Seminars in Pediatric Neurology
Volume 16, Issue 4 , Pages 226-236 , December 2009

A History of Our Understanding of Cerebral Vascular Development and Pathogenesis of Perinatal Brain Damage Over the Past 30 Years

  • Sachio Takashima, MD

      Affiliations

    • Yanagawa Institute for Developmental Disabilities, International University of Health and Welfare, Fukuoka, Japan
    • Corresponding Author InformationAddress reprint requests to Sachio Takashima, Yanagawa Institute for Developmental Disabilities, 284-2 Kamimiyanaga-machi, Yanagawa, Fukuoka 832-0059, Japan
  • ,
  • Masayuki Itoh, MD

      Affiliations

    • Division of Mental Retardation and Birth Defect Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan
  • ,
  • Akira Oka, MD

      Affiliations

    • Department of Pediatrics, Kyorin University Faculty of Medicine, Tokyo, Japan

References 

  1. Friede RL. Developmental Neuropathology. Berlin: Springer-Verlag; 1989;
  2. DeReuck J, Chattha AS, Richardson KP. Pathogenesis and evolution of periventricular leukomalacia in infancy. Arch Neurol. 1972;27:229–236
  3. Takashima S, Tanaka K. Development of cerebrovascular architecture and its relationship to periventricular leukomalacia. Arch Neurol. 1978;25:3–11
  4. Nakamura Y, Okudera T, Hashimoto T. Vascular architecture in white matter of neonates: Its relationship to periventricular leukomalacia. J Neuropathol Exp Neurol. 1994;53:582–589
  5. Nelson MD, Gonzalez-Gomez I, Gilles FH. The search for human telencephalic ventriculofugal arteries. AJNR Am J Neuroradiol. 1991;12:223–228
  6. Takashima S, Tanaka K. Microangiography and vascular permeability of the subependymal matrix in the premature infant. Can J Neurol Sci. 1978;5:45–50
  7. Kamei A, Houdou S, Mito T, et al. Developmental change in type VI collagen in human cerebral vessels. Pediatr Neurol. 1992;8:183–186
  8. Mito T, Konomi H, Houdou S, et al. Immunohistochemical study of the vasculature in the developing brain. Pediatr Neurol. 1991;7:18–22
  9. Miyawaki T, Matsui K, Takashima S. Developmental characteristics of vessel density in the human fetal and infant brains. Early Hum Dev. 1998;53:65–72
  10. Deguchi K, Mizuguchi M, Takashima S. Immunohistochemical expression of tumor necrosis factor alpha in neonatal leukomalacia. Pediatr Neurol. 1996;14:13–16
  11. Takashima S, Becker LE, Nishimura M, et al. Developmental changes of glial fibrillary acidic protein and myelin basic protein in perinatal leukomalacia: Relationship to a predisposing factor. Brain Dev. 1984;6:444–450
  12. Takashima S, Becker LE. Developmental neuropathology in bronchopulmonary dysplasia: Alteration of glial fibrillary acidic protein and myelination. Brain Dev. 1984;6:451–457
  13. Hirayama A, Oka A, Ito M, et al. Myelin transcription factor 1 (MyT1) immunoreactivity in infants with periventricular leukomalacia. Brain Res Dev Brain Res. 2003;140:85–92
  14. Takashima S, Mito T, Ando Y. Pathogenesis of periventricular white matter hemorrhages in preterm infants. Brain Dev. 1986;8:25–30
  15. Fukumizu M, Takashima S, Becker LE. Neonatal posthemorrhagic hydrocephalus: Neuropathologic and immunohistochemical studies. Pediatr Neurol. 1995;13:230–234
  16. Takashima S. Olivocerebellar lesions in infants born prematurely. Brain Dev. 1982;4:361–366
