The Quest for Neuroprotection for Injuries in the Developing Brain

Fatima Yousif Ismail; Ali Fatemi; Michael Johnston

doi:10.17724/jicna.2017.79

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October 15, 2016

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September 3, 2017

Published

September 21, 2017

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Abstract

The advancement in medical knowledge could have not been possible without interlocking and reinforcing the bedside-lab continuum. In the field of pediatric neurology, one of the best illustrative examples is our quest for finding neuroprotective therapies in the setting of neonatal hypoxic-ischemic encephalopathy. In this review, we discuss the careful clinical observations driven from the bedside dating back to the work of Frank Ford. We trace the relentless efforts to emulate the pathogenesis in animal models to testing potential therapies in clinical trials that made the transfer of this knowledge back to the bedside possible in order to save and improve the quality of life for hundred of thousands of newborns who suffered hypoxic ischemic insult.

Keywords

Neuroprotection hypoxic-ischemic injury neuroplasticity inflammation repair term and preterm infants encephalopathy glutamate excitotoxicity.

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Author Biographies

Fatima Yousif Ismail, Clinical and research Fellow, Department of Pediatrics, Neurology and Developmental Medicine, Kennedy Krieger Institute, Johns Hopkins Medical Institutions, Maryland, USA. Teaching Assistant, Department of Pediatrics, College of Medicine and Health Sciences, United Arab Emirates University.

Department of Pediatrics, Neurology and Developmental Medicine, Kennedy Krieger Institute, Johns Hopkins Medical Institutions, Maryland, USA.

Department of Pediatrics, College of Medicine and Health Sciences, United Arab Emirates University

Ali Fatemi

Departments of Neurology and Pediatrics, Kennedy Krieger Institute and Johns Hopkins University, School of Medicine, Maryland, USA.

Michael Johnston, Kennedy Krieger Institute and Johns Hopkins University School of Medicine

Professor of Neurology, Pediatrics and PM&R, Kennedy Krieger Institute and Johns Hopkins University, School of Medicine, Maryland, US.

How to Cite

Ismail, F. Y., Fatemi, A., & Johnston, M. (2017). The Quest for Neuroprotection for Injuries in the Developing Brain. Journal of the International Child Neurology Association, 1(1). https://doi.org/10.17724/jicna.2017.79

