Skip to main content
Springer Nature Link
Log in

Perinatal Panencephalopathy in Premature Infants: Is It Due to Hypoxia-Ischemia?

  • Chapter
Brain Hypoxia and Ischemia

Part of the book series: Contemporary Clinical Neuroscience ((CCNE))

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Volpe JJ. Cerebral white matter injury of the premature infant – more common than you think. Pediatrics 2003; 112: 176–180.

    PubMed  Google Scholar 

  2. Woodward LJ, Edgin JO, Thompson D, Inder TE. Object working memory deficits predicted by early brain injury and development in the preterm infant. Brain 2005; 128: 2578–2587.

    PubMed  Google Scholar 

  3. Ancel PY, Livinec F, Larroque B, et al. Cerebral palsy among very preterm children in relation to gestational age and neonatal ultrasound abnormalities: The EPIPAGE cohort study. Pediatrics 2006; 117: 828–835.

    PubMed  Google Scholar 

  4. Nosarti C, Giouroukou E, Micall N, Rifkin L, Morris RG, Murray RM. Impaired executive functioning in young adults born very preterm. J Int Neuropsychol Soc 2007; 13: 571–581.

    PubMed  Google Scholar 

  5. Volpe JJ. Neurology of the Newborn. 4th ed. Philadelphia, PA: WB Saunders, 2001.

    Google Scholar 

  6. Pierson CR, Folkerth RD, Billiards SS, Trachtenberg FL, Drinkwater ME, Volpe JJ, Kinney HC. Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 2007; 114: 619–631.

    PubMed  Google Scholar 

  7. Kinney HC, Panigrahy A, Newburger JW, Jonas RA, Sleeper LA. Hypoxic-ischemic brain injury in infants with congenital heart disease dying after cardiac surgery. Acta Neuropathol 2005; 110: 563–578.

    PubMed  Google Scholar 

  8. Dammann O, Kuban KCK, Leviton A. Perinatal infection, fetal inflammatory response, white matter damage, and cognitive limitations in children born preterm. Ment Retard Dev Disabil Res Rev 2002; 8: 46–50.

    PubMed  Google Scholar 

  9. Nelson KB. Is it HIE? Any why that matters. Acta Paediatr 2007; 96: 1113–1114.

    PubMed  Google Scholar 

  10. Kumar V, Abbas AK, Fausto N. Robbins and Cotran pathologic basis of disease. Philadelphia, PA: Elsevier Saunders, 2005, pp. 21–25.

    Google Scholar 

  11. Kinney HC, Haynes RL, Folkerth RD. White matter disorders in the perinatal period. In: Golden JA, Harding BN (eds). Pathology and Genetics: Acquired and Inherited Diseases of the Developing Nervous System. Basel: ISN Neuropathology Press, 2004, pp. 156–170.

    Google Scholar 

  12. Banker BQ, Larroche JC. Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. Arch Neurol 1962; 7: 386–410.

    CAS  PubMed  Google Scholar 

  13. Armstrong DL, Sauls CD, Goddard-Finegold J. Neuropathologic findings in short-term survivors of intraventricular hemorrhage. Am J Dis Child 1987; 141: 617–621.

    CAS  PubMed  Google Scholar 

  14. Armstrong D, Norman MG. Periventricular leucomalacia in neonates. Complications and sequelae. Arch Dis Child 1974; 49: 367–375.

    CAS  PubMed  Google Scholar 

  15. DeReuck J, Chattha AS, Richardson E Jr. Pathogenesis and evolution of periventricular leu-komalacia in infancy. Arch Neurol 1972; 27: 229–236.

    CAS  PubMed  Google Scholar 

  16. Marin Padilla M. Developmental neuropathology and impact of perinatal brain damage. III. Gray matter lesions of the neocortex. J Neuropathol Exp Neurol 1999; 58: 407–429.

    Google Scholar 

  17. 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. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000; 284: 1939–1947.

    CAS  PubMed  Google Scholar 

  18. Inder TE, Warfield SK, Wang H, Huppi PS, Volpe JJ. Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005; 115: 286–294.

    PubMed  Google Scholar 

  19. Lin Y, Okumura A, Hayakawa F, Kato K, Kuno T, Watanabe K. Quantitative evaluation of thalami and basal ganglia in infants with periventricular leukomalacia. Dev Med Child Neurol 2001; 43: 481–485.

    CAS  PubMed  Google Scholar 

  20. Ricci D, Anker S, Cowan F, Pane M, Gallini F, Luciano R, Donvito V, Baranello G, Cesarini L, Bianco F, Rutherford M, Romagnoli C, Atkinson J, Braddick O, Guzzetta F, Mercuri E. Thalamic atrophy in infants with PVL and cerebral visual impairment. Early Hum Dev 2006; 82: 591–595.

    PubMed  Google Scholar 

  21. Isaacs EB, Lucas A, Chong WK, Wood SJ, Johnson CL, Marshall C, Vargha-Khadem F, Gadian DG. Hippocampal volume and everyday memory in children of very low birth weight. Pediatr Res 2000; 47: 713–720.

