Effects of combination therapy using hypothermia and erythropoietin in a rat model of neonatal hypoxia–ischemia

Jacobs S, Hunt R, Tarnow-Mordi W, Inder T, Davis P . Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev 2007:CD003311.

Gonzalez FF, Ferriero DM . Therapeutics for neonatal brain injury. Pharmacol Ther 2008;120:43–53.

Gluckman PD, Wyatt JS, Azzopardi D, et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 2005;365:663–70.

Shankaran S, Laptook AR, Ehrenkranz RA, et al. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med 2005;353:1574–84.

Azzopardi DV, Strohm B, Edwards AD, et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med 2009;361:1349–58.

Drury PP, Bennet L, Gunn AJ . Mechanisms of hypothermic neuroprotection. Semin Fetal Neonatal Med 2010;15:287–92.

Thoresen M, Penrice J, Lorek A, et al. Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr Res 1995;37:667–70.

Laptook AR, Corbett RJ, Sterett R, Burns DK, Tollefsbol G, Garcia D . Modest hypothermia provides partial neuroprotection for ischemic neonatal brain. Pediatr Res 1994;35(4 Pt 1):436–42.

Gunn AJ, Gunn TR, de Haan HH, Williams CE, Gluckman PD . Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J Clin Invest 1997;99:248–56.

Perlman JM, Wyllie J, Kattwinkel J, et al.; Neonatal Resuscitation Chapter Collaborators. Part 11: Neonatal resuscitation: 2010 International Consensus on Cardiopulmonary Resuscitation and Emergency Cardiovascular Care Science With Treatment Recommendations. Circulation 2010;122:16 Suppl 2:S516–38.

Chang YS, Mu D, Wendland M, et al. Erythropoietin improves functional and histological outcome in neonatal stroke. Pediatr Res 2005;58:106–11.

Gonzalez FF, McQuillen P, Mu D, et al. Erythropoietin enhances long-term neuroprotection and neurogenesis in neonatal stroke. Dev Neurosci 2007;29:321–30.

Gonzalez FF, Abel R, Almli CR, Mu D, Wendland M, Ferriero DM . Erythropoietin sustains cognitive function and brain volume after neonatal stroke. Dev Neurosci 2009;31:403–11.

Kumral A, Uysal N, Tugyan K, et al. Erythropoietin improves long-term spatial memory deficits and brain injury following neonatal hypoxia-ischemia in rats. Behav Brain Res 2004;153:77–86.

Sun Y, Calvert JW, Zhang JH . Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke 2005;36:1672–8.

Iwai M, Cao G, Yin W, Stetler RA, Liu J, Chen J . Erythropoietin promotes neuronal replacement through revascularization and neurogenesis after neonatal hypoxia/ischemia in rats. Stroke 2007;38:2795–803.

Xiong T, Qu Y, Mu D, Ferriero D . Erythropoietin for neonatal brain injury: opportunity and challenge. Int J Dev Neurosci 2011;29:583–91.

Elmahdy H, El-Mashad AR, El-Bahrawy H, El-Gohary T, El-Barbary A, Aly H . Human recombinant erythropoietin in asphyxia neonatorum: pilot trial. Pediatrics 2010;125:e1135–42.

Zhu C, Kang W, Xu F, et al. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics 2009;124:e218–26.

Lee BS, Woo CW, Kim ST, Kim KS . Long-term neuroprotective effect of postischemic hypothermia in a neonatal rat model of severe hypoxic ischemic encephalopathy: a comparative study on the duration and depth of hypothermia. Pediatr Res 2010;68:303–8.

Trescher WH, Ishiwa S, Johnston MV . Brief post-hypoxic-ischemic hypothermia markedly delays neonatal brain injury. Brain Dev 1997;19:326–38.

Covey MV, Oorschot DE . Effect of hypothermic post-treatment on hypoxic-ischemic striatal injury, and normal striatal development, in neonatal rats: a stereological study. Pediatr Res 2007;62:646–51.

Kellert, McPherson RJ, Juul SE . A comparison of high-dose recombinant Epo treatment regimens in brain-injured neonatal rats. Pediatr Res 2007;61:451–5.

Bona E, Hagberg H, Løberg EM, Bågenholm R, Thoresen M . Protective effects of moderate hypothermia after neonatal hypoxia-ischemia: short- and long-term outcome. Pediatr Res 1998;43:738–45.

Fan X, Heijnen CJ, van der KOOIJ MA, Groenendaal F, van Bel F . Beneficial effect of erythropoietin on sensorimotor function and white matter after hypoxia-ischemia in neonatal mice. Pediatr Res 2011;69:56–61.

Iwai M, Stetler RA, Xing J, et al. Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 2010;41:1032–7.

Demers EJ, McPherson RJ, Juul SE . Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 2005;58:297–301.

Chen H, Spagnoli F, Burris M, et al. Nanoerythropoietin is 10-times more effective than regular erythropoietin in neuroprotection in a neonatal rat model of hypoxia and ischemia. Stroke 2012;43:884–7.

Hagberg H, Ichord R, Palmer C, Yager JY, Vannucci SJ . Animal models of developmental brain injury: relevance to human disease. A summary of the panel discussion from the Third Hershey Conference on Developmental Cerebral Blood Flow and Metabolism. Dev Neurosci 2002;24:364–6.

Thoresen M, Bågenholm R, Løberg EM, Apricena F, Kjellmer I . Posthypoxic cooling of neonatal rats provides protection against brain injury. Arch Dis Child Fetal Neonatal Ed 1996;74:F3–9.

Zhu C, Wang X, Cheng X, et al. Post-ischemic hypothermia-induced tissue protection and diminished apoptosis after neonatal cerebral hypoxia-ischemia. Brain Res 2004;996:67–75.

Nedelcu J, Klein MA, Aguzzi A, Martin E . Resuscitative hypothermia protects the neonatal rat brain from hypoxic-ischemic injury. Brain Pathol 2000;10:61–71.

Thoresen M, Satas S, Løberg EM, et al. Twenty-four hours of mild hypothermia in unsedated newborn pigs starting after a severe global hypoxic-ischemic insult is not neuroprotective. Pediatr Res 2001;50:405–11.

Simbruner G, Mittal RA, Rohlmann F, Muche R . Systemic hypothermia after neonatal encephalopathy: outcomes of neo.nEURO.network RCT. Pediatrics 2010;126:e771–8.

Rice JE 3rd, Vannucci RC, Brierley JB . The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 1981;9:131–41.

Wen TC, Rogido M, Peng H, Genetta T, Moore J, Sola A . Gender differences in long-term beneficial effects of erythropoietin given after neonatal stroke in postnatal day-7 rats. Neuroscience 2006;139:803–11.

Hurn PD, Vannucci SJ, Hagberg H . Adult or perinatal brain injury: does sex matter? Stroke 2005;36:193–5.

Gonzalez FF, Fang A, Ferriero DM . Is erythropoietin the answer? Pediatr Res 2011;69:2–3.

Ferriero DM, Sheldon RA, Black SM, Chuai J . Selective destruction of nitric oxide synthase neurons with quisqualate reduces damage after hypoxia-ischemia in the neonatal rat. Pediatr Res 1995;38:912–8.