White matter injury in infants with intraventricular haemorrhage: mechanisms and therapies (original) (raw)

• Courtney, S. E. et al. High-frequency oscillatory ventilation versus conventional mechanical ventilation for very-low-birth-weight infants. N. Engl. J. Med. 347, 643–652 (2002).
  PubMed Google Scholar
• Horbar, J. D. et al. Trends in mortality and morbidity for very low birth weight infants, 1991-1999. Pediatrics 110, 143–151 (2002).
  PubMed Google Scholar
• McGowan, E. C. & Vohr, B. R. Neurodevelopmental follow-up of preterm infants: what is new? Pediatr. Clin. North Am. 66, 509–523 (2019).
  PubMed Google Scholar
• Vohr, B. R. Neurodevelopmental outcomes of extremely preterm infants. Clin. Perinatol. 41, 241–255 (2014).
  PubMed Google Scholar
• Stoll, B. J. et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics 126, 443–456 (2010).
  PubMed Google Scholar
• Volpe, J. J. Intraventricular hemorrhage in the premature infant — current concepts. Part II. Ann. Neurol. 25, 109–116 (1989).
  CAS PubMed Google Scholar
• Papile, L. A., Burstein, J., Burstein, R. & Koffler, H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 g. J. Pediatr. 92, 529–534 (1978).
  CAS PubMed Google Scholar
• Perlman, J. M. & Volpe, J. J. Cerebral blood flow velocity in relation to intraventricular hemorrhage in the premature newborn infant. J. Pediatr. 100, 956–959 (1982).
  CAS PubMed Google Scholar
• Valdez Sandoval, P., Hernandez Rosales, P., Quinones Hernandez, D. G., Chavana Naranjo, E. A. & Garcia Navarro, V. Intraventricular hemorrhage and posthemorrhagic hydrocephalus in preterm infants: diagnosis, classification, and treatment options. Childs Nerv. Syst. 35, 917–927 (2019).
  PubMed Google Scholar
• Armstrong, D. L., Sauls, C. D. & Goddard-Finegold, J. Neuropathologic findings in short-term survivors of intraventricular hemorrhage. Am. J. Dis. Child. 141, 617–621 (1987).
  CAS PubMed Google Scholar
• Rushton, D. I., Preston, P. R. & Durbin, G. M. Structure and evolution of echo dense lesions in the neonatal brain. A combined ultrasound and necropsy study. Arch. Dis. Child. 60, 798–808 (1985).
  CAS PubMed PubMed Central Google Scholar
• Skullerud, K. & Westre, B. Frequency and prognostic significance of germinal matrix hemorrhage, periventricular leukomalacia, and pontosubicular necrosis in preterm neonates. Acta Neuropathol. 70, 257–261 (1986).
  CAS PubMed Google Scholar
• Bolisetty, S. et al. Intraventricular hemorrhage and neurodevelopmental outcomes in extreme preterm infants. Pediatrics 133, 55–62 (2014).
  PubMed Google Scholar
• Davis, A. S. et al. Outcomes of extremely preterm infants following severe intracranial hemorrhage. J. Perinatol. 34, 203–208 (2014).
  PubMed Google Scholar
• Vohr, B. R. et al. School-age outcomes of very low birth weight infants in the indomethacin intraventricular hemorrhage prevention trial. Pediatrics 111, e340–6 (2003).
  PubMed Google Scholar
• Nosarti, C. et al. Impaired executive functioning in young adults born very preterm. J. Int. Neuropsychol. Soc. 13, 571–581 (2007).
  PubMed Google Scholar
• Indredavik, M. S. et al. Low-birth-weight adolescents: psychiatric symptoms and cerebral MRI abnormalities. Pediatr. Neurol. 33, 259–266 (2005).
  PubMed Google Scholar
• Whitaker, A. H. et al. Neonatal head ultrasound abnormalities in preterm infants and adolescent psychiatric disorders. Arch. Gen. Psychiatry 68, 742–752 (2011).
  PubMed Google Scholar
• Taylor, H. G., Minich, N., Bangert, B., Filipek, P. A. & Hack, M. Long-term neuropsychological outcomes of very low birth weight: associations with early risks for periventricular brain insults. J. Int. Neuropsychol. Soc. 10, 987–1004 (2004).
  PubMed Google Scholar
• Volpe, J. J. Edward B. Neuhauser lecture. Current concepts of brain injury in the premature infant. AJR Am. J. Roentgenol. 153, 243–251 (1989).
  CAS PubMed Google Scholar
• Larroche, J. C. Post-haemorrhagic hydrocephalus in infancy. Anatomical study. Biol. Neonate 20, 287–299 (1972).
  CAS PubMed Google Scholar
• Buser, J. R. et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 71, 93–109 (2012).
  PubMed PubMed Central Google Scholar
• Bassan, H. et al. Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome. Pediatrics 117, 2111–2118 (2006).