    CAS  PubMed  Google Scholar 

  22. Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ, du Plessis AJ. Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 2005; 116: 844–850.

    PubMed  Google Scholar 

  23. Kinney HC, Armstrong DL. Perinatal neuropathology. In: Graham DI, Lantos PE (eds) Greenfield's Neuropathology. London: Arnold, 2002, pp. 557–559.

    Google Scholar 

  24. Leviton A, Gilles FH. Acquired perinatal leukoencephalopathy. Ann Neurol 1984; 16: 1–8.

    CAS  PubMed  Google Scholar 

  25. Haynes RL, Folkerth RF, Szweda LI, Volpe JJ, Kinney HC. Lipid peroxidation during human cerebral myelination. J Neuropathol Exp Neurol 2006; 65: 894–904.

    CAS  PubMed  Google Scholar 

  26. Haynes RL, Folkerth RD, Keefe RJ, Sung I, Swzeda LI, Rosenberg PA, Volpe JJ, Kinney HC. Nitrosative and oxidative injury to premyelinating oligodendrocytes is accompanied by micro-glial activation in periventricular leukomalacia in the human premature infant. J Neuropathol Exp Neurol 2003; 62: 441–450.

    PubMed  Google Scholar 

  27. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001; 21: 1302–1312.

    CAS  PubMed  Google Scholar 

  28. Back SA, Luo NL, Borenstein NS, Volpe JJ, Kinney HC. Arrested oligodendrocyte lineage progression during human cerebral white matter development: dissociation between the timing of progenitor differentiation and myelinogenesis. J Neuropathol Exp Neurol 2002; 61: 197–211.

    PubMed  Google Scholar 

  29. Back SA, Gan X, Li Y, Rosenberg PR, et al. Maturation-dependent vulnerability of oli-godendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 1998; 18: 6241–6253.

    CAS  PubMed  Google Scholar 

  30. Haynes RL, Baud O, Li J, et al. Oxidative and nitrative injury in periventricular leukomalacia: a review. Brain Pathol 2005; 15: 225–233.

    CAS  PubMed  Google Scholar 

  31. Counsell SJ, Allsop JM, Harrison MC, et al. Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 2003; 112 (Part 1): 1–7.

    PubMed  Google Scholar 

  32. Back SA, Luo NL, Mallinson RA, O'Malley JP, et al. Selective vulnerability of preterm white matter to oxidative damage defined by F(2)-isoprostanes. Ann Neurol 2005; 58: 108–120.

    CAS  PubMed  Google Scholar 

  33. Iida K, Takashima S, Ueda K. Immunohistochemical study of myelination and oligodendro-cyte in infants with periventricular leukomalacia. Pediatr Neurol 1995; 13: 296–304.

    CAS  PubMed  Google Scholar 

  34. Billiards SS, Haynes RL, Folkerth RD, Borenstein NS, Trachtenberg FL, Rowitch DH, Ligon KL, Volpe JJ, Kinney HC. Myelin abnormalities despite total oligodendrocyte cell preservation in periventricular leukomalacia. Brain Pathol 2008; 18: 156–163.

    Google Scholar 

  35. Ligon KL, Kesari S, Kitada M, et al. Development of NG2 neural progenitor cells requires Olig gene function. Proc Natl Acad Sci USA 2006; 103: 7853–7858.

    CAS  PubMed  Google Scholar 

  36. Sur M, Rubenstein JL. Patterning and plastiCity of the cerebral cortex. Science 2005; 310: 805–810.

    CAS  PubMed  Google Scholar 

  37. Monchi O, Petrides M, Strafella AP, Worsley KJ, Doyon J. Functional role of the basal ganglia in the planning and execution of actions. Ann Neurol 2006; 59: 257–264.

    PubMed  Google Scholar 

  38. Leutgeb S, Leutgeb JK, Moser MB, Moser EI. Place cells, spatial maps and the population code for memory. Curr Opin Neurobiol 2005; 15: 738–746.

    CAS  PubMed  Google Scholar 

  39. Schmahmann JD, Caplan D. Cognition, emotion and the cerebellum. Brain 2006; 129: 290–292.

    PubMed  Google Scholar 

  40. Ghosh A, Shatz CJ. A role for subplate neurons in the patterning of connections from thalamus to neocortex. Development 1993; 117: 1031–1047.

    CAS  PubMed  Google Scholar 

  41. McQuillen PS, Ferriero DM. Perinatal subplate neuron injury: implications for cortical development and plastiCity. Brain Pathol 2005; 15: 250–260.

    CAS  PubMed  Google Scholar 

  42. McQuillen PS, Sheldon RA, Shatz CJ, Ferriero DM. Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia. J Neurosci 2003; 23: 3308–3315.

