Abstract
Hypoxic-ischemic encephalopathy (HIE), a serious disease leading to neonatal death, is becoming a key area of pediatric neurological research. Despite remarkable advances in the understanding of HIE, the explicit pathogenesis of HIE is unclear, and well-established treatments are absent. Animal models are usually considered as the first step in the exploration of the underlying disease and in evaluating promising therapeutic interventions. Various animal models of HIE have been developed with distinct characteristics, and it is important to choose an appropriate animal model according to the experimental objectives. Generally, small animal models may be more suitable for exploring the mechanisms of HIE, whereas large animal models are better for translational studies. This review focuses on the features of commonly used HIE animal models with respect to their modeling strategies, merits, and shortcomings, and associated neuropathological changes, providing a comprehensive reference for improving existing animal models and developing new animal models.
Acknowledgments
This work was supported by the National Science Foundation of China (grant numbers 81330016 and 81270724), the Major State Basic Research Development Program (2013CB967404 and 2012BAl04B00), a grant from the Ministry of Education of China (IRT0935), grants from the Science and Technology Bureau of Sichuan province (2014SZ0149 and 2016TD0002), and a grant of the Clinical Discipline Program (Neonatology) from the Ministry of Health of China (1311200003303).
Conflict of interest statement: The authors declare that they have no conflict of interest.
References
Adamsons, K., Mueller-Heubach, E., and Myers, R.E. (1971). Production of fetal asphyxia in the rhesus monkey by administration of catecholamines to the mother. Am. J. Obstet. Gynecol. 109, 248–262.10.1016/0002-9378(71)90873-8Search in Google Scholar
Alonso-Alconada, D., Broad, K.D., Bainbridge, A., Chandrasekaran, M., Faulkner, S.D., Kerenyi, A., Hassell, J., Rocha-Ferreira, E., Hristova, M., Fleiss, B., et al. (2014). Brain cell death is reduced with cooling by 3.5°C to 5°C but increased with cooling by 8.5°C in a piglet asphyxia model. Stroke 46, 275–278.10.1161/STROKEAHA.114.007330Search in Google Scholar PubMed PubMed Central
Azzopardi, D. (2014). Predictive value of the amplitude integrated EEG in infants with hypoxic ischaemic encephalopathy: data from a randomised trial of therapeutic hypothermia. Arch. Dis. Child Fetal Neonatal Ed. 99, F80–F82.10.1136/archdischild-2013-303710Search in Google Scholar PubMed PubMed Central
Back, S.A. (2006). Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment. Retard Dev. Disabil. Res. Rev. 12, 129–140.10.1002/mrdd.20107Search in Google Scholar PubMed
Back, S.A., Riddle, A., and Hohimer, A.R. (2006). Role of instrumented fetal sheep preparations in defining the pathogenesis of human periventricular white-matter injury. J. Child Neurol. 21, 582–589.10.1177/08830738060210070101Search in Google Scholar PubMed
Back, S.A., Riddle, A., Dean, J., and Hohimer, A.R. (2012). The instrumented fetal sheep as a model of cerebral white matter injury in the premature infant. Neurotherapeutics 9, 359–370.10.1007/s13311-012-0108-ySearch in Google Scholar PubMed PubMed Central
Baud, O., Daire, J.L., Dalmaz, Y., Fontaine, R.H., Krueger, R.C., Sebag, G., Evrard, P., Gressens, P., and Verney, C. (2004). Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol. 14, 1–10.10.1111/j.1750-3639.2004.tb00492.xSearch in Google Scholar PubMed PubMed Central
Beckstrom, A.C., Humston, E.M., Snyder, L.R., Synovec, R.E., and Juul, S.E. (2011). Application of comprehensive two-dimensional gas chromatography with time-of-flight mass spectrometry method to identify potential biomarkers of perinatal asphyxia in a non-human primate model. J. Chromatogr. A 1218, 1899–1906.10.1016/j.chroma.2011.01.086Search in Google Scholar PubMed PubMed Central
Benjelloun, N., Renolleau, S., Represa, A., Ben-Ari, Y., and Charriaut-Marlangue, C. (1999). Inflammatory responses in the cerebral cortex after ischemia in the P7 neonatal Rat. Stroke 30, 1916–1923, 1923–1924.10.1161/01.STR.30.9.1916Search in Google Scholar PubMed