  PubMed Google Scholar
• Takashima, S., Mito, T. & Ando, Y. Pathogenesis of periventricular white matter hemorrhages in preterm infants. Brain Dev. 8, 25–30 (1986).
  CAS PubMed Google Scholar
• Volpe, J. J. Intraventricular hemorrhage in the premature infant–current concepts. Part I. Ann. Neurol. 25, 3–11 (1989).
  CAS PubMed Google Scholar
• Dummula, K. et al. Bone morphogenetic protein inhibition promotes neurological recovery after intraventricular hemorrhage. J. Neurosci. 31, 12068–12082 (2011).
  CAS PubMed PubMed Central Google Scholar
• Ou, X. et al. Impaired white matter development in extremely low-birth-weight infants with previous brain hemorrhage. Am. J. Neuroradiol. 35, 1983–1989 (2014).
  CAS PubMed PubMed Central Google Scholar
• van de Bor, M., Guit, G. L., Schreuder, A. M., Wondergem, J. & Vielvoye, G. J. Early detection of delayed myelination in preterm infants. Pediatrics 84, 407–411 (1989).
  PubMed Google Scholar
• Haynes, R. L., Billiards, S. S., Borenstein, N. S., Volpe, J. J. & Kinney, H. C. Diffuse axonal injury in periventricular leukomalacia as determined by apoptotic marker fractin. Pediatr. Res. 63, 656–661 (2008).
  CAS PubMed PubMed Central Google Scholar
• Georgiadis, P. et al. Characterization of acute brain injuries and neurobehavioral profiles in a rabbit model of germinal matrix hemorrhage. Stroke 39, 3378–3388 (2008).
  CAS PubMed Google Scholar
• Chua, C. O. et al. Consequences of intraventricular hemorrhage in a rabbit pup model. Stroke 40, 3369–3377 (2009).
  PubMed PubMed Central Google Scholar
• Goulding, D. S. et al. Acute brain inflammation, white matter oxidative stress, and myelin deficiency in a model of neonatal intraventricular hemorrhage. J. Neurosurg. Pediatr. https://doi.org/10.3171/2020.5.PEDS20124 (2020).
  Article PubMed PubMed Central Google Scholar
• Lin, S. et al. IGF-1 protects oligodendrocyte progenitor cells and improves neurological functions following cerebral hypoxia-ischemia in the neonatal rat. Brain Res. 1063, 15–26 (2005).
  CAS PubMed Google Scholar
• Keep, R. F. et al. Brain endothelial cell junctions after cerebral hemorrhage: Changes, mechanisms and therapeutic targets. J. Cereb. Blood Flow. Metab. 38, 1255–1275 (2018).
  CAS PubMed PubMed Central Google Scholar
• Aronowski, J. & Zhao, X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke 42, 1781–1786 (2011).
  PubMed PubMed Central Google Scholar
• Xue, M. et al. Does thrombin play a role in the pathogenesis of brain damage after periventricular hemorrhage? Brain Pathol. 15, 241–249 (2005).
  CAS PubMed Google Scholar
• Xi, G., Keep, R. F. & Hoff, J. T. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 5, 53–63 (2006).
  PubMed Google Scholar
• Coughlin, S. R. Thrombin signalling and protease-activated receptors. Nature 407, 258–264 (2000).
  CAS PubMed Google Scholar
• Gao, F. et al. Hydrocephalus after intraventricular hemorrhage: the role of thrombin. J. Cereb. Blood Flow. Metab. 34, 489–494 (2014).
  CAS PubMed Google Scholar
• Lekic, T. et al. PAR-1, -4, and the mTOR pathway following germinal matrix hemorrhage. Acta Neurochir. Suppl. 121, 213–216 (2016).
  PubMed Google Scholar
• Yoon, H., Radulovic, M., Drucker, K. L., Wu, J. & Scarisbrick, I. A. The thrombin receptor is a critical extracellular switch controlling myelination. Glia 63, 846–859 (2015).
  PubMed PubMed Central Google Scholar
• Hao, X. D. et al. Thrombin disrupts vascular endothelial-cadherin and leads to hydrocephalus via protease-activated receptors-1 pathway. CNS Neurosci. Ther. 25, 1142–1150 (2019).
  CAS PubMed PubMed Central Google Scholar
• Ley, D. et al. High presence of extracellular hemoglobin in the periventricular white matter following preterm intraventricular hemorrhage. Front. Physiol. 7, 330 (2016).
  PubMed PubMed Central Google Scholar
• Romantsik, O. et al. The heme and radical scavenger α1-microglobulin (A1M) confers early protection of the immature brain following preterm intraventricular hemorrhage. J. Neuroinflammation 16, 122 (2019).
  PubMed PubMed Central Google Scholar
• Huang, F. P. et al. Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J. Neurosurg. 96, 287–293 (2002).
  PubMed Google Scholar
• Wu, H., Wu, T., Xu, X., Wang, J. & Wang, J. Iron toxicity in mice with collagenase-induced intracerebral hemorrhage. J. Cereb. Blood Flow. Metab. 31, 1243–1250 (2011).
