Sex differences in brain MRI abnormalities and neurodevelopmental outcomes in a rat model of neonatal hypoxia-ischemia

References

• Glass HC, Ferriero DM. Treatment of hypoxic-ischemic encephalopathy in newborns. Curr Treat Options Neurol 2007;9(6):414–23. PMID: 18173941.
   PubMedGoogle Scholar
• Badr Zahr LK, Purdy I. Brain injury in the infant: the old, the new, and the uncertain. J Perinat Neonatal Nurs 2006;20(2):163–75; quiz 76-7. PMID: 16714917.
   PubMed Web of Science ®Google Scholar
• Volpe JJ. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001;50(5):553–62. doi: 10.1203/00006450-200111000-00003. PMID: 11641446.
   PubMed Web of Science ®Google Scholar
• (CDC) CfDCaP. Economic costs associated with mental retardation, cerebral palsy, hearing loss, and vision impairment – United States, 2003. MMWR Morb Mortal Wkly Rep 2004;53(3):57–9. PMID: 14749614.
   PubMedGoogle Scholar
• Fatemi A, Wilson MA, Johnston MV. Hypoxic-ischemic encephalopathy in the term infant. Clin Perinatol 2009;36(4):835–58, doi: 10.1016/j.clp.2009.07.011. PMID: 19944838.
   PubMed Web of Science ®Google Scholar
• Takashima S, Itoh M, Oka A. A history of our understanding of cerebral vascular development and pathogenesis of perinatal brain damage over the past 30 years. Semin Pediatr Neurol 2009;16(4):226–36. doi: 10.1016/j.spen.2009.09.004. PMID: 19945657.
   PubMed Web of Science ®Google Scholar
• Haddad B, Mercer BM, Livingston JC, et al. Outcome after successful resuscitation of babies born with apgar scores of 0 at both 1 and 5 minutes. Am J Obstet Gynecol 2000;182(5):1210–4. PMID: 10819860.
   PubMed Web of Science ®Google Scholar
• Carli G, Reiger I, Evans N. One-year neurodevelopmental outcome after moderate newborn hypoxic ischaemic encephalopathy. J Paediatr Child Health 2004;40(4):217–20. PMID: 15009553.
   PubMed Web of Science ®Google Scholar
• Gunn AJ, Bennet L. Timing of injury in the fetus and neonate. Curr Opin Obstet Gynecol 2008;20(2):175–81. doi: 10.1097/GCO.0b013e3282f4ef9e. PMID: 18388819.
   PubMed Web of Science ®Google Scholar
• Busse S, Breder J, Dinkel K, et al. Inhibitors of cation-chloride-cotransporters affect hypoxic/hypoglycemic injury in hippocampal slices. Brain Res 2005;1046(1–2):116–21. doi: 10.1016/j.brainres.2005.03.055. PMID: 15893737.
   PubMed Web of Science ®Google Scholar
• Cimino M, Balduini W, Carloni S, et al. Neuroprotective effect of simvastatin in stroke: a comparison between adult and neonatal rat models of cerebral ischemia. Neurotoxicology 2005;26(5):929–33. doi: 10.1016/j.neuro.2005.03.009. PMID: 15923039.
   PubMed Web of Science ®Google Scholar
• Drobyshevsky A, Luo K, Derrick M, et al. Motor deficits are triggered by reperfusion-reoxygenation injury as diagnosed by MRI and by a mechanism involving oxidants. J Neurosci 2012;32(16):5500–9. doi: 10.1523/JNEUROSCI.5986-11.2012. PMID: 22514312.
   PubMed Web of Science ®Google Scholar
• Azzopardi DV, Strohm B, Edwards AD, et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med 2009;361(14):1349–58. doi: 10.1056/NEJMoa0900854. PMID: 19797281.
   PubMed Web of Science ®Google Scholar
• Pimentel-Coelho PM, Mendez-Otero R. Cell therapy for neonatal hypoxic-ischemic encephalopathy. Stem Cells Dev 2010;19(3):299–310. doi: 10.1089/scd.2009.0403.PMID:19916801.
