Pharmacologic Neuroprotective Strategies in Neonatal Brain Injury

Clinics in Perinatology

Volumn 41, Issue 1, 2014, Pages 119-131

  Juul, Sandra E ^a   Ferriero, Donna M ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain injury; Hypoxic ischemic encephalopathy; Preconditioning; Prematurity

Indexed keywords

ACETYLCYSTEINE; ALLOPURINOL; ALPHA TOCOPHEROL; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; ASCORBIC ACID; ERYTHROPOIETIN; GRANULOCYTE COLONY STIMULATING FACTOR; GROWTH FACTOR; MAGNESIUM SULFATE; MELATONIN; MEMANTINE; NEURONAL NITRIC OXIDE SYNTHASE INHIBITOR; NEUROPROTECTIVE AGENT; OMEGA 3 FATTY ACID; PLACEBO; RESVERATROL; SOMATOMEDIN C; TETRAHYDROBIOPTERIN; TOPIRAMATE; UNCLASSIFIED DRUG; VASCULOTROPIN; XENON;

BRAIN INJURY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG MEGADOSE; EXCITOTOXICITY; GESTATIONAL AGE; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INDUCED HYPOTHERMIA; MAXIMUM PLASMA CONCENTRATION; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROPROTECTION; NEWBORN DEATH; NEWBORN DISEASE; NONHUMAN; ONSET AGE; OXIDATIVE STRESS; PERINATAL ASPHYXIA; PREMATURITY; PRIORITY JOURNAL; REVIEW; RISK REDUCTION; SALVAGE THERAPY;

EID: 84893719497     PISSN: 00955108     EISSN: 15579840     Source Type: Journal    
DOI: 10.1016/j.clp.2013.09.004     Document Type: Review

References (66)