  17. Ohyu J, Takashima S. Decreased expression of microtubule-associated protein 5 (MAP 5) in the molecular layer of cerebellum in preterm infants with olivocerebellar lesions. Brain Dev. 1998;20:22–26
  18. Inage YW, Itoh M, Wada K, et al. Glutamate transporters in neonatal cerebellar subarachnoid hemorrhage. Pediatr Neurol. 2000;23:42–48
  19. Takashima S, Armstrong DL, Becker LE. Subcortical leukomalacia (Relationship to development of the cerebral sulcus and its vascular supply). Arch Neurol. 1978;35:470–472
  20. Houdou S, Takashima S, Takeshita K, et al. Infantile subcortical leukohypodensity demonstrated by computed tomography. Pediatr Neurol. 1988;4:165–167
  21. Arai Y, Deguchi K, Takashima S. Vascular endothelial growth factor in brains with periventricular leukomalacia. Pediatr Neurol. 1998;19:45–49
  22. Iida K, Takashima S, Takeuchi Y, et al. Neuropathologic study of newborns with prenatal-onset leukomalacia. Pediatr Neurol. 1993;9:45–48
  23. Iida K, Takashima S, Takeuchi Y. Etiologies and distribution of neonatal leukomalacia. Pediatr Neurol. 1992;8:205–209
  24. Arai Y, Deguchi K, Mizuguchi M, et al. Expression of amyloid precursor protein in axons of periventricular leukomalacia brains. Pediatr Neurol. 1995;13:161–163
  25. Deguchi K, Oguchi K, Takashima S. Characteristic neuropathology of leukomalacia in extremely low birthweight infants. Pediatr Neurol. 1997;16:296–300
  26. Meng SZ, Arai Y, Deguchi K, et al. Early detection of axonal and neuronal lesions in prenatal-onset periventricular leukomalacia. Brain Dev. 1997;19:480–484
  27. Fujimoto S, Togari H, Takashima S, et al. National survey of periventricular leukomalacia in Japan. Acta Paediatr Jpn. 1998;40:239–243
  28. Hashimoto K, Hasegawa H, Kida Y, et al. Correlation between neuroimaging and neurological outcome in periventricular leukomalacia: Diagnostic outcome in periventricular leukomalacia: Diagnostic criteria. Pediatr Neurol. 2001;43:240–245
  29. Nanba Y, Matsui K, Aida N, et al. Detection of T1 hyperintensity in region of the corona radiata connecting with posterior limb of the internal capsule on magnetic resonance imaging at near term is sensitive in predicting gross motor problems in premature infants. Pediatrics. 2007;120:10–19
  30. Kamei A, Houdou S, Mito T, et al. Developmental change in type VI collagen in human cerebral vessels. Pediatr Neurol. 1992;8:183–186
  31. Inage YW, Itoh M, Takashima S. Correlation between cerebrovascular maturity and periventricular leukomalacia. Pediatr Neurol. 2000;22:204–208
  32. Takashima S, Hirayama A, Okoshi Y, et al. Vascular, axonal and glial pathogenesis of periventricular leukomalacia in fetuses and neonates. Neuroembryology. 2002;1:72–77
  33. Okoshi Y, Itoh M, Takashima S. Characteristic neuropathology and plasticity in periventricular leukomalacia. Pediatr Neurol. 2001;25:221–226
  34. Hirayama A, Okoshi Y, Hachiya Y, et al. Early immunohistochemical detection of axonal damage and glial activation in extremely immature brains with periventricular leukomalacia. Clin Neuropathol. 2001;20:87–91
  35. Hashimoto M, Nishida A, Minakami H, et al. Decreased expression of L-selectin on peripheral blood polymorphonuclear leukocytes in neonates with severe asphyxia. Biol Neonate. 2002;81:95–98
  36. Deguchi K, Oguchi K, Matsuura N, et al. Periventricular leukomalacia: Relation to gestational age and axonal injury. Pediatr Neurol. 1999;20:370–374