   PubMed Web of Science ®Google Scholar
• Jund R, Kastenbauer E. Susceptibility of isolated rat facial nerve to anaerobic stress. Eur Arch Otorhinolaryngol 1997;254(Suppl 1):S64–7. PMID: 9065631.
   PubMed Web of Science ®Google Scholar
• Peasley MA, Shi R. Ischemic insult exacerbates acrolein-induced conduction loss and axonal membrane disruption in guinea pig spinal cord white matter. J Neurol Sci 2003;216(1):23–32. PMID: 14607299.
   PubMed Web of Science ®Google Scholar
• Irani DN, Prow NA. Neuroprotective interventions targeting detrimental host immune responses protect mice from fatal alphavirus encephalitis. J Neuropathol Exp Neurol 2007;66(6):533–44. doi:10.1097/01.jnen.0000263867.46070.e2. PMID: 17549013.
   PubMed Web of Science ®Google Scholar
• Cotten CM, Shankaran S. Hypothermia for hypoxic-ischemic encephalopathy. Expert Rev Obstet Gynecol 2010;5(2):227–39. doi: 10.1586/eog.10.7. PMID: 20625441.
   PubMedGoogle Scholar
• Steinman KJ, Gorno-Tempini ML, Glidden DV, et al. Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 2009;123(3):1025–30. doi: 10.1542/peds.2008-1203. PMID: 19255035.
   PubMed Web of Science ®Google Scholar
• Rice JE, 3rd, Vannucci RC, Brierley JB. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 1981;9(2):131–41. doi: 10.1002/ana.410090206. PMID: 7235629.
   PubMed Web of Science ®Google Scholar
• Hill CA, Fitch RH. 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;2012:867531. doi: 10.1155/2012/867531. PMID: 22474588.
   PubMedGoogle Scholar
• Sanches EF, Arteni NS, Nicola F, et al. Early hypoxia-ischemia causes hemisphere and sex-dependent cognitive impairment and histological damage. Neuroscience 2013;237:208–15. doi: 10.1016/j.neuroscience.2013.01.066. PMID:23395861.
   PubMed Web of Science ®Google Scholar
• Zhu C, Xu F, Wang X, Shibata M, et al. Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. J Neurochem 2006;96(4):1016–27. PMID: 16412092.
   PubMed Web of Science ®Google Scholar
• Hurn PD, Vannucci SJ, Hagberg H. Adult or perinatal brain injury: does sex matter? Stroke 2005;36(2):193–5. doi: 10.1161/01.STR.0000153064.41332.f6. PMID: 15625289.
   PubMed Web of Science ®Google Scholar
• Smith AL, Alexander M, Rosenkrantz TS, et al. 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 2014;254:54–67. doi: 10.1016/j.expneurol.2014.01.003. PMID: 24434477.
   PubMed Web of Science ®Google Scholar
• Hill CA, Threlkeld SW, Fitch RH. Early testosterone modulated sex differences in behavioral outcome following neonatal hypoxia ischemia in rats. Int J Dev Neurosci 2011;29(4):381–8. doi: 10.1016/j.ijdevneu.2011.03.005. PMID: 21473905.
   PubMed Web of Science ®Google Scholar
• Ten VS, Bradley-Moore M, Gingrich JA, et al. Brain injury and neurofunctional deficit in neonatal mice with hypoxic-ischemic encephalopathy. Behav Brain Res 2003;145(1-2):209–19. PMID: 14529818.
   PubMed Web of Science ®Google Scholar
• Wang Y, Cheung PT, Shen GX, et al. Hypoxic-ischemic brain injury in the neonatal rat model: relationship between lesion size at early MR imaging and irreversible infarction. AJNR Am J Neuroradiol 2006;27(1):51–4. PMID: 16418355.
   PubMed Web of Science ®Google Scholar
• Wang Y, Cheung PT, Shen GX, et al. Comparing diffusion-weighted and T2-weighted MR imaging for the quantification of infarct size in a neonatal rat hypoxic-ischemic model at 24h post-injury. Int J Dev Neurosci 2007;25(1):1–5. doi: 10.1016/j.ijdevneu.2006.12.003. PMID: 17229540.