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References

D. A. Stumpf, “THE FOUNDING OF PEDIATRIC NEUROLOGY IN AMERICA,” Bull NY Acad Med, vol. 57, no. 9, pp. 804–816, 1981.
S. Ashwal and R. Rust, “Child neurology in the 20th century,” Pediatric Research, vol. 53, no. 2, pp. 345–361, 2003.
The American College of Obstetricians and Gynecologists, “Neonatal Encephalopathy and Neurologic Outcome, Second Edition. Report of the American College of Obstetricians and Gynecologists’ Task Force on Neonatal Encephalopathy,” OBSTETRICS & GYNECOLOGY, vol. 123, no. 4, pp. 896–901, 2014.
A. C. C. Lee, N. Kozuki, H. Blencowe, T. Vos, A. Bahalim, G. L. Darmstadt, S. Niermeyer, M. Ellis, N. J. Robertson, S. Cousens, and J. E. Lawn, “Intrapartum-related neonatal encephalopathy incidence and impairment at regional and global levels for 2010 with trends from 1990.,” Pediatric research, vol. 74 Suppl 1, no. December, pp. 50–72, 2013.
M. S. Sarnat, Harvey B. and Sarnat, “Neonatal Encephalopathy Following Fetal Distress: A Clinical and Electroencephalographic Study,” Arch Neurol, vol. 33, pp. 696–705, 1976.
C. E. Ahearne, N. M. Denihan, B. H. Walsh, S. N. Reinke, L. C. Kenny, G. B. Boylan, D. I. Broadhurst, and D. M. Murray, “Early Cord Metabolite Index and Outcome in Perinatal Asphyxia and Hypoxic-Ischaemic Encephalopathy,” Neonatology, pp. 296–302, 2016.
S. L. Bonifacioa, L. S. DeVriesb, and F. Groenendaalb, “Impact of hypothermia on predictors of poor outcome: how do we decide to redirect care?,” Semin fetal neonatol Med 2015, vol. 20, no. 2, pp. 122–127, 2015.
J. E. Rice, R. C. Vannucci, and J. B. Brierley, “The influence of immaturity on hypoxic-ischemic brain damage in the rat.,” Annals of neurology, vol. 9, no. 2, pp. 131–41, 1981.
R. C. Vannucci and S. J. Vannucci, “Perinatal hypoxic-ischemic brain damage: Evolution of an animal model,” Developmental Neuroscience, vol. 27, no. 2–4. pp. 81–86, 2005.
M. V. Johnston, “Neurotransmitter alterations in a model of perinatal hypoxrc-ischemc brain injury,” Annals of neurology, vol. 13, pp. 511–518, 1983.
L. Huang, F. Zhao, Y. Qu, L. Zhang, Y. Wang, and D. Mu, “Animal models of hypoxic-ischemic encephalopathy: optimal choices for the best outcomes,” Reviews in the Neurosciences, p. [Epub ahead of print], 2016.
J. W. McDonald and M. V Johnston, “Physiological and pathophysiological roles of excitatory amino acids during central nervous system development.,” Brain research Brain research reviews, vol. 15, no. 1, pp. 41–70, 1990.
M. V Johnston, A. Fatemi, M. A. Wilson, and F. Northington, “Treatment advances in neonatal neuroprotection and neurointensive care,” vol. 10, no. 4, pp. 372–382, 2011.
R. Lujan, R. Shigemoto, and G. Lopez-Bendito, “Glutamate and GABA receptor signalling in the developing brain,” Neuroscience, vol. 130, no. 3, pp. 567–580, 2005.
M. V Johnston, W. Nakajima, and H. Hagberg, “Mechanisms of hypoxic neurodegeneration in the developing brain,” Neuroscientist, vol. 8, no. 3, pp. 212–220, 2002.
M. V Johnston, “Excitotoxicity in Neonatal Hypoxia,” Mental retardation and developmental disabilities, vol. 7, pp. 229–234, 2001.
Q. Ma and L. Zhang, “Epigenetic programming of hypoxic-ischemic encephalopathy in response to fetal hypoxia,” Progress in Neurobiology, vol. 124, pp. 28–48, 2015.
M. V. Johnston, “Neurotransmitters and vulnerability of the developing brain,” Brain and Development, vol. 17, no. 5, pp. 301–306, 1995.
E. Rocha-Ferreira and M. Hristova, “Plasticity in the neonatal brain following hypoxic-ischaemic injury,” vol. 2016, 2016.
B. B. Kostandy, “The role of glutamate in neuronal ischemic injury: The role of spark in fire,” Neurological Sciences, vol. 33, no. 2, pp. 223–237, 2012.
S. M. Rothman and J. W. Olney, “Glutamate and the Pathophysiology of Hypoxic-Ischemic Brain Damage,” Annals of neurology, vol. 19, pp. 111–1986, 1986.
H. Hagberg, P. Andersson, I. Kjellmer, K. Thiringer, and M. Thordstein, “Extracellular overflow of glutamate, aspartate, GABA and taurine in the cortex and basal ganglia of fetal lambs during hypoxia-ischemia,” Neuroscience Letters, vol. 78, no. 3, pp. 311–317, 1987.
R. S. Riikonen, P. O. Kero, and O. G. Simell, “Excitatory amino acids in cerebrospinal fluid in neonatal asphyxia.,” Pediatric neurology, vol. 8, no. 1, pp. 37–40, 1992.
M. T. Khashaba, B. O. Shouman, A. A. Shaltout, H. M. Al-Marsafawy, M. M. Abdel-Aziz, K. Patel, and H. Aly, “Excitatory amino acids and magnesium sulfate in neonatal asphyxia,” Brain and Development, vol. 28, no. 6, pp. 375–379, 2006.
T. Logica, S. Riviere, M. I. Holubiec, R. Castilla, G. E. Barreto, and F. Capani, “Metabolic Changes Following Perinatal Asphyxia: Role of Astrocytes and Their Interaction with Neurons.,” Frontiers in aging neuroscience, vol. 8, p. 116, 2016.
A. A. Baburamani, C. J. Ek, D. W. Walker, and M. Castillo-melendez, “Vulnerability of the developing brain to hypoxic-ischemic damage : contribution of the cerebral vasculature to injury and repair ?,” vol. 3, no. November, pp. 1–21, 2012.
A. Looney, C. Ahearne, G. B. Boylan, and D. M. Murray, “Glial Fibrillary Acidic Protein Is Not an Early Marker of Injury in Perinatal Asphyxia and Hypoxic – Ischemic Encephalopathy,” Frontiers in neurology, vol. 6, no. December, pp. 1–6, 2015.
J. Jaworska, M. Ziemka-Nalecz, J. Sypecka, and T. Zalewska, “The potential neuroprotective role of a histone deacetylase inhibitor, sodium butyrate, after neonatal hypoxia-ischemia.,” Journal of neuroinflammation, vol. 14, no. 1, p. 34, Feb. 2017.
F. Zhang, E. Nance, Y. Alnasser, R. Kannan, and S. Kannan, “Microglial migration and interactions with dendrimer nanoparticles are altered in the presence of neuroinflammation,” Journal of Neuroinflammation, pp. 1–11, 2016.
M. Ziemka-Nalecz, J. Janowska, L. Strojek, J. Jaworska, T. Zalewska, M. Frontczak-Baniewicz, and J. Sypecka, “Impact of neonatal hypoxia-ischaemia on oligodendrocyte survival, maturation and myelinating potential.,” Journal of cellular and molecular medicine, Aug. 2017.
J. Janowska and J. Sypecka, “Therapeutic Strategies for Leukodystrophic Disorders Resulting from Perinatal Asphyxia : Focus on Myelinating Oligodendrocytes,” mol neurobiol, 2017.
K. Savman, M. Blennow, K. Gustafson, E. Tarkowski, and H. Hagberg, “Cytokine Response in Cerebrospinal Fluid after Birth Asphyxia,” Pediatr Res, vol. 43, no. 6, pp. 746–751, Jun. 1998.
H. yan Lu, Q. Zhang, Q. xia Wang, and J. ying Lu, “Contribution of Histologic Chorioamnionitis and Fetal Inflammatory Response Syndrome to Increased Risk of Brain Injury in Infants With Preterm Premature Rupture of Membranes,” Pediatric Neurology, vol. 61, p. 94–98.e1, 2015.
I. Lee, N. Jeffrey, P. Huettner, C. D. Smyser, C. E. Rogers, J. S. Shimony, H. Kidokoro, I. Mysorekar, and T. E. Inder, “The impact of prenatal and neonatal infection on neurodevelopmental outcomes in very preterm infants Iris,” J Perinatol, vol. 34, no. 10, pp. 741–747, 2015.
L. F. Chalak, “Inflammatory Biomarkers of Birth Asphyxia,” Clinics in Perinatology, vol. 43, no. 3, pp. 501–510, 2016.
G. Breier, A. Damert, K. H. Plate, and W. Risau, “Angiogenesis in embryos and ischemic diseases.,” Thrombosis and haemostasis, vol. 78, no. 1, pp. 678–683, Jul. 1997.
G. D. Yancopoulos, S. Davis, N. W. Gale, J. S. Rudge, S. J. Wiegand, and J. Holash, “Vascular-specific growth factors and blood vessel formation.,” Nature, vol. 407, no. 6801, pp. 242–248, Sep. 2000.
E. Maltepe, J. V Schmidt, D. Baunoch, C. A. Bradfield, and M. C. Simon, “Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT.,” Nature, vol. 386, no. 6623, pp. 403–407, Mar. 1997.
Y. Li, P. Gonzalez, and L. Zhang, “Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: mechanisms and possible interventions.,” Progress in neurobiology, vol. 98, no. 2, pp. 145–165, Aug. 2012.
R. M. Ruddy and C. M. Morshead, “Home sweet home: the neural stem cell niche throughout development and after injury.,” Cell and tissue research, Aug. 2017.