Björkman, S.T., Foster, K.A., O’Driscoll, S.M., Healy, G.N., Lingwood, B.E., Burke, C., and Colditz, P.B. (2006). Hypoxic/Ischemic models in newborn piglet: comparison of constant FiO2 versus variable FiO2 delivery. Brain Res. 1100, 110–117.10.1016/j.brainres.2006.04.119Search in Google Scholar PubMed
Boksa, P. (2010). Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24, 881–897.10.1016/j.bbi.2010.03.005Search in Google Scholar PubMed
Brann, A.J. and Myers, R.E. (1975). Central nervous system findings in the newborn monkey following severe in utero partial asphyxia. Neurology 25, 327–338.10.1212/WNL.25.4.327Search in Google Scholar
Brew, N., Azhan, A., den Heijer, I., Boomgardt, M., Davies, G.I., Nitsos, I., Miller, S.L., Walker, A.M., Walker, D.W., and Wong, F.Y. (2016). Dopamine treatment during acute hypoxia is neuroprotective in the developing sheep brain. Neuroscience 316, 82–93.10.1016/j.neuroscience.2015.12.022Search in Google Scholar PubMed
Broad, K.D., Fierens, I., Fleiss, B., Rocha-Ferreira, E., Ezzati, M., Hassell, J., Alonso-Alconada, D., Bainbridge, A., Kawano, G., Ma, D., et al. (2016). Inhaled 45–50% argon augments hypothermic brain protection in a piglet model of perinatal asphyxia. Neurobiol. Dis. 87, 29–38.10.1016/j.nbd.2015.12.001Search in Google Scholar PubMed PubMed Central
Buono, K.D., Goodus, M.T., Guardia, C.M., Jiang, Y., Loporchio, D., and Levison, S.W. (2015). Mechanisms of mouse neural precursor expansion after neonatal hypoxia-ischemia. J. Neurosci. 35, 8855–8865.10.1523/JNEUROSCI.2868-12.2015Search in Google Scholar PubMed PubMed Central
Buser, J.R., Segovia, K.N., Dean, J.M., Nelson, K., Beardsley, D., Gong, X., Luo, N.L., Ren, J., Wan, Y., Riddle, A., et al. (2010). Timing of appearance of late oligodendrocyte progenitors coincides with enhanced susceptibility of preterm rabbit cerebral white matter to hypoxia-ischemia. J. Cereb. Blood Flow Metab. 30, 1053–1065.10.1038/jcbfm.2009.286Search in Google Scholar PubMed PubMed Central
Cai, Z., Pan, Z.L., Pang, Y., Evans, O.B., and Rhodes, P.G. (2000). Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47, 64–72.10.1203/00006450-200001000-00013Search in Google Scholar PubMed
Castillo-Melendez, M., Baburamani, A.A., Cabalag, C., Yawno, T., Witjaksono, A., Miller, S. L., and Walker, D.W. (2013). Experimental modelling of the consequences of brief late gestation asphyxia on newborn lamb behaviour and brain structure. PLoS One 8, e77377.10.1371/journal.pone.0077377Search in Google Scholar PubMed PubMed Central
Chen, C.Y., Sun, W.Z., Kang, K.H., Chou, H.C., Tsao, P.N., Hsieh, W.S., and Fu, W.M. (2015). Hypoxic preconditioning suppresses glial activation and neuroinflammation in neonatal brain insults. Mediators Inflamm. 2015, 632592.10.1155/2015/632592Search in Google Scholar PubMed PubMed Central
Cheng, T., Xue, X., and Fu, J. (2015). Effect of OLIG1 on the development of oligodendrocytes and myelination in a neonatal rat PVL model induced by hypoxia-ischemia. Mol. Med. Rep. 11, 2379–2386.10.3892/mmr.2014.3028Search in Google Scholar PubMed PubMed Central
Cheung, P.Y., Gill, R.S., and Bigam, D.L. (2011). A swine model of neonatal asphyxia. J. Vis. Exp. 11, pii: 3166.10.3791/3166Search in Google Scholar
Coalson, J.J., Winter, V.T., Siler-Khodr, T., and Yoder, B.A. (1999). Neonatal chronic lung disease in extremely immature baboons. Am. J. Respir. Crit. Care Med. 160, 1333–1346.10.1164/ajrccm.160.4.9810071Search in Google Scholar
Craig, A., Ling, L.N., Beardsley, D.J., Wingate-Pearse, N., Walker, D.W., Hohimer, A.R., and Back, S.A. (2003). Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp. Neurol. 181, 231–240.10.1016/S0014-4886(03)00032-3Search in Google Scholar
D’Arceuil, H.E., de Crespigny, A.J., Rother, J., Seri, S., Moseley, M.E., Stevenson, D.K., and Rhine, W. (1998).Diffusion and perfusion magnetic resonance imaging of the evolution of hypoxic ischemic encephalopathy in the neonatal rabbit. J. Magn. Reson. Imaging 8, 820–828.10.1002/jmri.1880080411Search in Google Scholar PubMed
Dean, J.M., Farrag, D., Zahkouk, S.A., El, Z.E., Hagberg, H., Kjellmer, I., and Mallard, C. (2009). Cerebellar white matter injury following systemic endotoxemia in preterm fetal sheep. Neuroscience 160, 606–615.10.1016/j.neuroscience.2009.02.071Search in Google Scholar PubMed