   PubMed Web of Science ®Google Scholar
• Wideroe M, Olsen O, Pedersen TB, et al. Manganese-enhanced magnetic resonance imaging of hypoxic-ischemic brain injury in the neonatal rat. Neuroimage 2009;45(3):880–90. doi: 10.1016/j.neuroimage.2008.12.007. PMID: 19138750.
   PubMed Web of Science ®Google Scholar
• de Medinaceli L, Freed WJ, Wyatt RJ. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 1982;77(3):634–43. PMID: 7117467.
   PubMed Web of Science ®Google Scholar
• Vohr BR, Wright LL, Poole WK,et al. Neurodevelopmental outcomes of extremely low birth weight infants <32 weeks' gestation between 1993 and 1998. Pediatrics 2005;116(3):635–43. PMID:16143580.
   PubMed Web of Science ®Google Scholar
• Morken TS, Wideroe M, Vogt C, et al. Longitudinal diffusion tensor and manganese-enhanced MRI detect delayed cerebral gray and white matter injury after hypoxia-ischemia and hyperoxia. Pediatr Res 2013;73(2):171–9. doi: 10.1038/pr.2012.170. PMID: 23174702.
   PubMed Web of Science ®Google Scholar
• Wideroe M, Havnes MB, Morken TS, et al. Doxycycline treatment in a neonatal rat model of hypoxia-ischemia reduces cerebral tissue and white matter injury: a longitudinal magnetic resonance imaging study. Eur J Neurosci 2012;36(1):2006–16. doi: 10.1111/j.1460-9568.2012.08114.x. PMID: 22594966.
   PubMed Web of Science ®Google Scholar
• Tuor UI, Qiao M, Morgunov M, et al. Magnetization transfer and diffusion imaging of acute axonal damage in the cerebral peduncle following hypoxia-ischemia in neonatal rats. Pediatr Res 2013;73(3):325–31. doi: 10.1038/pr.2012.178. PMID: 23202723.
   PubMed Web of Science ®Google Scholar
• Fau S, Po C, Goyenvalle C, et al. Do early MRI signals predict lesion size in a neonatal stroke rat model? AJNR Am J Neuroradiol 2013;34(7):E73–6. doi: 10.3174/ajnr.A3069. PMID: 22555584.
   Google Scholar
• Robertson CM, Joffe AR, Moore AJ, et al. Neurodevelopmental outcome of young pediatric intensive care survivors of serious brain injury. Pediatr Crit Care Med 2002;3(4):345–50. doi: 10.1097/01.PCC.0000031473.93121.2E. PMID: 12780952.
   PubMedGoogle Scholar
• Johnston MV. Brain plasticity in paediatric neurology. Eur J Paediatr Neurol 2003;7(3):105–13. PMID: 12788036.
   PubMed Web of Science ®Google Scholar
• Wainwright MS, Mannix MK, Brown J, et al. L-carnitine reduces brain injury after hypoxia-ischemia in newborn rats. Pediatr Res 2003;54(5):688–95. doi: 10.1203/01.PDR.0000085036.07561.9C. PMID: 12904603.
   PubMed Web of Science ®Google Scholar
• Fox WM. Reflex-ontogeny and behavioural development of the mouse. Anim Behav 1965;13(2):234–41. PMID: 5835840.
   PubMed Web of Science ®Google Scholar
• Scher MS. Neonatal hypertonia: I. Classification and structural-functional correlates. Pediatr Neurol 2008;39(5):301–6. doi: 0.1016/j.pediatrneurol.2008.09.001. PMID:18940552.
   PubMed Web of Science ®Google Scholar
• Futagi Y, Suzuki Y, Goto M. Clinical significance of plantar grasp response in infants. Pediatr Neurol 1999;20(2):111–5. PMID: 10082338.
   PubMed Web of Science ®Google Scholar
• Zafeiriou DI, Tsikoulas IG, Kremenopoulos GM, et al. Moro reflex profile in high-risk infants at the first year of life. Brain Dev 1999;21(3):216–7. PMID: 10372911.
   PubMed Web of Science ®Google Scholar
• feiriou DI, Tsikoulas IG, Kremenopoulos GM, et al. Moro reflex profile in high-risk infants at the first year of life. Brain Dev 1999;21(3):216–7. PMID: 10372911.