N. Salmaso, S. Tomasi, and F. M. Vaccarino, “Neurogenesis and Maturation in Neonatal B rain Injury Preterm birth Neurogenesis Neonatal brain injury Cognitive delay,” Clinics in Perinatology, vol. 41, no. 1, pp. 229–239, 2014.
P. Morales, J. L. Fiedler, S. Andre´s, C. Berrios, D. Huaiquı´n, D. Bustamante, S. Cardenas, E. Parra, and H.-M. M., “Plasticity of Hippocampus Following Perinatal Asphyxia : Effects on Postnatal Apoptosis and Neurogenesis,” Journal of Neuroscience Research, vol. 86, pp. 2650–2662, 2008.
A. Tapia-Bustos, R. Perez-Lobos, V. Vio, C. Lespay-Rebolledo, E. Palacios, A. Chiti-Morales, D. Bustamante, M. Herrera-Marschitz, and P. Morales, “Modulation of Postnatal Neurogenesis by Perinatal Asphyxia: Effect of D1 and D2 Dopamine Receptor Agonists.,” Neurotoxicity research, vol. 31, no. 1, pp. 109–121, Jan. 2017.
J. Waddell, M. Hanscom, N. S. Edwards, M. C. Mckenna, and M. M. Mccarthy, “Sex differences in cell genesis , hippocampal volume and behavioral outcomes in a rat model of neonatal HI,” Experimental Neurology, vol. 275, pp. 285–295, 2016.
G. Orman, J. E. Benson, C. F. Kweldam, T. Bosemani, A. Tekes, M. R. de Jong, D. Seyfert, F. J. Northington, A. Poretti, and T. A. G. M. Huisman, “Neonatal Head Ultrasonography Today: A Powerful Imaging Tool!,” Journal of Neuroimaging, vol. 25, no. 1, pp. 31–55, 2015.
S. Miller, V. Ramaswamy, D. Michelson, B. AJ, B. Holshouser, N. Wycliffe, G. DV, D. Deming, P. JC, W. YW, S. Ashwal, and F. DM, “Patterns of brain injury in term neonatal encephalopathy,” J Pediatr, vol. 146, pp. 453–60, 2005.
L. S. De Vries and F. Groenendaal, “Patterns of neonatal hypoxic – ischaemic brain injury,” Neuroradiology, vol. 52, pp. 555–566, 2010.
J. J. Volpe, “Neonatal encephalopathy: An inadequate term for hypoxic-ischemic encephalopathy,” Annals of Neurology, vol. 72, no. 2, pp. 156–166, 2012.
J. J. Volpe, “The Encephalopathy of Prematurity-Brain Injury and Impaired Brain Development Inextricably Intertwined,” Seminars in Pediatric Neurology, vol. 16, no. 4, pp. 167–178, 2009.
A. J. Barkovich, B. L. Hajnal, D. Vigneron, A. Sola, J. C. Partridge, F. Allen, and D. M. Ferriero, “Prediction of neuromotor outcome in perinatal asphyxia: Evaluation of MR scoring systems,” American Journal of Neuroradiology, vol. 19, no. 1, pp. 143–149, 1998.
G. Arca-Diaz, T. J. Re, M. Drottar, C. R. Fortuno, K. De Macedo-Rodrigues, K. Im, J. Figueras-Aloy, and P. E. Grant, “Can cerebellar and brainstem apparent diffusion coefficient (ADC) values predict neuromotor outcome in term neonates with hypoxic-ischemic encephalopathy (HIE) treated with hypothermia?,” PloS one, vol. 12, no. 7, p. e0178510, 2017.
E.-M. Heursen, A. Zuazo Ojeda, I. Benavente Fernandez, G. Jimenez Gomez, R. Campuzano Fernandez-Colima, J. Paz-Exposito, and S. P. Lubian Lopez, “Prognostic Value of the Apparent Diffusion Coefficient in Newborns with Hypoxic-Ischaemic Encephalopathy Treated with Therapeutic Hypothermia.,” Neonatology, vol. 112, no. 1, pp. 67–72, 2017.
P. Ward, S. Counsell, J. Allsop, F. Cowan, Y. Shen, D. Edwards, and M. Rutherford, “Reduced Fractional Anisotropy on Diffusion Tensor Magnetic Resonance Imaging After Hypoxic-Ischemic Encephalopathy,” Pediatrics, vol. 117, no. 4, p. e619 LP-e630, Apr. 2006.
A. N. Massaro, R. B. Govindan, G. Vezina, T. Chang, N. N. Andescavage, Y. Wang, T. Al-shargabi, M. Metzler, K. Harris, A. J. Plessis, Y. Wang, M. Metzler, K. Harris, and P. Aj, “Impaired cerebral autoregulation and brain injury in newborns with hypoxic-ischemic encephalopathy treated with hypothermia,” J neurophsiol, vol. 114, pp. 818–824, 2015.
F. Groenendaal and L. S. de Vries, “Fifty years of brain imaging in neonatal encephalopathy following perinatal asphyxia.,” Pediatric research, no. May, 2016.
T. Alderliesten, L. S. de Vries, L. Staats, I. C. van Haastert, L. Weeke, M. J. N. L. Benders, C. Koopman-Esseboom, and F. Groenendaal, “MRI and spectroscopy in (near) term neonates with perinatal asphyxia and therapeutic hypothermia.,” Archives of disease in childhood Fetal and neonatal edition, vol. 102, no. 2, pp. F147–F152, Mar. 2017.
P. E. Sijens, K. Wischniowsky, and H. J. Ter Horst, “The prognostic value of proton magnetic resonance spectroscopy in term newborns treated with therapeutic hypothermia following asphyxia.,” Magnetic resonance imaging, vol. 42, pp. 82–87, Jun. 2017.
A. J. Barkovich, S. P. Miller, A. Bartha, N. Newton, S. E. G. Hamrick, P. Mukherjee, O. A. Glenn, D. Xu, J. C. Partridge, D. M. Ferriero, and D. B. Vigneron, “MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy,” American Journal of Neuroradiology, vol. 27, no. 3, pp. 533–547, 2006.
V. J. Burton, G. Gerner, E. Cristofalo, S. Chung, J. M. Jennings, C. Parkinson, R. C. Koehler, R. Chavez-Valdez, M. V Johnston, F. J. Northington, and J. K. Lee, “A pilot cohort study of cerebral autoregulation and 2-year neurodevelopmental outcomes in neonates with hypoxic-ischemic encephalopathy who received therapeutic hypothermia.,” BMC neurology, vol. 15, p. 209, 2015.
J. A. Howlett, F. J. Northington, M. M. Gilmore, A. Tekes, T. A. G. M. Huisman, C. Parkinson, S. Chung, J. M. Jennings, J. J. Jamrogowicz, A. C. Larson, C. U. Lehmann, E. Jackson, K. M. Brady, R. C. Koehler, and J. K. Lee, “Cerebrovascular autoregulation and neurologic injury in neonatal hypoxic–ischemic encephalopathy,” translational investigations, vol. 74, no. 5, pp. 525–535, 2013.
M. A. Awal, M. M. Lai, G. Azemi, B. Boashash, and P. B. Colditz, “EEG background features that predict outcome in term neonates with hypoxic ischaemic encephalopathy: A structured review,” Clinical Neurophysiology, vol. 127, no. 1, pp. 285–296, 2016.
L. Kharoshankaya, N. J. Stevenson, V. Livingstone, D. M. Murray, B. P. Murphy, C. E. Ahearne, and G. B. Boylan, “Seizure burden and neurodevelopmental outcome in neonates with hypoxic-ischemic encephalopathy,” Developmental Medicine & Child Neurology, 2016.
J. M. Perlman, “Intervention strategies for neonatal hypoxic-ischemic cerebral injury,” Clinical Therapeutics, vol. 28, no. 9, pp. 1353–1365, 2006.
A. J. Gunn, A. R. Laptook, N. J. Robertson, J. D. Barks, M. Thoresen, G. Wassink, and L. Bennet, “Therapeutic hypothermia translates from ancient history in to practice,” Pediatric Research, no. August, 2016.
J. W. McDonald, C. K. Chen, W. H. Trescher, and M. V. Johnston, “The severity of excitotoxic brain injury is dependent on brain temperature in immature rat,” Neuroscience Letters, vol. 126, no. 1, pp. 83–86, 1991.
M. Thoresen, S. Satas, M. Puka-Sundvall, A. Whitelaw, A. Hallstrom, E. M. Loberg, U. Ungerstedt, P. A. Steen, and H. Hagberg, “Post-hypoxic hypothermia reduces cerebrocortical release of NO and excitotoxins,” Neuroreport, vol. 8, no. 15, pp. 3359–3362, 1997.
S. Jacobs, R. Hunt, W. Tarnow-Mordi, T. Inder, and P. Davis, “Cooling for Newborns with Hypoxic Ischaemic Encephalopathy,” CochraneDatabase of SystematicReviews, no. 1, pp. 385–385, 2013.
J. J. Kim, N. Buchbinder, S. Ammanuel, R. Kim, E. Moore, N. O. Donnell, J. K. Lee, R. H. Allen, R. W. Lee, and M. V Johnston, “Cost-effective therapeutic hypothermia treatment device for hypoxic ischemic encephalopathy,” Medical Devices: Evidence and Research, pp. 1–10, 2013.
G. Favrais, P. Tourneux, E. Lopez, X. Durrmeyer, G. Gascoin, D. Ramful, E. Zana-Taieb, and O. Baud, “Impact of common treatments given in the perinatal period on the developing brain,” Neonatology, vol. 106, no. 3, pp. 163–172, 2014.
H. L. Halliday, “Update on Postnatal Steroids,” Neonatology, vol. 111, pp. 415–422, 2017.
R. Rao, S. Trivedi, Z. Vesoulis, S. M. Liao, C. D. Smyser, and A. M. Mathur, “Safety and Short-Term Outcomes of Therapeutic Hypothermia in Preterm Neonates 34-35 Weeks Gestational Age with Hypoxic-Ischemic Encephalopathy.,” The Journal of pediatrics, vol. 183, pp. 37–42, Apr. 2017.
J. W. McDonald, F. S. Silverstein, and M. V. Johnston, “Magnesium reduces N-methyl-d-aspartate (NMDA)-mediated brain injury in perinatal rats,” Neuroscience Letters, vol. 109, no. 1–2, pp. 234–238, 1990.