    CAS  PubMed  Google Scholar 

  43. Deguchi K, Oguchi K, Takashima S. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol 1997; 16: 296–300.

    CAS  PubMed  Google Scholar 

  44. Meng SZ, Arai Y, Deguchi K, Takashima S. Early detection of axonal and neuronal lesions in prenatal-onset periventricular leukomalacia. Brain Dev 1997; 19: 480–484.

    CAS  PubMed  Google Scholar 

  45. Arai Y, Deguchi K, Mizuguchi M, et al. Expression of beta-amyloid precursor protein in axons of periventricular leukomalacia brains. Pediatr Neurol 1995; 13: 161–163.

    CAS  PubMed  Google Scholar 

  46. Haynes RL, Billiards SS, Borenstein NS, Volpe JJ, Kinney HC. Diffuse axonal injury in periv-entricular leukomalacia. Pediatr Res 2008; 63: 656–661.

    CAS  PubMed  Google Scholar 

  47. Suurmeijer AJ, van der Wijk J, van Veldhuisen DJ, Yang F, Cole GM. Fractin immunostaining for the detection of apoptotic cells and apoptotic bodies in formalin-fixed and paraffin-embedded tissue. Lab Invest 1999; 79: 619–620.

    CAS  PubMed  Google Scholar 

  48. Underhill SM, Goldberg MP. Hypoxic injury of isolated axons is independent of ionotropic glutamate receptors. Neurobiol Dis 2007; 25: 284–290.

    CAS  PubMed  Google Scholar 

  49. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao M V, Falls DL, Role L, Salzer JL. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2005; 47: 681–694.

    CAS  PubMed  Google Scholar 

  50. Stevens B, Porta S, Haak LL, Gallo V, Fields RD. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 2002; 36: 855–868.

    CAS  PubMed  Google Scholar 

  51. Huppi PS, Murphy B, Maier SE, Zientara GP, Inder TE, Barnes PD, Kikinis R, Jolesz FA, Volpe JJ. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 2001; 107: 455–460.

    CAS  PubMed  Google Scholar 

  52. Counsell SJ, Dyet LE, Larkman DJ, Nunes RG, Boardman JP, Allsop JM, Fitzpatrick J, Srinivasan L, Cowan FM, Hajnal JV, Rutherford MA, Edwards AD. Thalamo-cortical connectivity in children born preterm mapped using probabilistic magnetic resonance tractography. Neuroimage 2007; 34: 896–904.

    PubMed  Google Scholar 

  53. Vangberg TR, Skranes J, Dale AM, Martinussen M, Brubakk AM, Haraldseth O. Changes in white matter diffusion anisotropy in adolescents born prematurely. Neuroimage 2006; 32: 1538–1548.

    PubMed  Google Scholar 

  54. Thomas B, Eyssen M, Peeters R, Molenaers G, Van Hecke P, De Cock P, Sunaert S. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 2005; 128: 2562–2577.

    PubMed  Google Scholar 

  55. Prayer D, Barkovich AJ, Kirschner DA, Prayer LM, Roberts TP, Kucharczyk J, Moseley ME. Visualization of nonstructural changes in early white matter development on diffusion-weighted MR images: evidence supporting premyelination anisotropy. Am J Neuroradiol 2001;22: 1572–1576.

    CAS  PubMed  Google Scholar 

  56. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ. Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms and prevention. J Neurosci 1993; 13: 1441–1453.

    CAS  PubMed  Google Scholar 

  57. Liu Y, Silverstein FS, Skoff R, Barks JDE. Hypoxic-ischemic oligodendroglial injury in neonatal rat brain. Pediatr Res 2002; 51: 25–33.

    PubMed  Google Scholar 

  58. Yoshioka A, Backskai B, Pleasure D. Pathophysiology of oligodendroglial excitotoxiCity. J Neurosci Res 1996; 46: 427–438.

    CAS  PubMed  Google Scholar 

  59. Jelinski SE, Yager J Y, Juurlink BHJ. Preferential injury of oligodendroblasts by a short hypoxic-ischemic insult. Brain Res 1999; 815: 150–153.

    CAS  PubMed  Google Scholar 

  60. Rosenberg PA, Dai W, Gan XD, Ali S, et al. Mature myelin basic protein expressing oli-godendrocytes are insensitive to kainate toxiCity. J Neurosci Res 2003; 71: 237–245.

    CAS  PubMed  Google Scholar 

  61. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, et al. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxiCity. Nat Med 1998; 4: 291–297.

    CAS  PubMed  Google Scholar 

  62. Rao VLR, Bowen KK, Dempsey RJ. Transient focal cerebral ischemia down-regulates glutamate transporters GLT-1 and EAAC1 expression in rat brain. Neurochem Res 2001; 26: 497–502.

    CAS  PubMed  Google Scholar 

  63. Ness JK, Romanko MJ, Rothstein RP, Wood TL, Levison SW. Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors. Dev Neurosci 2001; 23: 203–208.

    CAS  PubMed  Google Scholar 

  64. Sanchez-Gomez MV, Matute C. AMPA and kainate receptors each mediate excitotoxiCity in oligodendroglial cultures. Neurobiol Dis 1999; 6: 475–485.