  CAS PubMed Google Scholar
• Masuda, T. et al. Oral administration of metal chelator ameliorates motor dysfunction after a small hemorrhage near the internal capsule in rat. J. Neurosci. Res. 85, 213–222 (2007).
  CAS PubMed Google Scholar
• Guo, J. et al. Minocycline-induced attenuation of iron overload and brain injury after experimental germinal matrix hemorrhage. Brain Res. 1594, 115–124 (2015).
  CAS PubMed Google Scholar
• Meng, H. et al. Deferoxamine alleviates chronic hydrocephalus after intraventricular hemorrhage through iron chelation and Wnt1/Wnt3a inhibition. Brain Res. 1602, 44–52 (2015).
  CAS PubMed Google Scholar
• Wang, M. et al. Complement inhibition attenuates early erythrolysis in the hematoma and brain injury in aged rats. Stroke 50, 1859–1868 (2019).
  CAS PubMed PubMed Central Google Scholar
• Ahmad, S., Bhatia, K., Kindelin, A. & Ducruet, A. F. The role of complement C3a receptor in stroke. Neuromolecular Med. 21, 467–473 (2019).
  CAS PubMed Google Scholar
• Ducruet, A. F. et al. C3a receptor modulation of granulocyte infiltration after murine focal cerebral ischemia is reperfusion dependent. J. Cereb. Blood Flow. Metab. 28, 1048–1058 (2008).
  CAS PubMed Google Scholar
• Jarlestedt, K. et al. Receptor for complement peptide C3a: a therapeutic target for neonatal hypoxic-ischemic brain injury. FASEB J. 27, 3797–3804 (2013).
  PubMed Google Scholar
• Moran, J. et al. Intranasal C3a treatment ameliorates cognitive impairment in a mouse model of neonatal hypoxic-ischemic brain injury. Exp. Neurol. 290, 74–84 (2017).
  CAS PubMed Google Scholar
• Stokowska, A. et al. Complement peptide C3a stimulates neural plasticity after experimental brain ischaemia. Brain 140, 353–369 (2017).
  PubMed Google Scholar
• Yung, Y. C., Stoddard, N. C., Mirendil, H. & Chun, J. Lysophosphatidic acid signaling in the nervous system. Neuron 85, 669–682 (2015).
  CAS PubMed PubMed Central Google Scholar
• Yung, Y. C. et al. Lysophosphatidic acid signaling may initiate fetal hydrocephalus. Sci. Transl. Med. 3, 99ra87 (2011).
  PubMed PubMed Central Google Scholar
• Yu-Taeger, L. et al. Intranasal administration of mesenchymal stem cells ameliorates the abnormal dopamine transmission system and inflammatory reaction in the R6/2 mouse model of Huntington disease. Cells 8, 595 (2019).
  CAS PubMed Central Google Scholar
• Lopez-Serrano, C. et al. Lysophosphatidic acid receptor type 2 activation contributes to secondary damage after spinal cord injury in mice. Brain Behav. Immun. 76, 258–267 (2019).
  CAS PubMed Google Scholar
• Back, S. A. et al. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J. Neurosci. 21, 1302–1312 (2001).
  CAS PubMed PubMed Central Google Scholar
• Back, S. A., Riddle, A. & McClure, M. M. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 38, 724–730 (2007).
  PubMed Google Scholar
• Rakic, S. & Zecevic, N. Early oligodendrocyte progenitor cells in the human fetal telencephalon. Glia 41, 117–127 (2003).
  PubMed Google Scholar
• Vinukonda, G. et al. Neuroprotection in a rabbit model of intraventricular haemorrhage by cyclooxygenase-2, prostanoid receptor-1 or tumour necrosis factor-α inhibition. Brain 133, 2264–2280 (2010).
  PubMed PubMed Central Google Scholar
• Nicolay, D. J., Doucette, J. R. & Nazarali, A. J. Transcriptional control of oligodendrogenesis. Glia 55, 1287–1299 (2007).
  PubMed Google Scholar
• Dohare, P. et al. AMPA-kainate receptor inhibition promotes neurologic recovery in premature rabbits with intraventricular hemorrhage. J. Neurosci. 36, 3363–3377 (2016).
  CAS PubMed PubMed Central Google Scholar
• Zia, M. T. et al. Oxidative-nitrosative stress in a rabbit pup model of germinal matrix hemorrhage: role of NAD(P)H oxidase. Stroke 40, 2191–2198 (2009).
  PubMed PubMed Central Google Scholar
• Yang, Q., Huang, Q., Hu, Z. & Tang, X. Potential neuroprotective treatment of stroke: targeting excitotoxicity, oxidative stress, and inflammation. Front. Neurosci. 13, 1036 (2019).
  PubMed PubMed Central Google Scholar
• Tilleux, S. & Hermans, E. Neuroinflammation and regulation of glial glutamate uptake in neurological disorders. J. Neurosci. Res. 85, 2059–2070 (2007).