K. Nelson and J. Grether, “Can Magnesium Reduce the Risk of Cerebral Palsy in Very Low Birthweight infants?,” Pediatrics, vol. 95, no. 2, pp. 263–69, 1995.
S. Marret, L. Marpeau, C. Follet-Bouhamed, G. Cambonie, D. Astruc, B. Delaporte, H. Bruel, B. Guillois, D. Pinquier, V. Zupan-Simunek, and J. Bénichou, “Effet du sulfate de magnésium sur la mortalité et la morbidité neurologique chez le prématuré de moins de 33 semaines, avec recul à deux ans : résultats de l’essai prospectif multicentrique contre placebo PREMAG,” Gynecologie Obstetrique Fertilite, vol. 36, no. 3, pp. 278–288, 2008.
A. Conde-Agudelo and R. Romero, “Antenatal magnesium sulfate for the prevention of cerebral palsy in preterm infants less than 34 weeks’ gestation: a systematic review and metaanalysis,” American Journal of Obstetrics and Gynecology, vol. 200, no. 6, pp. 595–609, 2009.
M. Levene, M. Blennow, A. Whitelaw, E. Hanko, V. Fellman, and R. Hartley, “Acute effects of two different doses of magnesium sulphate in infants with birth asphyxia.,” Archives of disease in childhood Fetal and neonatal edition, vol. 73, no. 3, pp. F174-7, 1995.
A. VAN HARREVELD, “Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle.,” Journal of neurochemistry, vol. 3, no. 4, pp. 300–15, 1959.
J. W. Mcdonald, F. S. Silverstein, and M. V Johnston, “Neuroprotective effects of MK-801, TCP, PCP and CPP against N-methyl-o-aspartate induced neurotoxicity in an in vivo perinatal rat model,” Brain Research, vol. 490, pp. 33–40, 1989.
C. Hobbs, M. Thoresen, A. Tucker, K. Aquilina, E. Chakkarapani, and J. Dingley, “Xenon and hypothermia combine additively, offering long-term functional and histopathologic neuroprotection after neonatal hypoxia/ischemia.,” Stroke, vol. 39, no. 4, pp. 1307–1313, Apr. 2008.
M. Thoresen, C. E. Hobbs, T. Wood, E. Chakkarapani, and J. Dingley, “Cooling combined with immediate or delayed xenon inhalation provides equivalent long-term neuroprotection after neonatal hypoxia-ischemia.,” Journal of cerebral blood flow and metabolism, vol. 29, no. 4, pp. 707–714, Apr. 2009.
H. Sabir, D. Osredkar, E. Maes, T. Wood, and M. Thoresen, “Xenon combined with therapeutic hypothermia is not neuroprotective after severe hypoxia-ischemia in neonatal rats,” PLoS ONE, vol. 11, no. 6, pp. 1–10, 2016.
D. Azzopardi, N. J. Robertson, A. Bainbridge, E. Cady, G. Charles-edwards, A. Deierl, G. Fagiolo, N. P. Franks, J. Griffi, J. Hajnal, E. Juszczak, B. Kapetanakis, L. Linsell, M. Maze, O. Omar, B. Strohm, N. Tusor, and A. D. Edwards, “Moderate hypothermia within 6 h of birth plus inhaled xenon versus moderate hypothermia alone after birth asphyxia ( TOBY-Xe ): a proof-of-concept , open-label , randomised controlled trial,” Lancet Neurol, vol. 15, pp. 145–153, 2016.
X.-J. Tang and F. Xing, “Calcium-permeable AMPA receptors in neonatal hypoxic-ischemic encephalopathy (Review).,” Biomedical reports, vol. 1, no. 6, pp. 828–832, 2013.
L. Filippi, P. Fiorini, S. Catarzi, E. Berti, L. Padrini, E. Landucci, G. Donzelli, L. Bartalena, E. Fiorentini, A. Boldrini, M. Giampietri, R. T. Scaramuzzo, G. la Marca, M. L. Della Bona, S. Fiori, F. Tinelli, A. Bancale, A. Guzzetta, G. Cioni, T. Pisano, M. Falchi, and R. Guerrini, “Safety and efficacy of topiramate in neonates with hypoxic ischemic encephalopathy treated with hypothermia (NeoNATI): a feasibility study.,” The journal of maternal-fetal & neonatal medicine, pp. 1–8, Mar. 2017.
R. M. Pressler, G. B. Boylan, N. Marlow, M. Blennow, C. Chiron, J. H. Cross, L. S. de Vries, B. Hallberg, L. Hellström-Westas, V. Jullien, V. Livingstone, B. Mangum, B. Murphy, D. Murray, G. Pons, J. Rennie, R. Swarte, M. C. Toet, S. Vanhatalo, and S. Zohar, “Bumetanide for the treatment of seizures in newborn babies with hypoxic ischaemic encephalopathy (NEMO): An open-label, dose finding, and feasibility phase 1/2 trial,” The Lancet Neurology, vol. 14, no. 5, pp. 469–477, 2015.
T. Koyuncuoglu, M. Turkyilmaz, B. Goren, M. Cetinkaya, M. Cansev, and T. Alkan, “Uridine protects against hypoxic-ischemic brain injury by reducing histone deacetylase activity in neonatal rats.,” Restorative neurology and neuroscience, vol. 33, no. 5, pp. 777–784, 2015.
S. Tordjman, S. Chokron, R. Delorme, A. Charrier, E. Bellissant, N. Jaafari, and C. Fougerou, “Melatonin: Pharmacology, Functions and Therapeutic Benefits.,” Current neuropharmacology, vol. 15, no. 3, pp. 434–443, Apr. 2017.
B. Stankov, G. Biella, C. Panara, V. Lucini, S. Capsoni, J. Fauteck, B. Cozzi, and F. Fraschini, “Melatonin signal transduction and mechanism of action in the central nervous system: using the rabbit cortex as a model.,” Endocrinology, vol. 130, no. 4, pp. 2152–2159, Apr. 1992.
Y. W. Wu and F. F. Gonzalez, “Erythropoietin: A novel therapy for hypoxic-ischaemic encephalopathy?,” Developmental Medicine and Child Neurology, vol. 57, no. S3, pp. 34–39, 2015.
R. R. Malla, R. Asimi, M. A. Teli, F. Shaheen, and M. A. Bhat, “Erythropoietin monotherapy in perinatal asphyxia with moderate to severe encephalopathy : a randomized placebo-controlled trial,” vol. 37, no. 5, pp. 596–601, 2017.
Y. W. Wu, A. M. Mathur, T. Chang, R. C. Mckinstry, and S. B. Mulkey, “High-Dose Erythropoietin and Hypothermia for Hypoxic-Ischemic Encephalopathy : A Phase II Trial,” vol. 137, no. 6, 2016.
S. Kannan, H. Dai, R. S. Navath, B. Balakrishnan, a. Jyoti, J. Janisse, R. Romero, and R. M. Kannan, “Dendrimer-Based Postnatal Therapy for Neuroinflammation and Cerebral Palsy in a Rabbit Model,” Science Translational Medicine, vol. 4, no. 130, p. 130ra46-130ra46, 2012.
E. Nance, M. Porambo, F. Zhang, M. K. Mishra, M. Buelow, R. Getzenberg, M. Johnston, R. M. Kannan, A. Fatemi, and S. Kannan, “Systemic dendrimer-drug treatment of ischemia-induced neonatal white matter injury,” Journal of Controlled Release, vol. 214, pp. 112–120, 2015.
R. Sweda, A. W. Phillips, J. Marx, M. V. Johnston, M. A. Wilson, and A. Fatemi, “Glial-Restricted Precursors Protect Neonatal Brain Slices from Hypoxic-Ischemic Cell Death Without Direct Tissue Contact,” Stem Cells and Development, vol. 25, no. 13, pp. 975–985, 2016.
L. Braccioli, C. J. Heijnen, P. J. Coffer, and C. H. Nijboer, “Delayed administration of neural stem cells after hypoxia-ischemia reduces sensorimotor deficits, cerebral lesion size and neuroinflammation in neonatal mice,” Pediatric Research, no. February, 2016.
R. K. Jellema, V. Lima Passos, D. R. M. G. Ophelders, T. G. A. M. Wolfs, A. Zwanenburg, S. De Munter, M. Nikiforou, J. J. P. Collins, E. Kuypers, G. M. J. Bos, H. W. Steinbusch, J. Vanderlocht, P. Andriessen, W. T. V Germeraad, and B. W. Kramer, “Systemic G-CSF attenuates cerebral inflammation and hypomyelination but does not reduce seizure burden in preterm sheep exposed to global hypoxia-ischemia.,” Experimental neurology, vol. 250, pp. 293–303, Dec. 2013.
C. M. Cotten, A. P. Murtha, R. N. Goldberg, C. A. Grotegut, P. B. Smith, R. F. Goldstein, K. A. Fisher, K. E. Gustafson, B. Waters-Pick, G. K. Swamy, B. Rattray, S. Tan, and J. Kurtzberg, “Feasibility of autologous cord blood cells for infants with hypoxic-ischemic encephalopathy.,” The Journal of pediatrics, vol. 164, no. 5, p. 973–979.e1, May 2014.
P. Jouvet, F. M. Cowan, P. Cox, E. Lazda, M. A. Rutherford, J. Wigglesworth, H. Mehmet, and A. D. Edwards, “Reproducibility and Accuracy of MR Imaging of the Brain after Severe Birth Asphyxia,” American Journal of Neuroradiology, vol. 20, no. August, pp. 1343–1348, 1999.
B. Berg, M. J. Aminoff, and R. B. Daroff, “Child Neurology, History of,” in Encyclopedia of the Neurological Sciences, Second Edition., 2014, pp. 784–785.
F. R. Ford, Birth Injuries of the Central Nervous System. Part I - CEREBRAL BIRTH INJURIES. Baltimore, MD: The Williams and Wilkins Company, 1927.
S. Ashwal, The Founders of Child Neurology, First. San Fransciso, California: Norman Publishing, 1990.