1. Hamilton B.E., Hoyert D.L., Martin J.A., et al. Annual summary of vital statistics: 2010-2011. Pediatrics 2013, 131:548-558.
2. O'Shea T.M., Allred E.N., Dammann O., et al. The ELGAN study of the brain and related disorders in extremely low gestational age newborns. Early Hum Dev 2009, 85:719-725.
3. Stoll B.J., Hansen N.I., Bell E.F., et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics 2010, 126:443-456.
4. Gargus R.A., Vohr B.R., Tyson J.E., et al. Unimpaired outcomes for extremely low birth weight infants at 18 to 22 months. Pediatrics 2009, 124:112-121.
5. Lodygensky G.A., Vasung L., Sizonenko S.V., et al. Neuroimaging of cortical development and brain connectivity in human newborns and animal models. J Anat 2010, 217:418-428.
6. Volpe J.J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009, 8:110-124.
7. Back S.A., Riddle A., McClure M.M. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007, 38:724-730.
8. Black R.E., Cousens S., Johnson H.L., et al. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010, 375:1969-1987.
9. Kurinczuk J.J., White-Koning M., Badawi N. Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 2010, 86:329-338.
10. van Vliet E.O., de Kieviet J.F., Oosterlaan J., et al. Perinatal infections and neurodevelopmental outcome in very preterm and very low-birth-weight infants: a meta-analysis. JAMA Pediatr 2013, 167:662-668.
11. Badawi N., Kurinczuk J.J., Keogh J.M., et al. Intrapartum risk factors for newborn encephalopathy: the Western Australian case-control study. BMJ 1998, 317:1554-1558.
12. Wu Y.W., Croen L.A., Shah S.J., et al. Cerebral palsy in a term population: risk factors and neuroimaging findings. Pediatrics 2006, 118:690-697.
13. Eklind S., Mallard C., Arvidsson P., et al. Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res 2005, 58:112-116.
14. Vontell R., Supramaniam V., Thornton C., et al. Toll-like receptor 3 expression in glia and neurons alters in response to white matter injury in preterm infants. Dev Neurosci 2013, 35(2-3):130-139.
15. Stridh L., Ek C.J., Wang X., et al. Regulation of toll-like receptors in the choroid plexus in the immature brain after systemic inflammatory stimuli. Transl Stroke Res 2013, 4:220-227.
16. Fleiss B., Gressens P. Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsyα. Lancet Neurol 2012, 11:556-566.
17. Gucuyener K., Atalay Y., Aral Y.Z., et al. Excitatory amino acids and taurine levels in cerebrospinal fluid of hypoxic ischemic encephalopathy in newborn. Clin Neurol Neurosurg 1999, 101:171-174.
18. Jensen F.E. Developmental factors regulating susceptibility to perinatal brain injury and seizures. Curr Opin Pediatr 2006, 18:628-633.
19. Buonocore G., Perrone S., Bracci R. Free radicals and brain damage in the newborn. Biol Neonate 2001, 79:180-186.
20. Hagberg H., Gressens P., Mallard C. Inflammation during fetal and neonatal life: implications for neurologic and neuropsychiatric disease in children and adults. Ann Neurol 2012, 71:444-457.
21. Chavez-Valdez R., Martin L.J., Northington F.J. Programmed necrosis: a prominent mechanism of cell death following neonatal brain injury. Neurol Res Int 2012, 2012:257563.
22. Ikonomidou C., Turski L. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injuryα. Lancet Neurol 2002, 1:383-386.
23. Costantine M.M., Drever N. Antenatal exposure to magnesium sulfate and neuroprotection in preterm infants. Obstet Gynecol Clin North Am 2011, 38:351-366. xi.
24. Wilhelm W., Hammadeh M.E., White P.F., et al. General anesthesia versus monitored anesthesia care with remifentanil for assisted reproductive technologies: effect on pregnancy rate. J Clin Anesth 2002, 14:1-5.
25. Ma D., Lim T., Xu J., et al. Xenon preconditioning protects against renal ischemic-reperfusion injury via HIF-1alpha activation. J Am Soc Nephrol 2009, 20:713-720.
26. Yang T., Zhuang L., Rei Fidalgo A.M., et al. Xenon and sevoflurane provide analgesia during labor and fetal brain protection in a perinatal rat model of hypoxia-ischemia. PLoS One 2012, 7:e37020.
27. Thoresen M., Hobbs C.E., Wood T., et al. Cooling combined with immediate or delayed xenon inhalation provides equivalent long-term neuroprotection after neonatal hypoxia-ischemia. J Cereb Blood Flow Metab 2009, 29:707-714.
28. Palmer C., Towfighi J., Roberts R.L., et al. Allopurinol administered after inducing hypoxia-ischemia reduces brain injury in 7-day-old rats. Pediatr Res 1993, 33:405-411.
29. Benders M.J., Bos A.F., Rademaker C.M., et al. Early postnatal allopurinol does not improve short term outcome after severe birth asphyxia. Arch Dis Child Fetal Neonatal Ed 2006, 91:F163-F165.
30. Kaandorp J.J., Benders M.J., Rademaker C.M., et al. Antenatal allopurinol for reduction of birth asphyxia induced brain damage (ALLO-Trial); a randomized double blind placebo controlled multicenter study. BMC Pregnancy Childbirth 2010, 10:8.
31. Buonocore G., Groenendaal F. Anti-oxidant strategies. Semin Fetal Neonatal Med 2007, 12:287-295.
32. Yu L., Derrick M., Ji H., et al. Neuronal nitric oxide synthase inhibition prevents cerebral palsy following hypoxia-ischemia in fetal rabbits: comparison between JI-8 and 7-nitroindazole. Dev Neurosci 2011, 33:312-319.
33. Loren D.J., Seeram N.P., Schulman R.N., et al. Maternal dietary supplementation with pomegranate juice is neuroprotective in an animal model of neonatal hypoxic-ischemic brain injury. Pediatr Res 2005, 57:858-864.