  CAS PubMed Google Scholar
• Panfoli, I. et al. Oxidative stress as a primary risk factor for brain damage in preterm newborns. Front. Pediatr. 6, 369 (2018).
  PubMed PubMed Central Google Scholar
• Hagberg, H. et al. The role of inflammation in perinatal brain injury. Nat. Rev. Neurol. 11, 192–208 (2015).
  CAS PubMed PubMed Central Google Scholar
• Xue, M., Balasubramaniam, J., Buist, R. J., Peeling, J. & Del Bigio, M. R. Periventricular/intraventricular hemorrhage in neonatal mouse cerebrum. J. Neuropathol. Exp. Neurol. 62, 1154–1165 (2003).
  PubMed Google Scholar
• Follett, P. L. et al. Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J. Neurosci. 24, 4412–4420 (2004).
  CAS PubMed PubMed Central Google Scholar
• Follett, P. L., Rosenberg, P. A., Volpe, J. J. & Jensen, F. E. NBQX attenuates excitotoxic injury in developing white matter. J. Neurosci. 20, 9235–9241 (2000).
  CAS PubMed PubMed Central Google Scholar
• Perrone, S., Negro, S., Tataranno, M. L. & Buonocore, G. Oxidative stress and antioxidant strategies in newborns. J. Matern. Fetal Neonatal Med. 23, 63–65 (2010).
  PubMed Google Scholar
• Ozsurekci, Y. & Aykac, K. Oxidative stress related diseases in newborns. Oxid. Med. Cell Longev. 2016, 2768365 (2016).
  PubMed PubMed Central Google Scholar
• Perrone, S. et al. Early identification of the risk for free radical-related diseases in preterm newborns. Early Hum. Dev. 86, 241–244 (2010).
  CAS PubMed Google Scholar
• Ma, M. W. et al. NADPH oxidase in brain injury and neurodegenerative disorders. Mol. Neurodegener. 12, 7 (2017).
  PubMed PubMed Central Google Scholar
• Chen, H., Song, Y. S. & Chan, P. H. Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion. J. Cereb. Blood Flow. Metab. 29, 1262–1272 (2009).
  CAS PubMed Google Scholar
• Doverhag, C. et al. Pharmacological and genetic inhibition of NADPH oxidase does not reduce brain damage in different models of perinatal brain injury in newborn mice. Neurobiol. Dis. 31, 133–144 (2008).
  CAS PubMed Google Scholar
• Choi, B. Y. et al. Inhibition of NADPH oxidase activation reduces EAE-induced white matter damage in mice. J. Neuroinflammation 12, 104 (2015).
  PubMed PubMed Central Google Scholar
• Dohare, P. et al. Glycogen synthase kinase-3β inhibition enhances myelination in preterm newborns with intraventricular hemorrhage, but not recombinant Wnt3A. Neurobiol. Dis. 118, 22–39 (2018).
  CAS PubMed PubMed Central Google Scholar
• Bergles, D. E. & Richardson, W. D. Oligodendrocyte development and plasticity. Cold Spring Harb. Perspect. Biol. 8, a020453 (2015).
  PubMed Google Scholar
• Vinukonda, G. et al. Hyaluronidase and hyaluronan oligosaccharides promote neurological recovery after intraventricular hemorrhage. J. Neurosci. 36, 872–889 (2016).
  CAS PubMed PubMed Central Google Scholar
• Vose, L. R. et al. Treatment with thyroxine restores myelination and clinical recovery after intraventricular hemorrhage. J. Neurosci. 33, 17232–17246 (2013).
  CAS PubMed PubMed Central Google Scholar
• Dyer, A. H., Vahdatpour, C., Sanfeliu, A. & Tropea, D. The role of insulin-like growth factor 1 (IGF-1) in brain development, maturation and neuroplasticity. Neuroscience 325, 89–99 (2016).
  CAS PubMed Google Scholar
• Grinspan, J. B. et al. Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J. Neurobiol. 43, 1–17 (2000).
  CAS PubMed Google Scholar
• Gomes, W. A., Mehler, M. F. & Kessler, J. A. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev. Biol. 255, 164–177 (2003).
  CAS PubMed Google Scholar
• Samanta, J. & Kessler, J. A. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131, 4131–4142 (2004).
  CAS PubMed Google Scholar
• Chang, J., Dettman, R. W. & Dizon, M. L. V. Bone morphogenetic protein signaling: a promising target for white matter protection in perinatal brain injury. Neural Regen. Res. 13, 1183–1184 (2018).
  PubMed PubMed Central Google Scholar
• Palazuelos, J., Klingener, M. & Aguirre, A. TGFβ signaling regulates the timing of CNS myelination by modulating oligodendrocyte progenitor cell cycle exit through SMAD3/4/FoxO1/Sp1. J. Neurosci. 34, 7917–7930 (2014).
  CAS PubMed PubMed Central Google Scholar
• Cherian, S., Thoresen, M., Silver, I. A., Whitelaw, A. & Love, S. Transforming growth factor-βs in a rat model of neonatal posthaemorrhagic hydrocephalus. Neuropathol. Appl. Neurobiol. 30, 585–600 (2004).