Dean, J.M., Moravec, M.D., Grafe, M., Abend, N., Ren, J., Gong, X., Volpe, J.J., Jensen, F.E., Hohimer, A.R., and Back, S.A. (2011a). Strain-specific differences in perinatal rodent oligodendrocyte lineage progression and its correlation with human. Dev. Neurosci. 33, 251–260.10.1159/000327242Search in Google Scholar PubMed PubMed Central
Dean, J.M., van de Looij, Y., Sizonenko, S.V., Lodygensky, G.A., Lazeyras, F., Bolouri, H., Kjellmer, I., Huppi, P.S., Hagberg, H., and Mallard, C. (2011b). Delayed cortical impairment following lipopolysaccharide exposure in preterm fetal sheep. Ann. Neurol. 70, 846–856.10.1002/ana.22480Search in Google Scholar PubMed
Derrick, M. (2004). Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy? J. Neurosci. 24, 24–34.10.1523/JNEUROSCI.2816-03.2004Search in Google Scholar PubMed PubMed Central
Derrick, M., Drobyshevsky, A., Ji, X., and Tan, S. (2007). A model of cerebral palsy from fetal hypoxia-ischemia. Stroke 38, 731–735.10.1161/01.STR.0000251445.94697.64Search in Google Scholar PubMed
Dickerson, J.W. and Dobbing, J. (1967). Prenatal and postnatal growth and development of the central nervous system of the pig. Proc. R Soc. Lond. B Biol. Sci. 166, 384–395.10.1098/rspb.1967.0002Search in Google Scholar PubMed
Dixon, B.J., Reis, C., Ho, W.M., Tang, J., and Zhang, J.H. (2015). Neuroprotective strategies after neonatal hypoxic ischemic encephalopathy. Int. J. Mol. Sci. 16, 22368–22401.10.3390/ijms160922368Search in Google Scholar
Drobyshevsky, A., Derrick, M., Wyrwicz, A.M., Ji, X., Englof, I., Ullman, L.M., Zelaya, M.E., Northington, F.J., and Tan, S. (2007). White matter injury correlates with hypertonia in an animal model of cerebral palsy. J. Cereb. Blood Flow Metab. 27, 270–281.10.1038/sj.jcbfm.9600333Search in Google Scholar
Drobyshevsky, A., Derrick, M., Luo, K., Zhang, L.Q., Wu, Y.N., Takada, S.H., Yu, L., and Tan, S. (2012). Near-term fetal hypoxia-ischemia in rabbits: MRI can predict muscle tone abnormalities and deep brain injury. Stroke 43, 2757–2763.10.1161/STROKEAHA.112.653857Search in Google Scholar
Drury, P.P., Davidson, J.O., Bennet, L., Booth, L.C., Tan, S., Fraser, M., van den Heuij, L.G., and Gunn, A.J. (2014). Partial neural protection with prophylactic low-dose melatonin after asphyxia in preterm fetal sheep. J. Cereb. Blood Flow Metab. 34, 126–135.10.1038/jcbfm.2013.174Search in Google Scholar
Duncan, J.R., Cock, M.L., Scheerlinck, J.P., Westcott, K.T., McLean, C., Harding, R., and Rees, S.M. (2002). White matter injury after repeated endotoxin exposure in the preterm ovine fetus. Pediatr. Res. 52, 941–949.10.1203/00006450-200212000-00021Search in Google Scholar
Favrais, G., van de Looij, Y., Fleiss, B., Ramanantsoa, N., Bonnin, P., Stoltenburg-Didinger, G., Lacaud, A., Saliba, E., Dammann, O., Gallego, J., et al. (2011). Systemic inflammation disrupts the developmental program of white matter. Ann. Neurol. 70, 550–565.10.1002/ana.22489Search in Google Scholar
Foster, K.A., Colditz, P.B., Lingwood, B.E., Burke, C., Dunster, K.R., and Roberts, M.S. (2001). An improved survival model of hypoxia/ischaemia in the piglet suitable for neuroprotection studies. Brain Res. 919, 122–131.10.1016/S0006-8993(01)03011-6Search in Google Scholar
Gonzales-Portillo, G.S., Reyes, S., Aguirre, D., Pabon, M.M., and Borlongan, C.V. (2014). Stem cell therapy for neonatal hypoxic-ischemic encephalopathy. Front Neurol. 5, 147.10.3389/fneur.2014.00147Search in Google Scholar
Goto, M., Yoshioka, T., Ravindranath, T., Battelino, T., Young, R.I., and Zeller, W.P. (1994). LPS injected into the pregnant rat late in gestation does not induce fetal endotoxemia. Res. Commun. Mol. Pathol. Pharmacol. 85, 109–112.Search in Google Scholar
Guerguerian, A.M., Brambrink, A.M., Traystman, R.J., Huganir, R.L., and Martin, L.J. (2002). Altered expression and phosphorylation of N-methyl-d-aspartate receptors in piglet striatum after hypoxia-ischemia. Brain Res. Mol. Brain Res. 104, 66–80.10.1016/S0169-328X(02)00285-1Search in Google Scholar
