. Lind A, Parkkola R, Lehtonen L, Munck P, Maunu J, Lapinleimu H, Haataja L, Group PS (2011): Associations between regional brain volumes at term-equivalent age and development at 2 years of age in preterm children. Pediatr Radiol 41:953-961.
27. Messerschmidt A, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Pollak A, Weber M, Birnbacher R (2008): Preterm birth and disruptive cerebellar development: Assessment of perinatal risk factors. Eur J Paediatr Neurol 12:455-460.
28. Miller SP, Cozzio CC, Goldstein RB, Ferriero DM, Partridge JC, Vigneron DB, Barkovich AJ (2003): Comparing the diagnosis of white matter injury in premature newborns with serial MR imaging and transfontanel ultrasonography findings. AJNR Am J Neuroradiol 24:1661-1669.
29. Miller SP, Ferriero DM, Leonard C, Piecuch R, Glidden DV, Partridge JC, Perez M, Mukherjee P, Vigneron DB, Barkovich AJ (2005): Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr 147:609-616.
30. Morita T, Morimoto M, Yamada K, Hasegawa T, Morioka S, Kidowaki S, Moroto M, Yamashita S, Maeda H, Chiyonobu T, Tokuda S, Hosoi H (2015): Low-grade intraventricular hemorrhage disrupts cerebellar white matter in preterm infants: Evidence from diffusion tensor imaging. Neuroradiology 57:507-514.
31. Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2004): Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg 100:672-678.
32. Nowakowska-Kotas M, Kedzia A, Dudek K (2014): Development of external surfaces of human cerebellar lobes in the fetal period. Cerebellum 13:541-548.
33. Papile LA, Burstein J, Burstein R, Koffler H (1978): Incidence and evolution of subependymal and intraventricular hemorrhage: A study of infants with birth weights less than 1, 500 gm. J Pediatr 92:529-534.
34. Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung HY, Nosarti C, Santosh P, Rifkin L, Wyatt J, Murray RM, Allin M (2008): Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. Brain 131:1344-1351.
35. Payne AH, Hintz SR, Hibbs AM, Walsh MC, Vohr BR, Bann CM, Wilson-Costello DECEKSNI (2013): Neurodevelopmental outcomes of extremely low-gestational-age neonates with low-grade periventricular-intraventricular hemorrhage. JAMA Pediatr 167:451-459.
36. Rakic P, Sidman RL (1970): Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans. J Comp Neurol 139:473-500.
37. Sato K, Ishigame K, Ying SH, Oishi K, Miller MI, Mori S (2015): Macro- and microstructural changes in patients with spinocerebellar ataxia type 6: assessment of phylogenetic subdivisions of the cerebellum and the brain stem. Am J Neuroradiol, 36:84-90.
38. Sidman RL, Rakic P (1973): Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1-35.
39. Skiold B, Alexandrou G, Padilla N, Blennow M, Vollmer B, Aden U (2014): Sex differences in outcome and associations with neonatal brain morphology in extremely preterm children. J Pediatr 164:1012-1018.
40. 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.
41. Sotelo C (2004): Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295-339.
42. Styner M, Oguz I, Xu S, Brechbühler C, Pantazis D, Gerig G (2006): Statistical Shape Analysis of Brain Structures Using SPHARM-PDM. MICCAI 2006 Opensource workshop.
43. Tam EW, Chau V, Ferriero DM, Barkovich AJ, Poskitt KJ, Studholme C, Fok ED, Grunau RE, Glidden DV, Miller SP (2011a): Preterm cerebellar growth impairment after postnatal exposure to glucocorticoids. Sci Transl Med 3:105ra105.
44. Tam EW, Miller SP, Studholme C, Chau V, Glidden D, Poskitt KJ, Ferriero DM, Barkovich AJ (2011b): Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth. J Pediatr 158:366-371.
45. Tam EWY (2013): Potential mechanisms of cerebellar hypoplasia in prematurity. Neuroradiology 55:41-46.
46. ten Donkelaar HJ, Lammens M, Wesseling P, Thijssen HO, Renier WO (2003): Development and developmental disorders of the human cerebellum. J Neurol 250:1025-1036.
47. Van Braeckel KNJA, Taylor HG (2013): Visuospatial and visuomotor deficits in preterm children: The involvement of cerebellar dysfunctioning. Dev Med Child Neurol 55:19-22.
48. Van Kooij BJM, Benders MJNL, Anbeek P, Van Haastert IC, De Vries LS, Groenendaal F (2012): Cerebellar volume and proton magnetic resonance spectroscopy at term, and neurodevelopment at 2 years of age in preterm infants. Dev Med Child Neurol 54:260-266.
49. Wang VY, Zoghbi HY (2001): Genetic regulation of cerebellar development. Nat Rev Neurosci 2:484-491.
50. Yan J, Chen C, Hu Q, Yang X, Lei J, Yang L, Wang K, Qin L, Huang H, Zhou C (2008): The role of p53 in brain edema after 24 h of experimental subarachnoid hemorrhage in a rat model. Exp Neurol 214:37-46.
51. Yoo JYJ, Mak GK, Goldowitz D (2014): The effect of hemorrhage on the development of the postnatal mouse cerebellum. Exp Neurol 252:85-94.