  CAS PubMed Google Scholar
• Hoque, N., Thoresen, M., Aquilina, K., Hogan, S. & Whitelaw, A. Decorin and colchicine as potential treatments for post-haemorrhagic ventricular dilatation in a neonatal rat model. Neonatology 100, 271–276 (2011).
  PubMed Google Scholar
• Shimizu, T. et al. Wnt signaling controls the timing of oligodendrocyte development in the spinal cord. Dev. Biol. 282, 397–410 (2005).
  CAS PubMed Google Scholar
• Langseth, A. J. et al. Wnts influence the timing and efficiency of oligodendrocyte precursor cell generation in the telencephalon. J. Neurosci. 30, 13367–13372 (2010).
  CAS PubMed PubMed Central Google Scholar
• Ye, F. et al. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the β-catenin-TCF interaction. Nat. Neurosci. 12, 829–838 (2009).
  CAS PubMed PubMed Central Google Scholar
• Azim, K. & Butt, A. M. GSK3β negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 59, 540–553 (2011).
  PubMed Google Scholar
• Ortega, F. et al. Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt signalling. Nat. Cell Biol. 15, 602–613 (2013).
  CAS PubMed Google Scholar
• Genoud, S. et al. Notch1 control of oligodendrocyte differentiation in the spinal cord. J. Cell Biol. 158, 709–718 (2002).
  CAS PubMed PubMed Central Google Scholar
• Wang, S. et al. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63–75 (1998).
  PubMed Google Scholar
• Van Steenwinckel, J. et al. Decreased microglial Wnt/β-catenin signalling drives microglial pro-inflammatory activation in the developing brain. Brain 142, 3806–3833 (2019).
  PubMed PubMed Central Google Scholar
• Lu, Q. R. et al. Common developmental requirement for OLIG function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75–86 (2002).
  CAS PubMed Google Scholar
• Kessaris, N. et al. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173–179 (2006).
  CAS PubMed Google Scholar
• Carre, J. L. et al. Thyroid hormone receptor isoforms are sequentially expressed in oligodendrocyte lineage cells during rat cerebral development. J. Neurosci. Res. 54, 584–594 (1998).
  CAS PubMed Google Scholar
• Rodriguez-Pena, A. Oligodendrocyte development and thyroid hormone. J. Neurobiol. 40, 497–512 (1999).
  CAS PubMed Google Scholar
• Fernandez, M. et al. Thyroid hormone administration enhances remyelination in chronic demyelinating inflammatory disease. Proc. Natl Acad. Sci. USA 101, 16363–16368 (2004).
  CAS PubMed PubMed Central Google Scholar
• Harsan, L. A. et al. Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J. Neurosci. 28, 14189–14201 (2008).
  CAS PubMed PubMed Central Google Scholar
• Courtin, F. et al. Thyroid hormone deiodinases in the central and peripheral nervous system. Thyroid 15, 931–942 (2005).
  CAS PubMed Google Scholar
• Gereben, B. et al. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr. Rev. 29, 898–938 (2008).
  CAS PubMed PubMed Central Google Scholar
• Gonzalez-Perez, O. & Alvarez-Buylla, A. Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res. Rev. 67, 147–156 (2011).
  CAS PubMed PubMed Central Google Scholar
• Vinukonda, G. et al. Epidermal growth factor preserves myelin and promotes astrogliosis after intraventricular hemorrhage. Glia 64, 1987–2004 (2016).
  PubMed PubMed Central Google Scholar
• Hlavica, M. et al. Intrathecal insulin-like growth factor 1 but not insulin enhances myelin repair in young and aged rats. Neurosci. Lett. 648, 41–46 (2017).
  CAS PubMed Google Scholar
• Ley, D. et al. rhIGF-1/rhIGFBP-3 in preterm infants: a phase 2 randomized controlled trial. J. Pediatr. 206, 56–65.e8 (2019).
  CAS PubMed Google Scholar
• Wood, T. L. et al. Delayed IGF-1 administration rescues oligodendrocyte progenitors from glutamate-induced cell death and hypoxic-ischemic brain damage. Dev. Neurosci. 29, 302–310 (2007).
  CAS PubMed Google Scholar
• Lin, S., Fan, L. W., Rhodes, P. G. & Cai, Z. Intranasal administration of IGF-1 attenuates hypoxic-ischemic brain injury in neonatal rats. Exp. Neurol. 217, 361–370 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kiechl-Kohlendorfer, U., Ralser, E., Pupp Peglow, U., Pehboeck-Walser, N. & Fussenegger, B. Early risk predictors for impaired numerical skills in 5-year-old children born before 32 weeks of gestation. Acta Paediatr. 102, 66–71 (2013).
  PubMed Google Scholar
• Klebermass-Schrehof, K. et al. Impact of low-grade intraventricular hemorrhage on long-term neurodevelopmental outcome in preterm infants. Childs Nerv. Syst. 28, 2085–2092 (2012).