Guillet, R., Edwards, A.D., Thoresen, M., Ferriero, D.M., Gluckman, P.D., Whitelaw, A., and Gunn, A.J. (2012). Seven- to eight-year follow-up of the CoolCap trial of head cooling for neonatal encephalopathy. Pediatr. Res. 71, 205–209.10.1038/pr.2011.30Search in Google Scholar PubMed
Gunn, A.J., Parer, J.T., Mallard, E.C., Williams, C.E., and Gluckman, P.D. (1992). Cerebral histologic and electrocorticographic changes after asphyxia in fetal sheep. Pediatr. Res. 31, 486–491.10.1203/00006450-199205000-00016Search in Google Scholar PubMed
Haaland, K., Loberg, E.M., Steen, P.A., and Thoresen, M. (1997). Posthypoxic hypothermia in newborn piglets. Pediatr. Res. 41, 505–512.10.1203/00006450-199704000-00009Search in Google Scholar PubMed
Hattori, T., Sato, Y., Kondo, T., Ichinohashi, Y., Sugiyama, Y., Yamamoto, M., Kotani, T., Hirata, H., Hirakawa, A., Suzuki, S., et al. (2015). Administration of umbilical cord blood cells transiently decreased hypoxic-ischemic brain injury in neonatal rats. Dev. Neurosci. 37, 95–104.10.1159/000368396Search in Google Scholar PubMed
Herzog, M., Cerar, L.K., Srsen, T.P., Verdenik, I., and Lucovnik, M. (2015). Impact of risk factors other than prematurity on periventricular leukomalacia. A population-based matched case control study. Eur. J. Obstet. Gynecol. Reprod. Biol. 187, 57–59.10.1016/j.ejogrb.2015.02.008Search in Google Scholar PubMed
Hill, C.A. and Fitch, R.H. (2012). Sex differences in mechanisms and outcome of neonatal hypoxia-ischemia in rodent models: implications for sex-specific neuroprotection in clinical neonatal practice. Neurol. Res. Int. 2012, 867531.10.1155/2012/867531Search in Google Scholar PubMed PubMed Central
Hill, C.A., Threlkeld, S.W., and Fitch, R.H. (2011). Early testosterone modulated sex differences in behavioral outcome following neonatal hypoxia ischemia in rats. Int. J. Dev. Neurosci. 29, 381–388.10.1016/j.ijdevneu.2011.03.005Search in Google Scholar PubMed PubMed Central
Inder, T., Neil, J., Yoder, B., and Rees, S. (2004). Non-human primate models of neonatal brain injury. Semin. Perinatol. 28, 396–404.10.1053/j.semperi.2004.10.002Search in Google Scholar PubMed
Inder, T., Neil, J., Yoder, B., and Rees, S. (2005). Patterns of cerebral injury in a primate model of preterm birth and neonatal intensive care. J. Child Neurol. 20, 965–967.10.1177/08830738050200120601Search in Google Scholar PubMed
Jacobs, S.E., Berg, M., Hunt, R., Tarnow-Mordi, W.O., Inder, T.E., and Davis, P.G. (2013).Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst. Rev. 1, D3311.10.1002/14651858.CD003311.pub3Search in Google Scholar PubMed PubMed Central
Jin, S.J., Liu, Y., Deng, S.H., Liao, L.H., Lin, T.L., Ning, Q., and Luo, X.P. (2015). Neuroprotective effects of activated protein C on intrauterine inflammation-induced neonatal white matter injury are associated with the downregulation of fibrinogen-like protein 2/fibroleukin prothrombinase and the inhibition of pro-inflammatory cytokine expression. Int. J. Mol. Med. 35, 1199–1212.10.3892/ijmm.2015.2136Search in Google Scholar PubMed PubMed Central
Juul, S.E., Aylward, E., Richards, T., McPherson, R.J., Kuratani, J., and Burbacher, T.M. (2007). Prenatal cord clamping in newborn Macaca nemestrina: a model of perinatal asphyxia. Dev. Neurosci. 29, 311–320.10.1159/000105472Search in Google Scholar PubMed
Keogh, M.J., Drury, P.P., Bennet, L., Davidson, J.O., Mathai, S., Gunn, E.R., Booth, L.C., and Gunn, A.J. (2012). Limited predictive value of early changes in EEG spectral power for neural injury after asphyxia in preterm fetal sheep. Pediatr. Res. 71, 345–353.10.1038/pr.2011.80Search in Google Scholar PubMed
Kohlhauer, M., Lidouren, F., Remy-Jouet, I., Mongardon, N., Adam, C., Bruneval, P., Hocini, H., Levy, Y., Blengio, F., Carli, P., et al. (2015). Hypothermic total liquid ventilation is highly protective through cerebral hemodynamic preservation and sepsis-like mitigation after asphyxial cardiac arrest. Crit. Care Med. 43, e420–e430.10.1097/CCM.0000000000001160Search in Google Scholar PubMed
Kumral, A., Baskin, H., Yesilirmak, D.C., Ergur, B.U., Aykan, S., Genc, S., Genc, K., Yilmaz, O., Tugyan, K., Giray, O., et al. (2007). Erythropoietin attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain. Neonatology 92, 269–278.10.1159/000105493Search in Google Scholar PubMed