34. West T., Atzeva M., Holtzman D.M. Pomegranate polyphenols and resveratrol protect the neonatal brain against hypoxic-ischemic injury. Dev Neurosci 2007, 29:363-372.
35. Zhang W., Hu X., Yang W., et al. Omega-3 polyunsaturated fatty acid supplementation confers long-term neuroprotection against neonatal hypoxic-ischemic brain injury through anti-inflammatory actions. Stroke 2010, 41:2341-2347.
36. Ramanantsoa N., Fleiss B., Bouslama M., et al. Bench to cribside: the path for developing a neuroprotectant. Translational Stroke Research 2013, 4:258-277.
37. Welin A.K., Svedin P., Lapatto R., et al. Melatonin reduces inflammation and cell death in white matter in the mid-gestation fetal sheep following umbilical cord occlusion. Pediatr Res 2007, 61:153-158.
38. Villapol S., Fau S., Renolleau S., et al. Melatonin promotes myelination by decreasing white matter inflammation after neonatal stroke. Pediatr Res 2011, 69:51-55.
39. Robertson N.J., Faulkner S., Fleiss B., et al. Melatonin augments hypothermic neuroprotection in a perinatal asphyxia model. Brain 2013, 136:90-105.
40. Yu X., Shacka J.J., Eells J.B., et al. Erythropoietin receptor signalling is required for normal brain development. Development 2002, 129:505-516.
41. Mazur M., Miller R.H., Robinson S. Postnatal erythropoietin treatment mitigates neural cell loss after systemic prenatal hypoxic-ischemic injury. J Neurosurg Pediatr 2010, 6:206-221.
42. Digicaylioglu M., Lipton S.A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 2001, 412:641-647.
43. Sun Y., Calvert J.W., Zhang J.H. Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke 2005, 36:1672-1678.
44. Juul S.E., Beyer R.P., Bammler T.K., et al. Microarray analysis of high-dose recombinant erythropoietin treatment of unilateral brain injury in neonatal mouse hippocampus. Pediatr Res 2009, 65:485-492.
45. Zacharias R., Schmidt M., Kny J., et al. Dose-dependent effects of erythropoietin in propofol anesthetized neonatal rats. Brain Res 2010, 1343:14-19.
46. Kumral A., Tugyan K., Gonenc S., et al. Protective effects of erythropoietin against ethanol-induced apoptotic neurodegeneration and oxidative stress in the developing C57BL/6 mouse brain. Brain Res Dev Brain Res 2005, 160:146-156.
47. Chattopadhyay A., Choudhury T.D., Bandyopadhyay D., et al. Protective effect of erythropoietin on the oxidative damage of erythrocyte membrane by hydroxyl radical. Biochem Pharmacol 2000, 59:419-425.
48. Iwai M., Cao G., Yin W., et al. Erythropoietin promotes neuronal replacement through revascularization and neurogenesis after neonatal hypoxia/ischemia in rats. Stroke 2007, 38:2795-2803.
49. Osredkar D., Sall J.W., Bickler P.E., et al. Erythropoietin promotes hippocampal neurogenesis in in vitro models of neonatal stroke. Neurobiol Dis 2010, 38:259-265.
50. Kellert B.A., McPherson R.J., Juul S.E. A comparison of high-dose recombinant erythropoietin treatment regimens in brain-injured neonatal rats. Pediatr Res 2007, 61:451-455.
51. Gonzalez F.F., Abel R., Almli C.R., et al. Erythropoietin sustains cognitive function and brain volume after neonatal stroke. Dev Neurosci 2009, 31:403-411.
52. Demers E.J., McPherson R.J., Juul S.E. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 2005, 58:297-301.
53. Iwai M., Stetler R.A., Xing J., et al. Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 2010, 41:1032-1037.
54. Reitmeir R., Kilic E., Kilic U., et al. Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity. Brain 2011, 134:84-99.
55. Juul S. Erythropoietin in anemia of prematurity. J Matern Fetal Neonatal Med 2012, 25:80-84.
56. van der Kooij M.A., Groenendaal F., Kavelaars A., et al. Neuroprotective properties and mechanisms of erythropoietin in in vitro and in vivo experimental models for hypoxia/ischemia. Brain Res Rev 2008, 59:22-33.
57. Juul S.E., McPherson R.J., Bauer L.A., et al. A phase I/II trial of high-dose erythropoietin in extremely low birth weight infants: pharmacokinetics and safety. Pediatrics 2008, 122:383-391.
58. Fauchere J.C., Dame C., Vonthein R., et al. An approach to using recombinant erythropoietin for neuroprotection in very preterm infants. Pediatrics 2008, 122:375-382.
59. Wu Y.W., Bauer L.A., Ballard R.A., et al. Erythropoietin for neuroprotection in neonatal encephalopathy: safety and pharmacokinetics. Pediatrics 2012, 130:683-691.
60. Almeida R.D., Manadas B.J., Melo C.V., et al. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 2005, 12:1329-1343.
61. Feng Y., Rhodes P.G., Bhatt A.J. Neuroprotective effects of vascular endothelial growth factor following hypoxic ischemic brain injury in neonatal rats. Pediatr Res 2008, 64:370-374.
62. Xiao B.G., Lu C.Z., Link H. Cell biology and clinical promise of G-CSF: immunomodulation and neuroprotection. J Cell Mol Med 2007, 11:1272-1290.
63. Fathali N., Lekic T., Zhang J.H., et al. Long-term evaluation of granulocyte-colony stimulating factor on hypoxic-ischemic brain damage in infant rats. Intensive Care Med 2010, 36:1602-1608.
64. Schabitz W.R., Laage R., Vogt G., et al. AXIS: a trial of intravenous granulocyte colony-stimulating factor in acute ischemic stroke. Stroke 2010, 41:2545-2551.
65. Popken G.J., Hodge R.D., Ye P., et al. In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur J Neurosci 2004, 19:2056-2068.
66. Kannan S., Dai H., Navath R.S., et al. Dendrimer-based postnatal therapy for neuroinflammation and cerebral palsy in a rabbit model. Sci Transl Med 2012, 4:130ra46.