  CAS PubMed Google Scholar
• Sherlock, R. L., Anderson, P. J., Doyle, L. W. & Victorian Infant Collaborative Study Group. Neurodevelopmental sequelae of intraventricular haemorrhage at 8 years of age in a regional cohort of ELBW/very preterm infants. Early Hum. Dev. 81, 909–916 (2005).
  CAS PubMed Google Scholar
• Movsas, T. Z. et al. Autism spectrum disorder is associated with ventricular enlargement in a low birth weight population. J. Pediatr. 163, 73–78 (2013).
  PubMed PubMed Central Google Scholar
• Ment, L. R. et al. Practice parameter: neuroimaging of the neonate: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology 58, 1726–1738 (2002).
  CAS PubMed Google Scholar
• Spittle, A. J. et al. Neonatal white matter abnormality predicts childhood motor impairment in very preterm children. Dev. Med. Child. Neurol. 53, 1000–1006 (2011).
  PubMed PubMed Central Google Scholar
• Woodward, L. J., Anderson, P. J., Austin, N. C., Howard, K. & Inder, T. E. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N. Engl. J. Med. 355, 685–694 (2006).
  CAS PubMed Google Scholar
• Leijser, L. M. et al. Posthemorrhagic ventricular dilatation in preterm infants: when best to intervene? Neurology 90, e698–e706 (2018).
  PubMed PubMed Central Google Scholar
• Cayam-Rand, D. et al. Predicting developmental outcomes in preterm infants: a simple white matter injury imaging rule. Neurology 93, e1231–e1240 (2019).
  PubMed PubMed Central Google Scholar
• Cizmeci, M. N. et al. Randomized controlled Early versus Late Ventricular Intervention Study (ELVIS) in posthemorrhagic ventricular dilatation: outcome at 2 years. J. Pediatr. https://doi.org/10.1016/j.jpeds.2020.08.014 (2020).
  Article PubMed Google Scholar
• Lean, R. E. et al. Altered neonatal white and gray matter microstructure is associated with neurodevelopmental impairments in very preterm infants with high-grade brain injury. Pediatr. Res. 86, 365–374 (2019).
  PubMed PubMed Central Google Scholar
• Morita, T. et al. Low-grade intraventricular hemorrhage disrupts cerebellar white matter in preterm infants: evidence from diffusion tensor imaging. Neuroradiology 57, 507–514 (2015).
  PubMed Google Scholar
• Tortora, D. et al. The effects of mild germinal matrix-intraventricular haemorrhage on the developmental white matter microstructure of preterm neonates: a DTI study. Eur. Radiol. 28, 1157–1166 (2018).
  PubMed Google Scholar
• Roze, E. et al. Neonatal DTI early after birth predicts motor outcome in preterm infants with periventricular hemorrhagic infarction. Pediatr. Res. 78, 298–303 (2015).
  PubMed Google Scholar
• Ancel, P. Y. et al. Cerebral palsy among very preterm children in relation to gestational age and neonatal ultrasound abnormalities: the EPIPAGE cohort study. Pediatrics 117, 828–835 (2006).
  PubMed Google Scholar
• Patra, K., Wilson-Costello, D., Taylor, H. G., Mercuri-Minich, N. & Hack, M. Grades I-II intraventricular hemorrhage in extremely low birth weight infants: effects on neurodevelopment. J. Pediatr. 149, 169–173 (2006).
  PubMed Google Scholar
• Vavasseur, C., Slevin, M., Donoghue, V. & Murphy, J. F. Effect of low grade intraventricular hemorrhage on developmental outcome of preterm infants. J. Pediatr. 151, e6 (2007).
  PubMed Google Scholar
• Mukerji, A., Shah, V. & Shah, P. S. Periventricular/intraventricular hemorrhage and neurodevelopmental outcomes: a meta-analysis. Pediatrics 136, 1132–1143 (2015).
  PubMed Google Scholar
• Reubsaet, P. et al. The impact of low-grade germinal matrix-intraventricular hemorrhage on neurodevelopmental outcome of very preterm infants. Neonatology 112, 203–210 (2017).
  PubMed Google Scholar
• Morgan, C. et al. The pooled diagnostic accuracy of neuroimaging, general movements, and neurological examination for diagnosing cerebral palsy early in high-risk infants: a case control study. J. Clin. Med. 8, 1879 (2019).
  PubMed Central Google Scholar
• Soleimani, F. et al. Do NICU developmental care improve cognitive and motor outcomes for preterm infants? A systematic review and meta-analysis. BMC Pediatr. 20, 67 (2020).
  PubMed PubMed Central Google Scholar
• Spittle, A., Orton, J., Anderson, P. J., Boyd, R. & Doyle, L. W. Early developmental intervention programmes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants. Cochrane Database Syst. Rev. 11, CD005495 (2015).