Kurinczuk, J.J., White-Koning, M., and Badawi, N. (2010). Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum. Dev. 86, 329–338.10.1016/j.earlhumdev.2010.05.010Search in Google Scholar PubMed
Kyng, K.J., Skajaa, T., Kerrn-Jespersen, S., Andreassen, C.S., Bennedsgaard, K., and Henriksen, T.B. (2015). A piglet model of neonatal hypoxic-ischemic encephalopathy. J. Vis Exp. 16, e52454.10.3791/52454Search in Google Scholar PubMed PubMed Central
Kyu, H.H., Pinho, C., Wagner, J.A., Brown, J.C., Bertozzi-Villa, A., Charlson, F.J., Coffeng, L.E., Dandona, L., Erskine, H.E., Ferrari, A.J., et al. (2016). Global and national burden of diseases and injuries among children and adolescents between 1990 and 2013: findings from the Global Burden of Disease 2013 Study. JAMA Pediatr. 170, 267–287.10.1001/jamapediatrics.2015.4276Search in Google Scholar PubMed PubMed Central
Larson, A.C., Jamrogowicz, J.L., Kulikowicz, E., Wang, B., Yang, Z.J., Shaffner, D.H., Koehler, R.C., and Lee, J.K. (2013). Cerebrovascular autoregulation after rewarming from hypothermia in a neonatal swine model of asphyxic brain injury. J. Appl. Physiol. 115, 1433–1442.10.1152/japplphysiol.00238.2013Search in Google Scholar PubMed PubMed Central
Li, L., Xiong, Y., Qu, Y., Mao, M., Mu, W., Wang, H., and Mu, D. (2008). The requirement of extracellular signal-related protein kinase pathway in the activation of hypoxia inducible factor 1α in the developing rat brain after hypoxia-ischemia. Acta Neuropathol. 115, 297–303.10.1007/s00401-008-0339-5Search in Google Scholar PubMed
Mallard, E.C., Williams, C.E., Gunn, A.J., Gunning, M.I., and Gluckman, P.D. (1993). Frequent episodes of brief ischemia sensitize the fetal sheep brain to neuronal loss and induce striatal injury. Pediatr. Res. 33, 61–65.10.1203/00006450-199301000-00013Search in Google Scholar PubMed
Mallard, C., Welin, A.K., Peebles, D., Hagberg, H., and Kjellmer, I. (2003). White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem. Res. 28, 215–223.10.1023/A:1022368915400Search in Google Scholar
Manabat, C., Han, B.H., Wendland, M., Derugin, N., Fox, C.K., Choi, J., Holtzman, D.M., Ferriero, D.M., and Vexler, Z.S. (2003). Reperfusion differentially induces caspase-3 activation in ischemic core and penumbra after stroke in immature brain. Stroke 34, 207–213.10.1161/01.STR.0000047101.87575.3CSearch in Google Scholar
Mao, F.X., Li, W.J., Chen, H.J., Qian, L.H., and Buzby, J.S. (2012). Periventricular leukomalacia long-term prognosis may be improved by treatment with UDP-glucose, GDNF, and memantine in neonatal rats. Brain Res. 1486, 112–120.10.1016/j.brainres.2012.09.033Search in Google Scholar
Mao, F.X., Li, W.J., Chen, H.J., Qian, L.H., and Buzby, J.S. (2013). White matter and SVZ serve as endogenous sources of glial progenitor cells for self-repair in neonatal rats with ischemic PVL. Brain Res. 1535, 38–51.10.1016/j.brainres.2013.08.006Search in Google Scholar
Martin, L.J., Brambrink, A., Koehler, R.C., and Traystman, R.J. (1997). Primary sensory and forebrain motor systems in the newborn brain are preferentially damaged by hypoxia-ischemia. J. Comp. Neurol. 377, 262–285.10.1002/(SICI)1096-9861(19970113)377:2<262::AID-CNE8>3.0.CO;2-1Search in Google Scholar
Mirza, M.A., Ritzel, R., Xu, Y., McCullough, L.D., and Liu, F. (2015). Sexually dimorphic outcomes and inflammatory responses in hypoxic-ischemic encephalopathy. J. Neuroinflammation 12, 32.10.1186/s12974-015-0251-6Search in Google Scholar
Myers, R.E. (1969). Atrophic cortical sclerosis associated with status marmoratus in a perinatally damaged monkey. Neurology 19, 1177–1188.10.1212/WNL.19.12.1177Search in Google Scholar
Myers, R.E. (1972). Two patterns of perinatal brain damage and their conditions of occurrence. Am. J. Obstet. Gynecol. 112, 246–276.10.1016/0002-9378(72)90124-XSearch in Google Scholar
Ni, X., Yang, Z., Carter, E.L., Martin, L.J., and Koehler, R.C. (2011). Striatal neuroprotection from neonatal hypoxia-ischemia in piglets by antioxidant treatment with EUK-134 or edaravone. Dev. Neurosci. 33, 299–311.10.1159/000327243Search in Google Scholar