    CAS  PubMed  Google Scholar 

  65. Back SA, Craig AS, Kayton R, Luo NL, et al. Hypoxia-ischemia preferentially triggers gluta-mate depletion from oligodendroglia and axons in perinatal cerebral white matter. J Cereb Blood Flow Metab 2007; 27: 334–347.

    CAS  PubMed  Google Scholar 

  66. Deng W, Rosenberg PA, Volpe JJ, Jensen FE. Calcium-permeable AMPA/kainate receptors mediate toxiCity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc Natl Acad Sci USA 2003; 100: 6801–6806.

    CAS  PubMed  Google Scholar 

  67. Micu I, Jiang Q, Coderre E, et al. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 2006; 439: 988–992.

    CAS  PubMed  Google Scholar 

  68. Salter MG, Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 2005; 438: 1167–1171.

    CAS  PubMed  Google Scholar 

  69. Deng W, Wang H, Rosenberg PA, Volpe JJ, et al. Role of metabotropic glutamate receptors in oligodendrocyte excitotoxiCity and oxidative stress. Proc Natl Acad Sci USA 2004; 101: 7751–7756.

    CAS  PubMed  Google Scholar 

  70. Deng W, Yue Q, Rosenberg PA, Volpe JJ, et al. Oligodendrocyte excitotoxiCity determined by local glutamate accumulation and mitochondrial function. J Neurochem 2006; 96: 213–222.

    Google Scholar 

  71. Sanchez-Gomez M V, Alberdi E, Ibarretxe G, Torre I, et al. Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J Neurosci 2003; 23; 9519–9528.

    CAS  PubMed  Google Scholar 

  72. Follett P, Rosenberg P, Volpe JJ, Jensen FE. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 2000; 20: 9235–9241.

    CAS  PubMed  Google Scholar 

  73. Yonezawa M, Back SA, Gan X, Rosenberg PA, et al. Cystine deprivation induces oligoden-droglial death: rescue by free radical scavengers and by a diffusible glial factor. J Neurochem 1996; 67: 566–573.

    CAS  PubMed  Google Scholar 

  74. Baud O, Li J, Zhang Y, Neve RL, et al. Nitric oxide-induced cell death in developing oli-godendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eur J Neurosci 2004; 20: 1713–1726.

    PubMed  Google Scholar 

  75. Okuma Y, Uehara T, Miyazaki H, Miyasaka T, et al. The involvement of cytokines, chemok-ines and inducible nitric oxide synthase (iNOS) induced by a transient ischemia in neuronal survival/death in rat brain. Folia Pharmacol 1998; 111: 37–44.

    CAS  Google Scholar 

  76. Bona E, Andersson A-L, Blomgren K, Gilland E, et al. Chemokine and inflammatory cell response to hypoxia-ischemia in immature rats. Pediatr Res 1999; 45: 500–509.

    CAS  PubMed  Google Scholar 

  77. Andrews T, Zhang P, Bhat NR. TNF-α potentiates IFN gamma-induced cell death in oli-godendrocyte progenitors. J Neurosci Res 1998; 54: 574–583.

    CAS  PubMed  Google Scholar 

  78. Folkerth RD, Keefe RJ, Haynes RL, Trachtenberg FL, Volpe JJ, Kinney HC. Interferon-gamma expression in periventricular leukomalacia in the human brain. Brain Pathol 2004; 14: 265–274.

    CAS  PubMed  Google Scholar 

  79. Li J, Baud O, Vartanian T, Volpe JJ, et al. Peroxynitrite generated by inducible nitric oxide syn-thase and NADPH oxidase mediates microglial toxiCity to oligodendrocytes. Proc Natl Acad Sci USA 2005; 102: 9936–9941.

    CAS  PubMed  Google Scholar 

  80. Brown GC. Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans 2007; 35: 1119–1121.

    CAS  PubMed  Google Scholar 

  81. Nakamura Y, Okudera T, et al. Vascular architecture in white matter of neonates: its relationship to periventricular leukomalacia. J Neuropathol Exp Neurol 1994; 53: 582–589.

    CAS  PubMed  Google Scholar 

  82. Takashima S, Tanaka K. Development of cerebrovascular architecture and its relationship to periventricular leukomalacia. Arch Neurol 1978; 35: 11–16.

    CAS  PubMed  Google Scholar 

  83. Kuban KC, Gilles FH. Human telencephalic angiogenesis. Ann Neurol 1985; 17: 539–548.

    CAS  PubMed  Google Scholar 

  84. Rorke LB. Anatomical features of the developing brain implicated in pathogenesis of hypoxic– ischemic injury. Brain Pathol 1992; 2: 211–221.

    CAS  PubMed  Google Scholar 

  85. Van den Bergh R. Centrifugal elements in the vascular pattern of the deep intracerebral blood supply. Angiology 1960; 20: 88–94.

    Google Scholar 

  86. Wigglesworth JS, Pape KE. An integrated model for haemorrhagic and ischaemic lesions in the newborn brain. Early Hum Dev 1978; 2: 179–199.