  Google Scholar
• Spittle, A. & Treyvaud, K. The role of early developmental intervention to influence neurobehavioral outcomes of children born preterm. Semin. Perinatol. 40, 542–548 (2016).
  PubMed Google Scholar
• Council on Children With Disabilities, Section on Developmental Behavioral Pediatrics, Bright Futures Steering Committee and Medical Home Initiatives for Children With Special Needs Project Advisory Committee. Identifying infants and young children with developmental disorders in the medical home: an algorithm for developmental surveillance and screening. Pediatrics 118, 405–420 (2006).
  Google Scholar
• Bassan, H. et al. Timing of external ventricular drainage and neurodevelopmental outcome in preterm infants with posthemorrhagic hydrocephalus. Eur. J. Paediatr. Neurol. 16, 662–670 (2012).
  PubMed Google Scholar
• Levene, M. I. Measurement of the growth of the lateral ventricles in preterm infants with real-time ultrasound. Arch. Dis. Child. 56, 900–904 (1981).
  CAS PubMed PubMed Central Google Scholar
• de Vries, L. S. et al. Treatment thresholds for intervention in posthaemorrhagic ventricular dilation: a randomised controlled trial. Arch. Dis. Child. Fetal Neonatal Ed. 104, F70–F75 (2019).
  PubMed Google Scholar
• Agajany, N. et al. The impact of neonatal posthemorrhagic hydrocephalus of prematurity on family function at preschool age. Early Hum. Dev. 137, 104827 (2019).
  PubMed Google Scholar
• Burnett, A. C., Cheong, J. L. Y. & Doyle, L. W. Biological and social influences on the neurodevelopmental outcomes of preterm infants. Clin. Perinatol. 45, 485–500 (2018).
  PubMed Google Scholar
• Benavente-Fernandez, I. et al. Association of socioeconomic status and brain injury with neurodevelopmental outcomes of very preterm children. JAMA Netw. Open 2, e192914 (2019).
  PubMed PubMed Central Google Scholar
• Taveggia, C., Feltri, M. L. & Wrabetz, L. Signals to promote myelin formation and repair. Nat. Rev. Neurol. 6, 276–287 (2010).
  PubMed PubMed Central Google Scholar
• Wilkins, A., Chandran, S. & Compston, A. A role for oligodendrocyte-derived IGF-1 in trophic support of cortical neurons. Glia 36, 48–57 (2001).
  CAS PubMed Google Scholar
• Whitelaw, A. et al. Randomized trial of drainage, irrigation and fibrinolytic therapy for premature infants with posthemorrhagic ventricular dilatation: developmental outcome at 2 years. Pediatrics 125, e852–858 (2010).
  PubMed Google Scholar
• Luyt, K. et al. Drainage, irrigation and fibrinolytic therapy (DRIFT) for posthaemorrhagic ventricular dilatation: 10-year follow-up of a randomised controlled trial. Arch. Dis. Child. Fetal Neonatal Ed. 105, 466–473 (2020).
  PubMed Google Scholar
• Etus, V., Kahilogullari, G., Karabagli, H. & Unlu, A. Early endoscopic ventricular irrigation for the treatment of neonatal posthemorrhagic hydrocephalus: a feasible treatment option or not? a multicenter study. Turk. Neurosurg. 28, 137–141 (2018).
  PubMed Google Scholar
• Schulz, M., Buhrer, C., Pohl-Schickinger, A., Haberl, H. & Thomale, U. W. Neuroendoscopic lavage for the treatment of intraventricular hemorrhage and hydrocephalus in neonates. J. Neurosurg. Pediatr. 13, 626–35 (2014).
  PubMed Google Scholar
• d’Arcangues, C. et al. Extended experience with neuroendoscopic lavage for posthemorrhagic hydrocephalus in neonates. World Neurosurg. 116, e217–e224 (2018).
  PubMed Google Scholar
• Mahoney, L., Luyt, K., Harding, D. & Odd, D. Treatment for post-hemorrhagic ventricular dilatation: a multiple-treatment meta-analysis. Front. Pediatr. 8, 238 (2020).
  PubMed PubMed Central Google Scholar
• El-Dib, M. et al. Management of post-hemorrhagic ventricular dilatation in the infant born preterm. J. Pediatr. https://doi.org/10.1016/j.jpeds.2020.07.079 (2020).
  Article PubMed PubMed Central Google Scholar
• Klebe, D. et al. Dabigatran ameliorates post-haemorrhagic hydrocephalus development after germinal matrix haemorrhage in neonatal rat pups. J. Cereb. Blood Flow. Metab. 37, 3135–3149 (2017).
  CAS PubMed Google Scholar
• Liu, D. Z. et al. Blood–brain barrier breakdown and repair by Src after thrombin-induced injury. Ann. Neurol. 67, 526–533 (2010).
  CAS PubMed PubMed Central Google Scholar
• Ramos-Mandujano, G., Vazquez-Juarez, E., Hernandez-Benitez, R. & Pasantes-Morales, H. Thrombin potently enhances swelling-sensitive glutamate efflux from cultured astrocytes. Glia 55, 917–925 (2007).