Ni, X., Yang, Z., Wang, B., Carter, E.L., Larson, A.C., Martin, L.J., and Koehler, R.C. (2012). Early antioxidant treatment and delayed hypothermia after hypoxia–ischemia have no additive neuroprotection in newborn pigs. Anesth. Analg. 115, 627–637.10.1213/ANE.0b013e31825d3600Search in Google Scholar
Nitsos, I., Rees, S.M., Duncan, J., Kramer, B.W., Harding, R., Newnham, J.P., and Moss, T.J. (2006). Chronic exposure to intra-amniotic lipopolysaccharide affects the ovine fetal brain. J. Soc. Gynecol. Invest. 13, 239–247.10.1016/j.jsgi.2006.02.011Search in Google Scholar
Nitsos, I., Newnham, J.P., Rees, S.M., Harding, R., and Moss, T.J.M. (2014). The impact of chronic intrauterine inflammation on the physiologic and neurodevelopmental consequences of intermittent umbilical cord occlusion in fetal sheep. Reprod. Sci. 21, 658–670.10.1177/1933719111399928Search in Google Scholar
O’Shea, T.M., Shah, B., Allred, E.N., Fichorova, R.N., Kuban, K.C., Dammann, O., and Leviton, A. (2013). Inflammation-initiating illnesses, inflammation-related proteins, and cognitive impairment in extremely preterm infants. Brain Behav. Immun. 29, 104–112.10.1016/j.bbi.2012.12.012Search in Google Scholar
Painter, M.J. (1995).Animal models of perinatal asphyxia: contributions, contradictions, clinical relevance. Semin. Pediatr. Neurol. 2, 37–56.10.1016/S1071-9091(05)80004-XSearch in Google Scholar
Pimentel-Coelho, P.M., Michaud, J.P., and Rivest, S. (2015). C-C chemokine receptor type 2 (CCR2) signaling protects neonatal male mice with hypoxic-ischemic hippocampal damage from developing spatial learning deficits. Behav. Brain Res. 286, 146–151.10.1016/j.bbr.2015.02.053Search in Google Scholar PubMed
Recker, R., Adami, A., Tone, B., Tian, H.R., Lalas, S., Hartman, R.E., Obenaus, A., and Ashwal, S. (2009). Rodent neonatal bilateral carotid artery occlusion with hypoxia mimics human hypoxic-ischemic injury. J. Cereb. Blood Flow Metab. 29, 1305–1316.10.1038/jcbfm.2009.56Search in Google Scholar PubMed
Renolleau, S., Aggoun-Zouaoui, D., Ben-Ari, Y., and Charriaut-Marlangue, C. (1998). A model of transient unilateral focal ischemia with reperfusion in the P7 neonatal rat: morphological changes indicative of apoptosis. Stroke 29, 1454–1460, 1461.10.1161/01.STR.29.7.1454Search in Google Scholar
Rice, J.R., Vannucci, R.C., and Brierley, J.B. (1981). The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9, 131–141.10.1002/ana.410090206Search in Google Scholar PubMed
Robertson, N.J., Faulkner, S., Fleiss, B., Bainbridge, A., Andorka, C., Price, D., Powell, E., Lecky-Thompson, L., Thei, L., Chandrasekaran, M., et al. (2013). Melatonin augments hypothermic neuroprotection in a perinatal asphyxia model. Brain 136, 90–105.10.1093/brain/aws285Search in Google Scholar PubMed
Rocha-Ferreira, E., Phillips, E., Francesch-Domenech, E., Thei, L., Peebles, D.M., Raivich, G., and Hristova, M. (2015). The role of different strain backgrounds in bacterial endotoxin-mediated sensitization to neonatal hypoxic-ischemic brain damage. Neuroscience 311, 292–307.10.1016/j.neuroscience.2015.10.035Search in Google Scholar PubMed PubMed Central
Roohey, T., Raju, T.N., and Moustogiannis, A.N. (1997). Animal models for the study of perinatal hypoxic-ischemic encephalopathy: a critical analysis. Early Hum. Dev. 47, 115–146.10.1016/S0378-3782(96)01773-2Search in Google Scholar
Schwartz, P.H., Massarweh, W.F., Vinters, H.V., and Wasterlain, C.G. (1992). A rat model of severe neonatal hypoxic-ischemic brain injury. Stroke 23, 539–546.10.1161/01.STR.23.4.539Search in Google Scholar
Selway, L.D. (2010). State of the science: hypoxic ischemic encephalopathy and hypothermic intervention for neonates. Adv. Neonatal Care 10, 60–66, 67–68.10.1097/ANC.0b013e3181d54b30Search in Google Scholar PubMed
Shalak, L.F., Laptook, A.R., Jafri, H.S., Ramilo, O., and Perlman, J.M. (2002). Clinical chorioamnionitis, elevated cytokines, and brain injury in term infants. Pediatrics 110, 673–680.10.1542/peds.110.4.673Search in Google Scholar PubMed
Shankaran, S., Laptook, A.R., Ehrenkranz, R.A., Tyson, J.E., McDonald, S.A., Donovan, E.F., Fanaroff, A.A., Poole, W.K., Wright, L.L., Higgins, R.D., et al. (2005). Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 353, 1574–1584.10.1056/NEJMcps050929Search in Google Scholar PubMed