  37. Tanaka F, Ozawa Y, Inage Y, et al. Association of osteopontin with ischemic axonal death in periventricular leukomalacia. Acta Neuropathol. 2000;100:69–74
  38. Yoshioka H, Goma H, Nioka S, et al. Bilateral carotid artery occlusion causes periventricular leukomalacia in neonatal dogs. Brain Res. 1994;78:273–278
  39. Ohyu J, Marumo G, Ozawa H, et al. Early axonal and glial pathology in fetal sheep brains with leukomalacia induced by repeated umbilical cord occlusion. Brain Dev. 1999;21:248–252
  40. Marumo G, Kozuma S, Ohyu J, et al. Generation of periventricular leukomalacia by repeated umbilical cord occlusion in near-term fetal sheep and its possible pathogenetical mechanisms. Biol Neonate. 2001;79:39–45
  41. Gilles FH, Marphy SF. Perinatal telencephalic leukoencephalopathy. J Neurol Neurosurg Psychiatry. 1969;32:404–413
  42. Young RSK, Hernandez MJ, Yagel SK. Selective reduction of blood flow to white matter during hypotension in newborn dogs: A possible mechanism of periventricular leukomalacia. Ann Neurol. 1982;12:445–448
  43. Takashima S, Ohno K, Ando M. Pathogenesis of perinatal leukomalacia: Neonatal brain and behavior. H In:  Yabuuchi K,  Watanabe S editor. Okada Nagoya: University Nagoya Press; 1987;p. 45–52
  44. Ando M, Takashima S, Mito T. Endotoxin, cerebral blood flow, amino acids and brain damage in young rabbits. Brain Dev. 1988;10:365–370
  45. Zupan V, Gonzalez P, Lacaze-Masmonteil T, et al. Periventricular leukomalacia: Risk factors revisited. Dev Med Child Neurol. 1996;38:1061–1067
  46. Yoon BH, Romero R, Yang SH, et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol. 1996;174:1433–1440
  47. Mallard C, Welin AK, Peebles D, et al. White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res. 2003;28:215–223
  48. Duncan JR, Cock ML, Suzuki K, et al. Chronic endotoxin exposure causes brain injury in the ovine fetus in the absence of hypoxemia. J Soc Gynecol Invest. 2006;13:87–96
  49. Meng S, Takashima S. Expression of transforming growth factor-betha 1 in periventricular leukomalacia. J Child Neurol. 1999;14:377–381
  50. Iida K, Takashima S, Ueda K. Immunohistochemical study of myelination and oligodendrocyte in infants with periventricular leukomalacia. Pediatr Neurol. 1995;13:296–304
  51. Hirayama A, Oka A, Ito M, et al. Myelin transcription factor 1 (MyT1) immunoreactivity in infants with periventricular leukomalacia. Brain Res Dev Brain Res. 2003;140:85–92
  52. Okoshi Y, Mizuguchi M, Itoh M, et al. Altered nestin expression in the cerebrum with periventricular leukomalacia. Pediatr Neurol. 2007;36:170–174
  53. Iai M, Takashima S. Thalamocortical development of parvalbumin neurons in normal and periventricular leukomalacia brains. Neuropediatrics. 1999;30:14–18
  54. Resch B, Radinger A, Mannhalter C, et al. Interleukin-6 G(-174)C polymorphism is associated with mental retardation in cystic periventricular leukomalacia in preterm infants. Arch Dis Child Fetal Neonatal Ed. 2009;94:F304–F306
  55. Friede RL. Pontosubicular lesions of gray matter in perinatal anoxia. Arch Pathol. 1972;94:343–354
  56. Bruck Y, Bruck W, Kretzschmar HA, et al. Evidence for neuronal apoptosis in pontosubicular neuron necrosis. Neuropathol Appl Neurobiol. 1996;22:23–29
  57. Sohma O, Mito T, Mizuguchi M, et al. The prenatal age critical for the development of the pontosubicular necrosis. Acta Neuropathol. 1995;90:7–10