References

D. A. Stumpf, “THE FOUNDING OF PEDIATRIC NEUROLOGY IN AMERICA,” Bull NY Acad Med, vol. 57, no. 9, pp. 804–816, 1981.

S. Ashwal and R. Rust, “Child neurology in the 20th century,” Pediatric Research, vol. 53, no. 2, pp. 345–361, 2003.

The American College of Obstetricians and Gynecologists, “Neonatal Encephalopathy and Neurologic Outcome, Second Edition. Report of the American College of Obstetricians and Gynecologists’ Task Force on Neonatal Encephalopathy,” OBSTETRICS & GYNECOLOGY, vol. 123, no. 4, pp. 896–901, 2014.

A. C. C. Lee, N. Kozuki, H. Blencowe, T. Vos, A. Bahalim, G. L. Darmstadt, S. Niermeyer, M. Ellis, N. J. Robertson, S. Cousens, and J. E. Lawn, “Intrapartum-related neonatal encephalopathy incidence and impairment at regional and global levels for 2010 with trends from 1990.,” Pediatric research, vol. 74 Suppl 1, no. December, pp. 50–72, 2013.

M. S. Sarnat, Harvey B. and Sarnat, “Neonatal Encephalopathy Following Fetal Distress: A Clinical and Electroencephalographic Study,” Arch Neurol, vol. 33, pp. 696–705, 1976.

C. E. Ahearne, N. M. Denihan, B. H. Walsh, S. N. Reinke, L. C. Kenny, G. B. Boylan, D. I. Broadhurst, and D. M. Murray, “Early Cord Metabolite Index and Outcome in Perinatal Asphyxia and Hypoxic-Ischaemic Encephalopathy,” Neonatology, pp. 296–302, 2016.

S. L. Bonifacioa, L. S. DeVriesb, and F. Groenendaalb, “Impact of hypothermia on predictors of poor outcome: how do we decide to redirect care?,” Semin fetal neonatol Med 2015, vol. 20, no. 2, pp. 122–127, 2015.

J. E. Rice, R. C. Vannucci, and J. B. Brierley, “The influence of immaturity on hypoxic-ischemic brain damage in the rat.,” Annals of neurology, vol. 9, no. 2, pp. 131–41, 1981.

R. C. Vannucci and S. J. Vannucci, “Perinatal hypoxic-ischemic brain damage: Evolution of an animal model,” Developmental Neuroscience, vol. 27, no. 2–4. pp. 81–86, 2005.

M. V. Johnston, “Neurotransmitter alterations in a model of perinatal hypoxrc-ischemc brain injury,” Annals of neurology, vol. 13, pp. 511–518, 1983.

L. Huang, F. Zhao, Y. Qu, L. Zhang, Y. Wang, and D. Mu, “Animal models of hypoxic-ischemic encephalopathy: optimal choices for the best outcomes,” Reviews in the Neurosciences, p. [Epub ahead of print], 2016.

J. W. McDonald and M. V Johnston, “Physiological and pathophysiological roles of excitatory amino acids during central nervous system development.,” Brain research Brain research reviews, vol. 15, no. 1, pp. 41–70, 1990.

M. V Johnston, A. Fatemi, M. A. Wilson, and F. Northington, “Treatment advances in neonatal neuroprotection and neurointensive care,” vol. 10, no. 4, pp. 372–382, 2011.

R. Lujan, R. Shigemoto, and G. Lopez-Bendito, “Glutamate and GABA receptor signalling in the developing brain,” Neuroscience, vol. 130, no. 3, pp. 567–580, 2005.

M. V Johnston, W. Nakajima, and H. Hagberg, “Mechanisms of hypoxic neurodegeneration in the developing brain,” Neuroscientist, vol. 8, no. 3, pp. 212–220, 2002.

M. V Johnston, “Excitotoxicity in Neonatal Hypoxia,” Mental retardation and developmental disabilities, vol. 7, pp. 229–234, 2001.

Q. Ma and L. Zhang, “Epigenetic programming of hypoxic-ischemic encephalopathy in response to fetal hypoxia,” Progress in Neurobiology, vol. 124, pp. 28–48, 2015.

M. V. Johnston, “Neurotransmitters and vulnerability of the developing brain,” Brain and Development, vol. 17, no. 5, pp. 301–306, 1995.

E. Rocha-Ferreira and M. Hristova, “Plasticity in the neonatal brain following hypoxic-ischaemic injury,” vol. 2016, 2016.

B. B. Kostandy, “The role of glutamate in neuronal ischemic injury: The role of spark in fire,” Neurological Sciences, vol. 33, no. 2, pp. 223–237, 2012.

S. M. Rothman and J. W. Olney, “Glutamate and the Pathophysiology of Hypoxic-Ischemic Brain Damage,” Annals of neurology, vol. 19, pp. 111–1986, 1986.

H. Hagberg, P. Andersson, I. Kjellmer, K. Thiringer, and M. Thordstein, “Extracellular overflow of glutamate, aspartate, GABA and taurine in the cortex and basal ganglia of fetal lambs during hypoxia-ischemia,” Neuroscience Letters, vol. 78, no. 3, pp. 311–317, 1987.

R. S. Riikonen, P. O. Kero, and O. G. Simell, “Excitatory amino acids in cerebrospinal fluid in neonatal asphyxia.,” Pediatric neurology, vol. 8, no. 1, pp. 37–40, 1992.

M. T. Khashaba, B. O. Shouman, A. A. Shaltout, H. M. Al-Marsafawy, M. M. Abdel-Aziz, K. Patel, and H. Aly, “Excitatory amino acids and magnesium sulfate in neonatal asphyxia,” Brain and Development, vol. 28, no. 6, pp. 375–379, 2006.

T. Logica, S. Riviere, M. I. Holubiec, R. Castilla, G. E. Barreto, and F. Capani, “Metabolic Changes Following Perinatal Asphyxia: Role of Astrocytes and Their Interaction with Neurons.,” Frontiers in aging neuroscience, vol. 8, p. 116, 2016.

A. A. Baburamani, C. J. Ek, D. W. Walker, and M. Castillo-melendez, “Vulnerability of the developing brain to hypoxic-ischemic damage : contribution of the cerebral vasculature to injury and repair ?,” vol. 3, no. November, pp. 1–21, 2012.

A. Looney, C. Ahearne, G. B. Boylan, and D. M. Murray, “Glial Fibrillary Acidic Protein Is Not an Early Marker of Injury in Perinatal Asphyxia and Hypoxic – Ischemic Encephalopathy,” Frontiers in neurology, vol. 6, no. December, pp. 1–6, 2015.

J. Jaworska, M. Ziemka-Nalecz, J. Sypecka, and T. Zalewska, “The potential neuroprotective role of a histone deacetylase inhibitor, sodium butyrate, after neonatal hypoxia-ischemia.,” Journal of neuroinflammation, vol. 14, no. 1, p. 34, Feb. 2017.