    CAS  PubMed  Google Scholar 

  87. Altman DI, Powers WJ, Perlman JM, Herscovitch P, et al. Cerebral blood flow requirement for brain viability in newborn infants is lower than in adults. Ann Neurol 1988; 24: 218–226.

    CAS  PubMed  Google Scholar 

  88. Greisen G, Pryds O. Low CBF, discontinuous EEG activity, and periventricular brain injury in ill, preterm neonates. Brain Dev 1989; 11: 164–168.

    CAS  PubMed  Google Scholar 

  89. Borch K, Greisen G. Blood flow distribution in the normal human preterm brain. Pediatr Res 1998; 41: 28–33.

    Google Scholar 

  90. Powers WJ, Grubb RL, Darriet D, Raichle ME. Cerebral blood flow and cerebral metabolic rate of oxygen requirements for cerebral function and viability in humans. J Cereb Blood Flow Metab 1985; 5: 600–608.

    CAS  PubMed  Google Scholar 

  91. Muller AM, Morales C, Briner J, Baenziger O, et al. Loss of CO2 reactivity of cerebral blood flow is associated with severe brain damage in mechanically ventilated very low birth weight infants. Eur J Paediatr Neurol 1997; 5: 157–163.

    Google Scholar 

  92. Pryds O, Edwards AD. Cerebral blood flow in the newborn infant. Arch Dis Child 1996; 74: F63–F69.

    CAS  Google Scholar 

  93. Soul JS, Hammer PE, Tsuji M, Saul P, et al. Fluctuating pressure-passivity is common in the cerebral circulation of sick premature infants. Pediatr Res 2007; 61: 467–473.

    PubMed  Google Scholar 

  94. Tsuji M, Saul JP, du Plessis A, Eichenwald E, et al. Cerebral intravascular oxygenation correlates with mean arterial pressure in critically ill premature infants. Pediatrics 2000; 106: 625–632.

    CAS  PubMed  Google Scholar 

  95. Lemmers PM, Toet M, van Schelven LJ, van Bel F. Cerebral oxygenation and cerebral oxygen extraction in the preterm infant: the impact of respiratory distress syndrome. Exp Brain Res 2006; 173: 458–467.

    PubMed  Google Scholar 

  96. Nelson MD, Gonzalez-Gomez I, Gilles FH. The search for human telencephalic ventriculo-fugal arteries. Am J Neuroradiol 1991; 12: 215–222.

    PubMed  Google Scholar 

  97. von Siebenthal K, Beran J, Wolf M, Keel M, et al. Cyclical fluctuations in blood pressure, heart rate and cerebral blood volume in preterm infants. Brain Dev 1999; 21: 529–534.

    Google Scholar 

  98. Wiswell TE, Graziani LJ, Kornhauser MS, Stanley C, et al. Effects of hypocarbia on the development of cystic periventricular leukomalacia in premature infants treated with high-frequency jet ventilation. Pediatrics 1996; 98: 918–924.

    CAS  PubMed  Google Scholar 

  99. Shankaran S, Langer JC, Kazzi SN, Laptook AR, et al. Cumulative index of exposure to hypocarbia and hyperoxia as risk factors for periventricular leukomalacia in low birth weight infants. Pediatrics 2006; 118: 1654–1659.

    PubMed  Google Scholar 

  100. Graziani LJ, Baumgart S, Desai S, Stanley C, et al. Clinical antecedents of neurologic and audiologic abnormalities in survivors of neonatal extracorporeal membrane oxygenation. J Child Neurol 1997; 12: 415–422.

    CAS  PubMed  Google Scholar 

  101. Shortland DB, Gibson NA, Levene MI, Archer LN, et al. Patent ductus arteriosus and cerebral circulation in preterm infants. Dev Med Child Neurol 1990; 32: 386–393.

    CAS  PubMed  Google Scholar 

  102. Bandera E, Botteri M, Minelli C, Sutton A, Abrams KR, Latronico N. Cerebral blood flow threshold of ischemic penumbra and infarct core in acute ischemic stroke: a systematic review. Stroke 2006; 37; 1334–1339.

    PubMed  Google Scholar 

  103. Levison SW, Rothstein RP, Romanko MJ, Snyder MJ, et al. Hypoxia-ischemia depletes the rat perinatal subventricular zone of oligodendrocyte progenitors and neural stem cells. Dev Neurosci 2001; 23: 234–247.

    CAS  PubMed  Google Scholar 

  104. 103a. Folkerth RD, Trachtenberg FL, Haynes RL. Oxidative injury in the cerebral cortex and subplate neurons in periventricular leukomalacia. J Neuropathol Exp Neurol 2008; 67: 677–686.

    PubMed  Google Scholar 

  105. Zaidi AU, Bessert DA, Ong JE, Xu H, et al. New oligodendrocytes are generated after neonatal hypoxic-ischemic brain injury in rodents. Glia 2004; 46: 380–390.