Shen, Y., Plane, J.M., and Deng, W. (2010). Mouse models of periventricular leukomalacia. J. Vis. Exp.10.3791/1951Search in Google Scholar PubMed PubMed Central
Smith, A.L., Alexander, M., Rosenkrantz, T.S., Sadek, M.L., and Fitch, R.H. (2014). Sex differences in behavioral outcome following neonatal hypoxia ischemia: insights from a clinical meta-analysis and a rodent model of induced hypoxic ischemic brain injury. Exp. Neurol. 254, 54–67.10.1016/j.expneurol.2014.01.003Search in Google Scholar PubMed
Smith, A.L., Garbus, H., Rosenkrantz, T.S., and Fitch, R.H. (2015). Sex differences in behavioral outcomes following temperature modulation during induced neonatal hypoxic ischemic injury in rats. Brain Sci. 5, 220–240.10.3390/brainsci5020220Search in Google Scholar PubMed PubMed Central
Spinillo, A., Capuzzo, E., Stronati, M., Ometto, A., De Santolo, A., and Acciano, S. (1998). Obstetric risk factors for periventricular leukomalacia among preterm infants. Br. J. Obstet. Gynaecol. 105, 865–871.10.1111/j.1471-0528.1998.tb10231.xSearch in Google Scholar PubMed
Tan, S., Zhou, F., Nielsen, V.G., Wang, Z., Gladson, C.L., Parks, D.A. (1999). Increased injury following intermittent fetal hypoxia-reoxygenation is associated with increased free radical production in fetal rabbit brain. J. Neuropathol. Exp. Neurol. 58, 972–981.10.1097/00005072-199909000-00007Search in Google Scholar PubMed
Ten, V.S., Bradley-Moore, M., Gingrich, J.A., Stark, R.I., and Pinsky, D.J. (2003). Brain injury and neurofunctional deficit in neonatal mice with hypoxic-ischemic encephalopathy. Behav. Brain Res. 145, 209–219.10.1016/S0166-4328(03)00146-3Search in Google Scholar
Thatipamula, S., Al, R.M., Zhang, J., and Hossain, M.A. (2015). Genetic deletion of neuronal pentraxin 1 expression prevents brain injury in a neonatal mouse model of cerebral hypoxia-ischemia. Neurobiol. Dis. 75, 15–30.10.1016/j.nbd.2014.12.016Search in Google Scholar
Uehara, H., Yoshioka, H., Kawase, S., Nagai, H., Ohmae, T., Hasegawa, K., and Sawada, T. (1999). A new model of white matter injury in neonatal rats with bilateral carotid artery occlusion. Brain Res. 837, 213–220.10.1016/S0006-8993(99)01675-3Search in Google Scholar
Vannucci, R.C., and Vannucci, S.J. (2005). Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Dev. Neurosci. 27, 81–86.10.1159/000085978Search in Google Scholar PubMed
Volpe, J.J., Kinney, H.C., Jensen, F.E., and Rosenberg, P.A. (2011). The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int. J. Dev. Neurosci. 29, 423–440.10.1016/j.ijdevneu.2011.02.012Search in Google Scholar PubMed PubMed Central
Wang, X., Stridh, L., Li, W., Dean, J., Elmgren, A., Gan, L., Eriksson, K., Hagberg, H., and Mallard, C. (2009). Lipopolysaccharide sensitizes neonatal hypoxic-ischemic brain injury in a MyD88-dependent manner. J. Immunol. 183, 7471–7477.10.4049/jimmunol.0900762Search in Google Scholar PubMed
Wang, L., Chang, Y., Lin, C., Hong, J., and Huang, C. (2010). Low-dose lipopolysaccharide selectively sensitizes hypoxic ischemia-induced white matter injury in the immature brain. Pediatr. Res. 68, 41–47.10.1203/PDR.0b013e3181df5f6bSearch in Google Scholar PubMed PubMed Central
Wang, L.Y., Tu, Y.F., Lin, Y.C., and Huang, C.C. (2016). CXCL5 signaling is a shared pathway of neuroinflammation and blood-brain barrier injury contributing to white matter injury in the immature brain. J. Neuroinflammation 13, 6.10.1186/s12974-015-0474-6Search in Google Scholar PubMed PubMed Central
Wei, Z.Z., Gu, X., Ferdinand, A., Lee, J.H., Ji, X., Ji, X.M., Yu, S.P., and Wei, L. (2015). Intranasal delivery of bone marrow mesenchymal stem cells improved neurovascular regeneration and rescued neuropsychiatric deficits after neonatal stroke in rats. Cell Transplant 24, 391–402.10.3727/096368915X686887Search in Google Scholar PubMed
Welin, A.K., Sandberg, M., Lindblom, A., Arvidsson, P., Nilsson, U.A., Kjellmer, I., and Mallard, C. (2005). White matter injury following prolonged free radical formation in the 0.65 gestation fetal sheep brain. Pediatr. Res. 58, 100–105.10.1203/01.PDR.0000163388.04017.26Search in Google Scholar PubMed