F. Zhang, E. Nance, Y. Alnasser, R. Kannan, and S. Kannan, “Microglial migration and interactions with dendrimer nanoparticles are altered in the presence of neuroinflammation,” Journal of Neuroinflammation, pp. 1–11, 2016.

M. Ziemka-Nalecz, J. Janowska, L. Strojek, J. Jaworska, T. Zalewska, M. Frontczak-Baniewicz, and J. Sypecka, “Impact of neonatal hypoxia-ischaemia on oligodendrocyte survival, maturation and myelinating potential.,” Journal of cellular and molecular medicine, Aug. 2017.

J. Janowska and J. Sypecka, “Therapeutic Strategies for Leukodystrophic Disorders Resulting from Perinatal Asphyxia : Focus on Myelinating Oligodendrocytes,” mol neurobiol, 2017.

K. Savman, M. Blennow, K. Gustafson, E. Tarkowski, and H. Hagberg, “Cytokine Response in Cerebrospinal Fluid after Birth Asphyxia,” Pediatr Res, vol. 43, no. 6, pp. 746–751, Jun. 1998.

H. yan Lu, Q. Zhang, Q. xia Wang, and J. ying Lu, “Contribution of Histologic Chorioamnionitis and Fetal Inflammatory Response Syndrome to Increased Risk of Brain Injury in Infants With Preterm Premature Rupture of Membranes,” Pediatric Neurology, vol. 61, p. 94–98.e1, 2015.

I. Lee, N. Jeffrey, P. Huettner, C. D. Smyser, C. E. Rogers, J. S. Shimony, H. Kidokoro, I. Mysorekar, and T. E. Inder, “The impact of prenatal and neonatal infection on neurodevelopmental outcomes in very preterm infants Iris,” J Perinatol, vol. 34, no. 10, pp. 741–747, 2015.

L. F. Chalak, “Inflammatory Biomarkers of Birth Asphyxia,” Clinics in Perinatology, vol. 43, no. 3, pp. 501–510, 2016.

G. Breier, A. Damert, K. H. Plate, and W. Risau, “Angiogenesis in embryos and ischemic diseases.,” Thrombosis and haemostasis, vol. 78, no. 1, pp. 678–683, Jul. 1997.

G. D. Yancopoulos, S. Davis, N. W. Gale, J. S. Rudge, S. J. Wiegand, and J. Holash, “Vascular-specific growth factors and blood vessel formation.,” Nature, vol. 407, no. 6801, pp. 242–248, Sep. 2000.

E. Maltepe, J. V Schmidt, D. Baunoch, C. A. Bradfield, and M. C. Simon, “Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT.,” Nature, vol. 386, no. 6623, pp. 403–407, Mar. 1997.

Y. Li, P. Gonzalez, and L. Zhang, “Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: mechanisms and possible interventions.,” Progress in neurobiology, vol. 98, no. 2, pp. 145–165, Aug. 2012.

R. M. Ruddy and C. M. Morshead, “Home sweet home: the neural stem cell niche throughout development and after injury.,” Cell and tissue research, Aug. 2017.

N. Salmaso, S. Tomasi, and F. M. Vaccarino, “Neurogenesis and Maturation in Neonatal B rain Injury Preterm birth Neurogenesis Neonatal brain injury Cognitive delay,” Clinics in Perinatology, vol. 41, no. 1, pp. 229–239, 2014.

P. Morales, J. L. Fiedler, S. Andre´s, C. Berrios, D. Huaiquı´n, D. Bustamante, S. Cardenas, E. Parra, and H.-M. M., “Plasticity of Hippocampus Following Perinatal Asphyxia : Effects on Postnatal Apoptosis and Neurogenesis,” Journal of Neuroscience Research, vol. 86, pp. 2650–2662, 2008.

A. Tapia-Bustos, R. Perez-Lobos, V. Vio, C. Lespay-Rebolledo, E. Palacios, A. Chiti-Morales, D. Bustamante, M. Herrera-Marschitz, and P. Morales, “Modulation of Postnatal Neurogenesis by Perinatal Asphyxia: Effect of D1 and D2 Dopamine Receptor Agonists.,” Neurotoxicity research, vol. 31, no. 1, pp. 109–121, Jan. 2017.

J. Waddell, M. Hanscom, N. S. Edwards, M. C. Mckenna, and M. M. Mccarthy, “Sex differences in cell genesis , hippocampal volume and behavioral outcomes in a rat model of neonatal HI,” Experimental Neurology, vol. 275, pp. 285–295, 2016.

G. Orman, J. E. Benson, C. F. Kweldam, T. Bosemani, A. Tekes, M. R. de Jong, D. Seyfert, F. J. Northington, A. Poretti, and T. A. G. M. Huisman, “Neonatal Head Ultrasonography Today: A Powerful Imaging Tool!,” Journal of Neuroimaging, vol. 25, no. 1, pp. 31–55, 2015.

S. Miller, V. Ramaswamy, D. Michelson, B. AJ, B. Holshouser, N. Wycliffe, G. DV, D. Deming, P. JC, W. YW, S. Ashwal, and F. DM, “Patterns of brain injury in term neonatal encephalopathy,” J Pediatr, vol. 146, pp. 453–60, 2005.

L. S. De Vries and F. Groenendaal, “Patterns of neonatal hypoxic – ischaemic brain injury,” Neuroradiology, vol. 52, pp. 555–566, 2010.

J. J. Volpe, “Neonatal encephalopathy: An inadequate term for hypoxic-ischemic encephalopathy,” Annals of Neurology, vol. 72, no. 2, pp. 156–166, 2012.

J. J. Volpe, “The Encephalopathy of Prematurity-Brain Injury and Impaired Brain Development Inextricably Intertwined,” Seminars in Pediatric Neurology, vol. 16, no. 4, pp. 167–178, 2009.

A. J. Barkovich, B. L. Hajnal, D. Vigneron, A. Sola, J. C. Partridge, F. Allen, and D. M. Ferriero, “Prediction of neuromotor outcome in perinatal asphyxia: Evaluation of MR scoring systems,” American Journal of Neuroradiology, vol. 19, no. 1, pp. 143–149, 1998.

G. Arca-Diaz, T. J. Re, M. Drottar, C. R. Fortuno, K. De Macedo-Rodrigues, K. Im, J. Figueras-Aloy, and P. E. Grant, “Can cerebellar and brainstem apparent diffusion coefficient (ADC) values predict neuromotor outcome in term neonates with hypoxic-ischemic encephalopathy (HIE) treated with hypothermia?,” PloS one, vol. 12, no. 7, p. e0178510, 2017.

E.-M. Heursen, A. Zuazo Ojeda, I. Benavente Fernandez, G. Jimenez Gomez, R. Campuzano Fernandez-Colima, J. Paz-Exposito, and S. P. Lubian Lopez, “Prognostic Value of the Apparent Diffusion Coefficient in Newborns with Hypoxic-Ischaemic Encephalopathy Treated with Therapeutic Hypothermia.,” Neonatology, vol. 112, no. 1, pp. 67–72, 2017.

P. Ward, S. Counsell, J. Allsop, F. Cowan, Y. Shen, D. Edwards, and M. Rutherford, “Reduced Fractional Anisotropy on Diffusion Tensor Magnetic Resonance Imaging After Hypoxic-Ischemic Encephalopathy,” Pediatrics, vol. 117, no. 4, p. e619 LP-e630, Apr. 2006.

A. N. Massaro, R. B. Govindan, G. Vezina, T. Chang, N. N. Andescavage, Y. Wang, T. Al-shargabi, M. Metzler, K. Harris, A. J. Plessis, Y. Wang, M. Metzler, K. Harris, and P. Aj, “Impaired cerebral autoregulation and brain injury in newborns with hypoxic-ischemic encephalopathy treated with hypothermia,” J neurophsiol, vol. 114, pp. 818–824, 2015.