  PubMed Google Scholar
• Lekic, T. et al. Cyclooxygenase-2 inhibition provides lasting protection following germinal matrix hemorrhage in premature infant rats. Acta Neurochir. Suppl. 121, 203–207 (2016).
  PubMed Google Scholar
• Garrido-Mesa, N., Zarzuelo, A. & Galvez, J. Minocycline: far beyond an antibiotic. Br. J. Pharmacol. 169, 337–352 (2013).
  CAS PubMed PubMed Central Google Scholar
• Malhotra, K. et al. Minocycline for acute stroke treatment: a systematic review and meta-analysis of randomized clinical trials. J. Neurol. 265, 1871–1879 (2018).
  CAS PubMed Google Scholar
• Hanada, T. et al. Perampanel: a novel, orally active, noncompetitive AMPA-receptor antagonist that reduces seizure activity in rodent models of epilepsy. Epilepsia 52, 1331–1340 (2011).
  CAS PubMed Google Scholar
• Rogawski, M. A. Revisiting AMPA receptors as an antiepileptic drug target. Epilepsy Curr. 11, 56–63 (2011).
  PubMed PubMed Central Google Scholar
• Gidal, B. E. et al. Perampanel efficacy and tolerability with enzyme-inducing AEDs in patients with epilepsy. Neurology 84, 1972–1980 (2015).
  CAS PubMed PubMed Central Google Scholar
• Vazquez, B., Yang, H., Williams, B., Zhou, S. & Laurenza, A. Perampanel efficacy and safety by gender: subanalysis of phase III randomized clinical studies in subjects with partial seizures. Epilepsia 56, e90–4 (2015).
  CAS PubMed PubMed Central Google Scholar
• La Gamma, E. F. et al. Phase 1 trial of 4 thyroid hormone regimens for transient hypothyroxinemia in neonates of <28 weeks’ gestation. Pediatrics 124, e258–e268 (2009).
  PubMed Google Scholar
• van Wassenaer, A. G. et al. Effects of thyroxine supplementation on neurologic development in infants born at less than 30 weeks’ gestation. N. Engl. J. Med. 336, 21–26 (1997).
  PubMed Google Scholar
• van Wassenaer, A. G., Westera, J., Houtzager, B. A. & Kok, J. H. Ten-year follow-up of children born at <30 weeks’ gestational age supplemented with thyroxine in the neonatal period in a randomized, controlled trial. Pediatrics 116, e613–e618 (2005).
  PubMed Google Scholar
• Aguirre, A., Rizvi, T. A., Ratner, N. & Gallo, V. Overexpression of the epidermal growth factor receptor confers migratory properties to nonmigratory postnatal neural progenitors. J. Neurosci. 25, 11092–11106 (2005).
  CAS PubMed PubMed Central Google Scholar
• Scafidi, J. et al. Intranasal epidermal growth factor treatment rescues neonatal brain injury. Nature 506, 230–234 (2014).
  CAS PubMed Google Scholar
• Hognason, T. et al. Epidermal growth factor receptor induced apoptosis: potentiation by inhibition of Ras signaling. FEBS Lett. 491, 9–15 (2001).
  CAS PubMed Google Scholar
• van Velthoven, C. T., Gonzalez, F., Vexler, Z. S. & Ferriero, D. M. Stem cells for neonatal stroke — the future is here. Front. Cell Neurosci. 8, 207 (2014).
  PubMed PubMed Central Google Scholar
• Chang, Y. S., Ahn, S. Y., Sung, S. & Park, W. S. Stem cell therapy for neonatal disorders: prospects and challenges. Yonsei Med. J. 58, 266–271 (2017).
  PubMed PubMed Central Google Scholar
• Ahn, S. Y., Chang, Y. S. & Park, W. S. Mesenchymal stem cells transplantation for neuroprotection in preterm infants with severe intraventricular hemorrhage. Korean J. Pediatr. 57, 251–256 (2014).
  PubMed PubMed Central Google Scholar
• Ahn, S. Y. et al. Mesenchymal stem cells prevent hydrocephalus after severe intraventricular hemorrhage. Stroke 44, 497–504 (2013).
  CAS PubMed Google Scholar
• Kim, E. S. et al. Human umbilical cord blood-derived mesenchymal stem cell transplantation attenuates severe brain injury by permanent middle cerebral artery occlusion in newborn rats. Pediatr. Res. 72, 277–284 (2012).
  CAS PubMed Google Scholar
• Ahn, S. Y., Chang, Y. S., Sung, S. I. & Park, W. S. Mesenchymal stem cells for severe intraventricular hemorrhage in preterm infants: phase I dose-escalation clinical trial. Stem Cell Transl. Med. 7, 847–856 (2018).
  CAS Google Scholar
• Keller, T. et al. Intranasal breast milk for premature infants with severe intraventricular hemorrhage-an observation. Eur. J. Pediatr. 178, 199–206 (2019).
  CAS PubMed Google Scholar