    PubMed  Google Scholar 

  106. Inder TE, Mocatta T, Darlow B, Spencer C, et al. Elevated free radical products in the cerebrospinal fluid of VLBW infants with cerebral white matter injury. Pediatr Res 2002; 52: 213–218.

    CAS  PubMed  Google Scholar 

  107. Touil T, Deloire-Grassin MS, Vital C, Petry KG, Broachet B. In vivo damage of CNS myelin and axons induced by peroxynitrite. Neuroreport 2001; 12: 3637–3644.

    CAS  PubMed  Google Scholar 

  108. DeSilva TM, Billiards SS, Borenstein NS, Trachenberg FL, Volpe JJ, Kinney HC, Rosenberg PA. Glutamate transporter EAAT2 expression is upregulated in reactive astro-cytes in human periventricular leukomalacia. J Comp Neurol 2008; 508: 238–248.

    Google Scholar 

  109. Baud O, Daire JL, Dalmaz Y, Fontaine RH, et al. Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol 2004; 14: 1–10.

    PubMed  Google Scholar 

  110. Cai ZW, Pang Y, Xiao F, Rhodes PG. Chronic ischemia preferentially causes white matter injury in the neonatal rat brain. Brain Res 2001; 898: 126–135.

    CAS  PubMed  Google Scholar 

  111. Duncan JR, Cock ML, Harding R, Rees SM. Relation between damage to the placenta and the fetal brain after late-gestation placental embolization and fetal growth restriction in sheep. Am J Obstet Gynecol 2000; 183: 1013–1022.

    CAS  PubMed  Google Scholar 

  112. Ikeda T, Murata Y, Quilligan EJ, Choi BH, et al. Physiologic and histologic changes in near-term fetal lambs exposed to asphyxia by partial umbilical cord occlusion. Am J Obstet Gynecol 1998; 178: 24–32.

    CAS  PubMed  Google Scholar 

  113. Ivacko JA, Sun R, Silverstein FS. Hypoxic-ischemic brain injury induces an acute micro-glial reaction in perinatal rats. Pediatr Res 1995; 39: 39–47.

    Google Scholar 

  114. Lou HC, Lassen NA, Tweed WA, Johnson G, et al. Pressure passive cerebral blood flow and breakdown of the blood-brain barrier in experimental fetal asphyxia. Acta Paediatr Scand 1970; 68: 57–63.

    Google Scholar 

  115. Mallard EC, Rees S, Stringer M, Cock MI, et al. Effects of chronic placental insufficiency on brain development in fetal sheep. Pediatr Res 1998; 43: 262–270.

    CAS  PubMed  Google Scholar 

  116. Matsuda T, Okuyama K, Cho K, Hoshi N, et al. Induction of antenatal periventricular leukomalacia by hemorrhagic hypotension in the chronically instrumented fetal sheep. Am J Obstet Gynecol 1999; 181: 725–730.

    CAS  PubMed  Google Scholar 

  117. Meng S, Qiao M, Scobie K, Tomanek B, et al. Evolution of magnetic resonance imaging changes associated with cerebral hypoxia-ischemia and a relatively selective white matter injury in neonatal rats. Pediatr Res 2006; 59: 554–559.

    PubMed  Google Scholar 

  118. Olivier P, Baud O, Evrard P, Gressens P, et al. Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol 2005; 64: 998–1006.

    PubMed  Google Scholar 

  119. Uehara H, Yoshioka H, Kawase S, Nagai H, et al. A new model of white matter injury in neonatal rats with bilateral carotid artery occlusion. Brain Res 1999; 837: 213–220.

    CAS  PubMed  Google Scholar 

  120. Petersson KH, Pinar H, Stopa EG, Faris RA, et al. White matter injury after cerebral ischemia in ovine fetuses. Pediatr Res 2002; 51: 768–776.

    PubMed  Google Scholar 

  121. Skoff RP, Bessert DA, Barks JDE, Song DK, et al. Hypoxic-ischemic injury results in acute disruption of myelin gene expression and death of oligodendroglial precursors in neonatal mice. Int J Dev Neurosci 2001; 19: 197–208.

    CAS  PubMed  Google Scholar 

  122. Rees S, Stringer M, Just Y, Hooper SB, et al. The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation. Brain Res Dev Brain Res 1997; 103: 103–118.

    CAS  PubMed  Google Scholar 

  123. Riddle A, Luo NL, Manese M, Beardsley DJ, et al. Spatial heterogeneity in oligodendrocyte lineage maturation and not cerebral blood flow predicts fetal ovine periventricular white matter injury. J Neurosci 2006; 26: 3045–3055.

    CAS  PubMed  Google Scholar 

  124. Li Y, Zhongyang L, Keogh CL, Yu SP, Wei L. Erythropoientin-induced neurovascular protection, angiogenesis, and cerebral blood flow restoration after focal ischemia in mice. J Cereb Blood Flow Metabol 2007; 27: 1043–1054.