   PubMed Web of Science ®Google Scholar
• Palmer FB. Strategies for the early diagnosis of cerebral palsy. J Pediatr 2004;145(2 Suppl):S8–S11. PMID:15292881.
   Web of Science ®Google Scholar
• Alkayed NJ, Harukuni I, Kimes AS, et al. Gender-linked brain injury in experimental stroke. Stroke 1998;29(1):159–65; discussion 66. PMID: 9445346.
   PubMed Web of Science ®Google Scholar
• McCullough LD, Hurn PD. Estrogen and ischemic neuroprotection: an integrated view. Trends Endocrinol Metab 2003;14(5):228–35. PMID: 12826329.
   PubMed Web of Science ®Google Scholar
• Rose J, Butler EE, Lamont LE, et al. Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev Med Child Neurol 2009;51(7):526–35. doi: 10.1111/j.1469-8749.2008.03231.x. PMID: 19459915.
   PubMed Web of Science ®Google Scholar
• Mayoral SR, Omar G, Penn AA. Sex differences in a hypoxia model of preterm brain damage. Pediatr Res 2009;66(3):248–53. doi: 10.1203/PDR.0b013e3181b1bc34. PMID: 19542909.
   PubMed Web of Science ®Google Scholar
• Desgent S, Duss S, Sanon NT, et al. Early-life stress is associated with gender-based vulnerability to epileptogenesis in rat pups. PLoS One 2012;7(8):e42622. doi: 10.1371/journal.pone.0042622. PMID: 22880055.
   Google Scholar
• Grafe MR, Woodworth KN, Noppens K, et al. Long-term histological outcome after post-hypoxic treatment with 100% or 40% oxygen in a model of perinatal hypoxic-ischemic brain injury. Int J Dev Neurosci 2008;26(1):119–24. doi: 10.1016/j.ijdevneu.2007.09.004. PMID: 17964109.
   PubMed Web of Science ®Google Scholar
• Fleiss B, Nilsson MK, Blomgren K, et al. Neuroprotection by the histone deacetylase inhibitor trichostatin A in a model of lipopolysaccharide-sensitised neonatal hypoxic-ischaemic brain injury. J Neuroinflammation 2012;9:70. doi: 10.1186/1742-2094-9-70. PMID: 22512781.
   PubMed Web of Science ®Google Scholar
• Hurn PD, Brass LM. Estrogen and stroke: a balanced analysis. Stroke 2003;34(2):338–41. PMID: 12574529.
   PubMed Web of Science ®Google Scholar
• Simpkins JW, Yang SH, Liu R, et al. Estrogen-like compounds for ischemic neuroprotection. Stroke 2004;35(11 Suppl 1):2648–51. doi: 10.1161/01.STR.0000143734.59507.88. PMID: 15472107.
   PubMed Web of Science ®Google Scholar
• Hill CA, Alexander ML, McCullough LD, et al. Inhibition of X-linked inhibitor of apoptosis with embelin differentially affects male versus female behavioral outcome following neonatal hypoxia-ischemia in rats. Dev Neurosci 2011;33(6):494–504. doi: 10.1159/000331651. PMID: 22041713.
   PubMed Web of Science ®Google Scholar
• Nunez J. Sex and steroid hormones in early brain injury. Rev Endocr Metab Disord 2012;13(3):173–86. doi: 10.1007/s11154-012-9219-3. PMID: 22565659.
   PubMed Web of Science ®Google Scholar
• Martin N, Pourie G, Bossenmeyer-Pourie C, et al. Conditioning-like brief neonatal hypoxia improves cognitive function and brain tissue properties with marked gender dimorphism in adult rats. Semin Perinatol 2010;34(3):193–200. doi: 10.1053/j.semperi.2010.02.003. PMID: 20494735.
   PubMed Web of Science ®Google Scholar
• Marlow N, Rose AS, Rands CE, et al. Neuropsychological and educational problems at school age associated with neonatal encephalopathy. Arch Dis Child Fetal Neonatal Ed 2005;90(5):F380–7. doi: 10.1136/adc.2004.067520. PMID: 16113154.
   Google Scholar