F. Groenendaal and L. S. de Vries, “Fifty years of brain imaging in neonatal encephalopathy following perinatal asphyxia.,” Pediatric research, no. May, 2016.

T. Alderliesten, L. S. de Vries, L. Staats, I. C. van Haastert, L. Weeke, M. J. N. L. Benders, C. Koopman-Esseboom, and F. Groenendaal, “MRI and spectroscopy in (near) term neonates with perinatal asphyxia and therapeutic hypothermia.,” Archives of disease in childhood Fetal and neonatal edition, vol. 102, no. 2, pp. F147–F152, Mar. 2017.

P. E. Sijens, K. Wischniowsky, and H. J. Ter Horst, “The prognostic value of proton magnetic resonance spectroscopy in term newborns treated with therapeutic hypothermia following asphyxia.,” Magnetic resonance imaging, vol. 42, pp. 82–87, Jun. 2017.

A. J. Barkovich, S. P. Miller, A. Bartha, N. Newton, S. E. G. Hamrick, P. Mukherjee, O. A. Glenn, D. Xu, J. C. Partridge, D. M. Ferriero, and D. B. Vigneron, “MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy,” American Journal of Neuroradiology, vol. 27, no. 3, pp. 533–547, 2006.

V. J. Burton, G. Gerner, E. Cristofalo, S. Chung, J. M. Jennings, C. Parkinson, R. C. Koehler, R. Chavez-Valdez, M. V Johnston, F. J. Northington, and J. K. Lee, “A pilot cohort study of cerebral autoregulation and 2-year neurodevelopmental outcomes in neonates with hypoxic-ischemic encephalopathy who received therapeutic hypothermia.,” BMC neurology, vol. 15, p. 209, 2015.

J. A. Howlett, F. J. Northington, M. M. Gilmore, A. Tekes, T. A. G. M. Huisman, C. Parkinson, S. Chung, J. M. Jennings, J. J. Jamrogowicz, A. C. Larson, C. U. Lehmann, E. Jackson, K. M. Brady, R. C. Koehler, and J. K. Lee, “Cerebrovascular autoregulation and neurologic injury in neonatal hypoxic–ischemic encephalopathy,” translational investigations, vol. 74, no. 5, pp. 525–535, 2013.

M. A. Awal, M. M. Lai, G. Azemi, B. Boashash, and P. B. Colditz, “EEG background features that predict outcome in term neonates with hypoxic ischaemic encephalopathy: A structured review,” Clinical Neurophysiology, vol. 127, no. 1, pp. 285–296, 2016.

L. Kharoshankaya, N. J. Stevenson, V. Livingstone, D. M. Murray, B. P. Murphy, C. E. Ahearne, and G. B. Boylan, “Seizure burden and neurodevelopmental outcome in neonates with hypoxic-ischemic encephalopathy,” Developmental Medicine & Child Neurology, 2016.

J. M. Perlman, “Intervention strategies for neonatal hypoxic-ischemic cerebral injury,” Clinical Therapeutics, vol. 28, no. 9, pp. 1353–1365, 2006.

A. J. Gunn, A. R. Laptook, N. J. Robertson, J. D. Barks, M. Thoresen, G. Wassink, and L. Bennet, “Therapeutic hypothermia translates from ancient history in to practice,” Pediatric Research, no. August, 2016.

J. W. McDonald, C. K. Chen, W. H. Trescher, and M. V. Johnston, “The severity of excitotoxic brain injury is dependent on brain temperature in immature rat,” Neuroscience Letters, vol. 126, no. 1, pp. 83–86, 1991.

M. Thoresen, S. Satas, M. Puka-Sundvall, A. Whitelaw, A. Hallstrom, E. M. Loberg, U. Ungerstedt, P. A. Steen, and H. Hagberg, “Post-hypoxic hypothermia reduces cerebrocortical release of NO and excitotoxins,” Neuroreport, vol. 8, no. 15, pp. 3359–3362, 1997.

S. Jacobs, R. Hunt, W. Tarnow-Mordi, T. Inder, and P. Davis, “Cooling for Newborns with Hypoxic Ischaemic Encephalopathy,” CochraneDatabase of SystematicReviews, no. 1, pp. 385–385, 2013.

J. J. Kim, N. Buchbinder, S. Ammanuel, R. Kim, E. Moore, N. O. Donnell, J. K. Lee, R. H. Allen, R. W. Lee, and M. V Johnston, “Cost-effective therapeutic hypothermia treatment device for hypoxic ischemic encephalopathy,” Medical Devices: Evidence and Research, pp. 1–10, 2013.

G. Favrais, P. Tourneux, E. Lopez, X. Durrmeyer, G. Gascoin, D. Ramful, E. Zana-Taieb, and O. Baud, “Impact of common treatments given in the perinatal period on the developing brain,” Neonatology, vol. 106, no. 3, pp. 163–172, 2014.

H. L. Halliday, “Update on Postnatal Steroids,” Neonatology, vol. 111, pp. 415–422, 2017.

R. Rao, S. Trivedi, Z. Vesoulis, S. M. Liao, C. D. Smyser, and A. M. Mathur, “Safety and Short-Term Outcomes of Therapeutic Hypothermia in Preterm Neonates 34-35 Weeks Gestational Age with Hypoxic-Ischemic Encephalopathy.,” The Journal of pediatrics, vol. 183, pp. 37–42, Apr. 2017.

J. W. McDonald, F. S. Silverstein, and M. V. Johnston, “Magnesium reduces N-methyl-d-aspartate (NMDA)-mediated brain injury in perinatal rats,” Neuroscience Letters, vol. 109, no. 1–2, pp. 234–238, 1990.

K. Nelson and J. Grether, “Can Magnesium Reduce the Risk of Cerebral Palsy in Very Low Birthweight infants?,” Pediatrics, vol. 95, no. 2, pp. 263–69, 1995.

S. Marret, L. Marpeau, C. Follet-Bouhamed, G. Cambonie, D. Astruc, B. Delaporte, H. Bruel, B. Guillois, D. Pinquier, V. Zupan-Simunek, and J. Bénichou, “Effet du sulfate de magnésium sur la mortalité et la morbidité neurologique chez le prématuré de moins de 33 semaines, avec recul à deux ans : résultats de l’essai prospectif multicentrique contre placebo PREMAG,” Gynecologie Obstetrique Fertilite, vol. 36, no. 3, pp. 278–288, 2008.

A. Conde-Agudelo and R. Romero, “Antenatal magnesium sulfate for the prevention of cerebral palsy in preterm infants less than 34 weeks’ gestation: a systematic review and metaanalysis,” American Journal of Obstetrics and Gynecology, vol. 200, no. 6, pp. 595–609, 2009.

M. Levene, M. Blennow, A. Whitelaw, E. Hanko, V. Fellman, and R. Hartley, “Acute effects of two different doses of magnesium sulphate in infants with birth asphyxia.,” Archives of disease in childhood Fetal and neonatal edition, vol. 73, no. 3, pp. F174-7, 1995.

A. VAN HARREVELD, “Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle.,” Journal of neurochemistry, vol. 3, no. 4, pp. 300–15, 1959.

J. W. Mcdonald, F. S. Silverstein, and M. V Johnston, “Neuroprotective effects of MK-801, TCP, PCP and CPP against N-methyl-o-aspartate induced neurotoxicity in an in vivo perinatal rat model,” Brain Research, vol. 490, pp. 33–40, 1989.

C. Hobbs, M. Thoresen, A. Tucker, K. Aquilina, E. Chakkarapani, and J. Dingley, “Xenon and hypothermia combine additively, offering long-term functional and histopathologic neuroprotection after neonatal hypoxia/ischemia.,” Stroke, vol. 39, no. 4, pp. 1307–1313, Apr. 2008.

M. Thoresen, C. E. Hobbs, T. Wood, E. Chakkarapani, and J. Dingley, “Cooling combined with immediate or delayed xenon inhalation provides equivalent long-term neuroprotection after neonatal hypoxia-ischemia.,” Journal of cerebral blood flow and metabolism, vol. 29, no. 4, pp. 707–714, Apr. 2009.