    CAS  Google Scholar 

  125. Matuez E, Moricz K, Gigler G, Benedek A, Barkoczy J, Levay G, Harsing LG, Szenasi G. Therapeutic time window of neuroprotection by non-competitive AMPA antagonists in transient and permanent focal cerebral ischemia in rats. Brain Res 2006; 1123: 60–67.

    Google Scholar 

  126. Folkerth RD, Haynes RL, Borenstein N, Belliveau RA, Trachtenberg FL, Rosenberg PA, Volpe JJ, Kinney HC. Developmental lag of superoxide dismutases relative to other anti-oxidant enzymes in premyelinated human telencephalic white matter. J Neuropathol Exp Neurol 2004; 14: 265–274.

    CAS  Google Scholar 

  127. Connor JR, Menzies SL. Relationship of iron to oligodendrocytes and myelination. Glia 1996; 17: 83–93.

    CAS  PubMed  Google Scholar 

  128. Savman K, Nilsson UA, Blennow M, Kjellmer I, et al. Non-protein-bound iron is elevated in cerebrospinal fluid from preterm infants with posthemorrhagic ventricular dilation. Pediatr Res 2001; 49: 208–212.

    CAS  PubMed  Google Scholar 

  129. Talos DM, Follett PL, Folkerth RD, Fishman RE, et al. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 2006; 497: 61–77.

    CAS  PubMed  Google Scholar 

  130. DeSilva TM, Kinney HC, Borenstein NS, Trachtenberg FL, Irwin N, Volpe JJ, Rosenberg PA. The glutamate transporter EAAT2 is transiently expressed in developing human cerebral white matter. J Comp Neurol 2007; 501: 879–890.

    Google Scholar 

  131. Billiards SS, Haynes RL, Folkerth RD, Trachtenberg FL, Liu L, Volpe JJ, Kinney HC. Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol 2006; 497: 1990–2008.

    Google Scholar 

  132. Haynes RL, Borenstein NS, DeSilva TM, Folkerth RD, Liu LG, Volpe JJ, Kinney HC. Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol 2005; 484: 156–167.

    PubMed  Google Scholar 

  133. De Felice C, Toti P, Laurini RN, Stumpo M, et al. Early neonatal brain injury in histologic chorioamnionitis. J Pediatr 2001; 138: 101–104.

    PubMed  Google Scholar 

  134. Yoon BH, Jun JK, Romero R, Park KH, et al. Amniotic fluid inflammatory cytokines (inter-leukin-6, interleukin-1β, and tumor necrosis factor-α), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997; 177: 19–26.

    CAS  PubMed  Google Scholar 

  135. Yoon BH, Romero R, Park JS, Kim CJ, et al. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol 2000; 182: 675–681.

    CAS  PubMed  Google Scholar 

  136. Yoon BH, Romero R, Yang SH, Jun JK, 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.

    CAS  PubMed  Google Scholar 

  137. Perlman JM, Risser R, Broyles RS. Bilateral cystic periventricular leukomalacia in the premature infant: associated risk factors. Pediatrics 1996; 97: 822–827.

    CAS  PubMed  Google Scholar 

  138. Duggan PJ, Maalouf EF, Watts TL, Sullivan MHF, et al. Intrauterine T-cell activation and increased cytokine concentrations in preterm infants with cerebral lesions. Lancet 2001; 358: 1699–1700.

    CAS  PubMed  Google Scholar 

  139. Nelson KB, Grether JK, Dambrosia JM, Walsh E, et al. Neonatal cytokines and cerebral palsy in very preterm infants. Pediatr Res 2003; 53: 600–607.

    CAS  PubMed  Google Scholar 

  140. Kaukola T, Saryaraj E, Patel DD, Tchernev V, et al. Cerebral palsy is characterized by protein mediators in cord serum. Ann Neurol 2004; 55: 186–194.

    CAS  PubMed  Google Scholar 

  141. Locatelli A, Vergani P, Ghidini A, Assi F, et al. Duration of labor and risk of cerebral white-matter damage in very preterm infants who are delivered with intrauterine infection. Am J Obstet Gynecol 2005; 193: 928–932.

    PubMed  Google Scholar 

  142. Kadhim HJ, Tabarki B, Verellen G, De Prez C, et al. Inflammatory cytokines in the patho-genesis of periventricular leukomalacia. Neurology 2001; 56: 1278–1284.

    CAS  PubMed  Google Scholar 

  143. Deguchi K, Mizuguchi M, Takashima S. Immunohistochemical expression of tumor necrosis factor a in neonatal leukomalacia. Pediatr Neurol 1996; 14: 13–16.

    CAS  PubMed  Google Scholar 

  144. Stoll BJ, Hansen NI, AdamsChapman I, Fanaroff AA, et al. Neurodevelopmental and growth impairment among extremely low-birth-weight infants with neonatal infection. JAMA 2004; 292: 2357–2365.

    CAS  PubMed  Google Scholar 

  145. Kadhim HJ, Tabarki B, De Prez C, Rona A-M, et al. Interleukin-2 in the pathogenesis of perinatal white matter damage. Neurology 2002; 58: 1125–1128.