  58. Takashima S, Mito T, Houdou S, et al. Hypoxic-ischemic brain damage: Detection of early stage. No To Hattatsu (Japanese). 1991;23:147–152
  59. Mito T, Kamei A, Takashima S, et al. Clinicopathological study of pontosubicular necrosis. Neuropediatrics. 1993;24:204–207
  60. Mitani A, Watanabe M, Kataoka K. Functional change of NMDA receptors related to enhancement of susceptibility to neurotoxicity in the developing pontine nucleus. J Neurosci. 1998;18:7941–7952
  61. Ahdab-Barmada M, Moossy J, Painter M. Pontosubicular necrosis and hyperoxemia. Pediatrics. 1980;66:840–847
  62. Hashimoto K, Takeuchi Y, Takashima S. Hypocarbia as a pathogenetic factor in pontosubicular necrosis. Brain Dev. 1991;13:155–157
  63. Takizawa Y, Takashima S, Itoh M. A histopathological study of premature and mature infants with pontosubicular neuron necrosis: Neuronal cell death in perinatal brain damage. Brain Res. 2006;1095:200–206
  64. Taylor DL, Edwards AD, Mehmet H. Oxidative metabolism, apoptosis and perinatal brain damage. Brain Pathol. 1999;9:93–117
  65. Yue X, Mehmet H, Penrice J, et al. Apoptosis and necrosis in newborn piglet brain following transient cerebral hypoxic-ischemia. Neuropathol Appl Neurobiol. 1997;23:16–25
  66. Walton M, Connor B, Lawlor P, et al. Neuronal death and survival in two models of hypoxic-ischemic brain damage. Brain Res Brain Res Rev. 1999;29:137–168
  67. Ohyu J, Endo A, Itoh M, et al. Hypocapnia under hypotension induces apoptotic neuronal cell death in the hippocampus of newborn rabbits. Pediatr Review. 2000;48:24–29
  68. Isumi H, Uchida Y, Hayashi T, et al. Neuron death and glial response in pontosubicular necrosis (The role of the growth inhibition factor). Clin Neuropathol. 2000;19:77–84
  69. Ozawa H, Nishida A, Mito T, et al. Ferritin immunohistochemical study on pontine nuclei from infants with pontosubicular neuron necrosis. Brain Dev. 1995;17:20–23
  70. Arai Y, Mizuguchi M, Ikeda K, et al. Transient expression of apolipoprotein-E in neonates with pontosubicular neuron necrosis. Acta Neuropathol (Berl). 1996;91:396–399
  71. Ozawa H, Fukuda T, Nishida A, et al. Cu, Zn-superoxide dismutase reaction in neonatal pontosubicular neuron necrosis. Pediatr Neurol. 1997;16:126–130
  72. Itakura A, Kurauchi O, Takashima S, et al. Immunological detection of 4-hydroxynonenal protein adducts in developing pontine and Purkinje neurons and in karyorrhexis in pontosubicular neuronal necrosis. Early Hum Dev. 2002;67:19–28
  73. Stadelman C, Mews I, Srinivasan A, et al. Expression of cell death-associated proteins in neuronal apoptosis associated with pontosubicular neuron necrosis. Brain Pathol. 2001;11:273–281
  74. Rossiter JP, Anderson LL, Yang F, et al. Caspase-3 activation and caspase-like proteolytic activity in human perinatal hypoxic-ischemic brain injury. Acta Neuropathol. 2002;103:66–73
  75. van Landeghem FK, Felder-Mueser U, Moysich A, et al. Fas (CD95/Apo-1)/ Fas ligand expression in neonates with pontosubicular neuron necrosis. Pediatr Res. 2002;51:129–135
  76. Meng SZ, Itoh M, Obonai T, et al. Roles of glutamate transporter and receptors, poly (ADPribose) polymerase, and transforming growth factor-beta1 in pontosubicular neuron necrosis. J Child Neurol. 2000;15:362–369

PII: S1071-9091(09)00062-X

doi: 10.1016/j.spen.2009.09.004

Seminars in Pediatric Neurology
Volume 16, Issue 4 , Pages 226-236 , December 2009