H. Sabir, D. Osredkar, E. Maes, T. Wood, and M. Thoresen, “Xenon combined with therapeutic hypothermia is not neuroprotective after severe hypoxia-ischemia in neonatal rats,” PLoS ONE, vol. 11, no. 6, pp. 1–10, 2016.

D. Azzopardi, N. J. Robertson, A. Bainbridge, E. Cady, G. Charles-edwards, A. Deierl, G. Fagiolo, N. P. Franks, J. Griffi, J. Hajnal, E. Juszczak, B. Kapetanakis, L. Linsell, M. Maze, O. Omar, B. Strohm, N. Tusor, and A. D. Edwards, “Moderate hypothermia within 6 h of birth plus inhaled xenon versus moderate hypothermia alone after birth asphyxia ( TOBY-Xe ): a proof-of-concept , open-label , randomised controlled trial,” Lancet Neurol, vol. 15, pp. 145–153, 2016.

X.-J. Tang and F. Xing, “Calcium-permeable AMPA receptors in neonatal hypoxic-ischemic encephalopathy (Review).,” Biomedical reports, vol. 1, no. 6, pp. 828–832, 2013.

L. Filippi, P. Fiorini, S. Catarzi, E. Berti, L. Padrini, E. Landucci, G. Donzelli, L. Bartalena, E. Fiorentini, A. Boldrini, M. Giampietri, R. T. Scaramuzzo, G. la Marca, M. L. Della Bona, S. Fiori, F. Tinelli, A. Bancale, A. Guzzetta, G. Cioni, T. Pisano, M. Falchi, and R. Guerrini, “Safety and efficacy of topiramate in neonates with hypoxic ischemic encephalopathy treated with hypothermia (NeoNATI): a feasibility study.,” The journal of maternal-fetal & neonatal medicine, pp. 1–8, Mar. 2017.

R. M. Pressler, G. B. Boylan, N. Marlow, M. Blennow, C. Chiron, J. H. Cross, L. S. de Vries, B. Hallberg, L. Hellström-Westas, V. Jullien, V. Livingstone, B. Mangum, B. Murphy, D. Murray, G. Pons, J. Rennie, R. Swarte, M. C. Toet, S. Vanhatalo, and S. Zohar, “Bumetanide for the treatment of seizures in newborn babies with hypoxic ischaemic encephalopathy (NEMO): An open-label, dose finding, and feasibility phase 1/2 trial,” The Lancet Neurology, vol. 14, no. 5, pp. 469–477, 2015.

T. Koyuncuoglu, M. Turkyilmaz, B. Goren, M. Cetinkaya, M. Cansev, and T. Alkan, “Uridine protects against hypoxic-ischemic brain injury by reducing histone deacetylase activity in neonatal rats.,” Restorative neurology and neuroscience, vol. 33, no. 5, pp. 777–784, 2015.

S. Tordjman, S. Chokron, R. Delorme, A. Charrier, E. Bellissant, N. Jaafari, and C. Fougerou, “Melatonin: Pharmacology, Functions and Therapeutic Benefits.,” Current neuropharmacology, vol. 15, no. 3, pp. 434–443, Apr. 2017.

B. Stankov, G. Biella, C. Panara, V. Lucini, S. Capsoni, J. Fauteck, B. Cozzi, and F. Fraschini, “Melatonin signal transduction and mechanism of action in the central nervous system: using the rabbit cortex as a model.,” Endocrinology, vol. 130, no. 4, pp. 2152–2159, Apr. 1992.

Y. W. Wu and F. F. Gonzalez, “Erythropoietin: A novel therapy for hypoxic-ischaemic encephalopathy?,” Developmental Medicine and Child Neurology, vol. 57, no. S3, pp. 34–39, 2015.

R. R. Malla, R. Asimi, M. A. Teli, F. Shaheen, and M. A. Bhat, “Erythropoietin monotherapy in perinatal asphyxia with moderate to severe encephalopathy : a randomized placebo-controlled trial,” vol. 37, no. 5, pp. 596–601, 2017.

Y. W. Wu, A. M. Mathur, T. Chang, R. C. Mckinstry, and S. B. Mulkey, “High-Dose Erythropoietin and Hypothermia for Hypoxic-Ischemic Encephalopathy : A Phase II Trial,” vol. 137, no. 6, 2016.

S. Kannan, H. Dai, R. S. Navath, B. Balakrishnan, a. Jyoti, J. Janisse, R. Romero, and R. M. Kannan, “Dendrimer-Based Postnatal Therapy for Neuroinflammation and Cerebral Palsy in a Rabbit Model,” Science Translational Medicine, vol. 4, no. 130, p. 130ra46-130ra46, 2012.

E. Nance, M. Porambo, F. Zhang, M. K. Mishra, M. Buelow, R. Getzenberg, M. Johnston, R. M. Kannan, A. Fatemi, and S. Kannan, “Systemic dendrimer-drug treatment of ischemia-induced neonatal white matter injury,” Journal of Controlled Release, vol. 214, pp. 112–120, 2015.

R. Sweda, A. W. Phillips, J. Marx, M. V. Johnston, M. A. Wilson, and A. Fatemi, “Glial-Restricted Precursors Protect Neonatal Brain Slices from Hypoxic-Ischemic Cell Death Without Direct Tissue Contact,” Stem Cells and Development, vol. 25, no. 13, pp. 975–985, 2016.

L. Braccioli, C. J. Heijnen, P. J. Coffer, and C. H. Nijboer, “Delayed administration of neural stem cells after hypoxia-ischemia reduces sensorimotor deficits, cerebral lesion size and neuroinflammation in neonatal mice,” Pediatric Research, no. February, 2016.

R. K. Jellema, V. Lima Passos, D. R. M. G. Ophelders, T. G. A. M. Wolfs, A. Zwanenburg, S. De Munter, M. Nikiforou, J. J. P. Collins, E. Kuypers, G. M. J. Bos, H. W. Steinbusch, J. Vanderlocht, P. Andriessen, W. T. V Germeraad, and B. W. Kramer, “Systemic G-CSF attenuates cerebral inflammation and hypomyelination but does not reduce seizure burden in preterm sheep exposed to global hypoxia-ischemia.,” Experimental neurology, vol. 250, pp. 293–303, Dec. 2013.

C. M. Cotten, A. P. Murtha, R. N. Goldberg, C. A. Grotegut, P. B. Smith, R. F. Goldstein, K. A. Fisher, K. E. Gustafson, B. Waters-Pick, G. K. Swamy, B. Rattray, S. Tan, and J. Kurtzberg, “Feasibility of autologous cord blood cells for infants with hypoxic-ischemic encephalopathy.,” The Journal of pediatrics, vol. 164, no. 5, p. 973–979.e1, May 2014.

P. Jouvet, F. M. Cowan, P. Cox, E. Lazda, M. A. Rutherford, J. Wigglesworth, H. Mehmet, and A. D. Edwards, “Reproducibility and Accuracy of MR Imaging of the Brain after Severe Birth Asphyxia,” American Journal of Neuroradiology, vol. 20, no. August, pp. 1343–1348, 1999.

B. Berg, M. J. Aminoff, and R. B. Daroff, “Child Neurology, History of,” in Encyclopedia of the Neurological Sciences, Second Edition., 2014, pp. 784–785.

F. R. Ford, Birth Injuries of the Central Nervous System. Part I - CEREBRAL BIRTH INJURIES. Baltimore, MD: The Williams and Wilkins Company, 1927.

S. Ashwal, The Founders of Child Neurology, First. San Fransciso, California: Norman Publishing, 1990.

The Quest for Neuroprotection for Injuries in the Developing Brain

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Ali Fatemi

Michael Johnston, Kennedy Krieger Institute and Johns Hopkins University School of Medicine

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