Wen, T.C., Rogido, M., Peng, H., Genetta, T., Moore, J., and Sola, A. (2006). Gender differences in long-term beneficial effects of erythropoietin given after neonatal stroke in postnatal day-7 rats. Neuroscience 139, 803–811.10.1016/j.neuroscience.2006.02.057Search in Google Scholar
WHO. Newborns: reducing mortality, 2016. Available at http://www.who.int/mediacentre/factsheets/fs333/en/.Search in Google Scholar
Xie, C., Ginet, V., Sun, Y., Koike, M., Zhou, K., Li, T., Li, H., Li, Q., Wang, X., Uchiyama, Y., et al. (2016). Neuroprotection by selective neuronal deletion of Atg7 in neonatal brain injury. Autophagy 12, 410–423.10.1080/15548627.2015.1132134Search in Google Scholar
Yager, J.Y., and Ashwal, S. (2009). Animal models of perinatal hypoxic-ischemic brain damage. Pediatr. Neurol. 40, 156–167.10.1016/j.pediatrneurol.2008.10.025Search in Google Scholar
Yang, S.H., Perez, E., Cutright, J., Liu, R., He, Z., Day, A.L., and Simpkins, J.W. (2002). Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model. J. Appl. Physiol. (1985) 92, 195–201.10.1152/jappl.2002.92.1.195Search in Google Scholar
Yoder, B., Martin, H., McCurnin, D.C., and Coalson, J.J. (2002). Impaired urinary cortisol excretion and early cardiopulmonary dysfunction in immature baboons. Pediatr. Res. 51, 426–432.10.1203/00006450-200204000-00006Search in Google Scholar
Yoon, B.H., Kim, C.J., Romero, R., Jun, J.K., Park, K.H., Choi, S.T., and Chi, J.G. (1997). Experimentally induced intrauterine infection causes fetal brain white matter lesions in rabbits. Am. J. Obstet. Gynecol. 177, 797–802.10.1016/S0002-9378(97)70271-0Search in Google Scholar
Yu, L., Derrick, M., Ji, H., Silverman, R.B., Whitsett, J., Vasquez-Vivar, J., and Tan, S. (2011). Neuronal nitric oxide synthase inhibition prevents cerebral palsy following hypoxia-ischemia in fetal rabbits: comparison between JI-8 and 7-nitroindazole. Dev. Neurosci. 33, 312–319.10.1159/000327244Search in Google Scholar PubMed PubMed Central
Zhou, Y., Fathali, N., Lekic, T., Ostrowski, R.P., Chen, C., Martin, R.D., Tang, J., and Zhang, J.H. (2011). Remote limb ischemic postconditioning protects against neonatal hypoxic-ischemic brain injury in rat pups by the opioid receptor/Akt pathway. Stroke 42, 439–444.10.1161/STROKEAHA.110.592162Search in Google Scholar PubMed PubMed Central
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Articles in the same Issue
- Frontmatter
- Effect of acute stress on auditory processing: a systematic review of human studies
- Experimental spinal cord trauma: a review of mechanically induced spinal cord injury in rat models
- Brain metabolic DNA in memory processing and genome turnover
- Animal models of hypoxic-ischemic encephalopathy: optimal choices for the best outcomes
- Highway to thermosensation: a traced review, from the proteins to the brain
- Complex effects of apoplexy secondary to pituitary adenoma
- Regenerative peripheral neuropathic pain: novel pathological pain, new therapeutic dimension
- Possible role of biochemiluminescent photons for lysergic acid diethylamide (LSD)-induced phosphenes and visual hallucinations
- Therapeutic potential of flavonoids in spinal cord injury
- Is daily replication necessary when sampling cortisol concentrations in association studies of children with autism spectrum disorder? A systematic review and discussion paper
Articles in the same Issue
- Frontmatter
- Effect of acute stress on auditory processing: a systematic review of human studies
- Experimental spinal cord trauma: a review of mechanically induced spinal cord injury in rat models
- Brain metabolic DNA in memory processing and genome turnover
- Animal models of hypoxic-ischemic encephalopathy: optimal choices for the best outcomes
- Highway to thermosensation: a traced review, from the proteins to the brain
- Complex effects of apoplexy secondary to pituitary adenoma
- Regenerative peripheral neuropathic pain: novel pathological pain, new therapeutic dimension
- Possible role of biochemiluminescent photons for lysergic acid diethylamide (LSD)-induced phosphenes and visual hallucinations
- Therapeutic potential of flavonoids in spinal cord injury
- Is daily replication necessary when sampling cortisol concentrations in association studies of children with autism spectrum disorder? A systematic review and discussion paper