    CAS  PubMed  Google Scholar 

  146. Vartanian T, Li Y, Zhao M, Stefansson K. Interferon-gamma reduced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Mol Med 1995; 1: 732–743.

    CAS  PubMed  Google Scholar 

  147. Lee SC, Dickerson DW, Liu W, Brojann CF. Induction of nitric oxide synthase activity in human astrocytes by interleukin-1 beta and interferon-gamma. J Neuroimmunol 1993; 46; 19–24.

    CAS  PubMed  Google Scholar 

  148. Sairanen T, Carpen O, Karjalainen-Lindsberg ML, Paetau A, et al. Evolution of cerebral tumor necrosis factor-alpha production during human ischemic stroke. Stroke 2001; 32: 1750–1757.

    CAS  PubMed  Google Scholar 

  149. Zhang Z, Chopp M, Powers C. Temporal profile of microglial response following transient (2h) middle cerebral artery occlusion. Brain Res 1997; 744: 189–198.

    CAS  PubMed  Google Scholar 

  150. Wang X, Hagberg H, Nie C, Zhu C, et al. Dual role of intrauterine immune challenge on neonatal and adult brain vulnerability to hypoxia-ischemia. J Neuropathol Exp Neurol 2007; 66: 552–561.

    CAS  PubMed  Google Scholar 

  151. Ikeda T, Mishima K, Aoo N, Egashira N, et al. Combination treatment of neonatal rats with hypoxia-ischemia and endotoxin induces long-lasting memory and learning impairment that is associated with extended cerebral damage. Am J Obstet Gynecol 2004; 191: 2132–2141.

    CAS  PubMed  Google Scholar 

  152. Larouche A, Roy M, Kadhim H, Tsanaclis AM, et al. Neuronal injuries induced by perinatal hypoxic-ischemic insults are potentiated by prenatal exposure to lipopolysaccharide: animal model for perinatally acquired encephalopathy. Dev Neurosci 2005; 27: 134–142.

    CAS  PubMed  Google Scholar 

  153. Garnier Y, Coumans ABC, Berger R, Jensen A, et al. Endotoxemia severely affects circulation during normoxia and asphyxia in immature fetal sheep. J Soc Gynecol Invest 2003; 8: 134–142.

    Google Scholar 

  154. Yanowitz TD, Jordan JA, Gilmour CH, Towbin R, et al. Hemodynamic disturbances in premature infants born after chorioamnionitis: association with cord blood cytokine concentrations. Pediatr Res 2002; 51: 310–316.

    PubMed  Google Scholar 

  155. Yanowitz TD, Baker RW, Roberts JM, Brozanski BS. Low blood pressure among very-low-birth-weight infants with fetal vessel inflammation. J Perinatol 2004; 24: 299–304.

    PubMed  Google Scholar 

  156. Yanowitz TD, Potter DM, Bowen A, Baker RW, et al. Variability in cerebral oxygen delivery is reduced in premature neonates exposed to chorioamnionitis. Pediatr Res 2006; 59: 299–304.

    CAS  PubMed  Google Scholar 

  157. Cheranov S Y, Jaggar JH. TNF-alpha dilates cerebral arteries via NAD(P)H oxidase-depend-ent Ca2+ spark activation. Am J Physiol Cell Physiol 2005; 290: C964–C971.

    PubMed  Google Scholar 

  158. Maalouf EF, Duggan PJ, Counsell S, Rutherford MA, et al. Comparison of findings on cranial ultrasound and magnetic resonance imaging in preterm infants. Pediatrics 2001; 107: 719–727.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful for the many contributions of our dedicated collaborators to the work in perinatal brain injury from our institution. We also appreciate the help of Mr. Richard A. Belliveau and Ms. Irene Miller in manuscript preparation. This work was supported by grants from the NINDS (PO1-NS38475) and NICHD (Children's Hospital Developmental Disabilities Research Center) (P30-HD18655).

Author information

Authors and Affiliations

  1. Department of Pathology, Children's Hospital Boston, MA 02115, Boston, USA

    Hannah C. Kinney

  2. Department of Neurology, Children's Hospital Boston, MA 02115, Boston, USA

    Joseph J. Volpe

Authors
  1. Hannah C. Kinney
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph J. Volpe
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of California, San Diego, CA

    Gabriel G. Haddad

  2. Rady Children's Hospital, San Diego, CA

    Gabriel G. Haddad

  3. Emory University, Atlanta, GA

    Shan Ping Yu

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Kinney, H.C., Volpe, J.J. (2009). Perinatal Panencephalopathy in Premature Infants: Is It Due to Hypoxia-Ischemia?. In: Haddad, G.G., Yu, S.P. (eds) Brain Hypoxia and Ischemia. Contemporary Clinical Neuroscience. Humana Press. https://doi.org/10.1007/978-1-60327-579-8_8

Download citation

Publish with us

Policies and ethics