Neonatal encephalopathy: Pre-clinical studies in neuroprotection

Biochemical Society Transactions

Volumn 42, Issue 2, 2014, Pages 564-568

  Patel, Shyama D ^a   Pierce, Leslie ^a   Ciardiello, Amber J ^a   Vannucci, Susan J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cerebral energy failure; Hypoxia ischaemia; Mast cell; Perinatal asphyxia

Indexed keywords

BRAIN DAMAGE; BRAIN DISEASE; GESTATIONAL AGE; HUMAN; INDUCED HYPOTHERMIA; MAST CELL; NEUROPATHOLOGY; NEUROPROTECTION; NEWBORN DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PERINATAL PERIOD; PREGNANCY; PRIORITY JOURNAL; REVIEW; TRANSLATIONAL RESEARCH; ANIMAL; DISEASE MODEL; HYPOXIC ISCHEMIC ENCEPHALOPATHY; NEWBORN;

ANIMALS; BRAIN DISEASES; DISEASE MODELS, ANIMAL; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INFANT, NEWBORN;

EID: 84896947704     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130247     Document Type: Review

References (53)

1. Wu, Y.W., March, W.M., Croen, L.A., Grether, J.K., Escobar, G.J. and Newman, T.B. (2004) Perinatal stroke in children with motor impairment: a population-based study. Pediatrics 114, 612-619 (Pubitemid 41529514)
2. Vannucci, R.C. (2000) Hypoxic-ischemic encephalopathy. Am. J. Perinatol. 17, 113-120
3. de Vries, L.S. and Cowan, F.M. (2009) Evolving understanding of hypoxic-ischemic encephalopathy in the term infant. Semin. Pediatr. Neurol. 16, 216-225
4. Rice, 3rd, J.E., 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 (Pubitemid 11191192)
5. Dirnagl, U. (2006) Bench to bedside: the quest for quality in experimental stroke research. J. Cereb. Blood Flow Metab. 26, 1465-1478
6. Macleod, M.R., Fisher, M., O'Collins, V., Sena, E.S., Dirnagl, U., Bath, P.M., Buchan, A., van der Worp, H.B., Traystman, R.J., Minematsu, K. et al. (2009) Good laboratory practice: preventing introduction of bias at the bench. Stroke 40, e50-e52
7. Hagberg, H., Peebles, D. and Mallard, C. (2002) Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment. Retard. Dev. Disabil. Res. Rev. 8, 30-38 (Pubitemid 34754491)
8. Derrick, M., Drobyshevsky, A., Ji, X. and Tan, S. (2007) A model of cerebral palsy from fetal hypoxia-ischemia. Stroke 38, 731-735 (Pubitemid 46184250)
9. Derugin, N., Wendland, M., Muramatsu, K., Roberts, T.P., Gregory, G., Ferriero, D.M. and Vexler, Z.S. (2000) Evolution of brain injury after transient middle cerebral artery occlusion in neonatal rats. Stroke 31, 1752-1761 (Pubitemid 30437533)
10. Lorek, A., Takei, Y., Cady, E.B., Wyatt, J.S., Penrice, J., Edwards, A.D., Peebles, D., Wylezinska, M., Owen-Reece, H., Kirkbride, V. et al. (1994) Delayed ("secondary") cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr. Res. 36, 699-706 (Pubitemid 24357779)
11. Azzopardi, D., Wyatt, J.S., Cady, E.B., Delpy, D.T., Baudin, J., Stewart, A.L., Hope, P.L., Hamilton, P.A. and Reynolds, E.O. (1989) Prognosis of newborn infants with hypoxic-ischemic brain injury assessed by phosphorus magnetic resonance spectroscopy. Pediatr. Res. 25, 445-451 (Pubitemid 19128271)
12. Roth, S.C., Baudin, J., Cady, E., Johal, K., Townsend, J.P., Wyatt, J.S., Reynolds, E.O. and Stewart, A.L. (1997) Relation of deranged neonatal cerebral oxidative metabolism with neurodevelopmental outcome and head circumference at 4 years. Dev. Med. Child Neurol. 39, 718-725 (Pubitemid 27488564)
13. Vannucci, S.J., Seaman, L.B. and Vannucci, R.C. (1996) Effects of hypoxia-ischemia on GLUT1 and GLUT3 glucose transporters in immature rat brain. J. Cereb. Blood Flow Metab. 16, 77-81 (Pubitemid 26007952)
14. Vannucci, R.C. and Vannucci, S.J. (1997) A model of perinatal hypoxic-ischemic brain damage. Ann. N.Y. Acad. Sci. 835, 234-249 (Pubitemid 28046111)
15. Sheldon, R.A., Sedik, C. and Ferriero, D.M. (1998) Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res. 810, 114-122 (Pubitemid 29003396)
16. Vannucci, R.C., Towfighi, J. and Vannucci, S.J. (1998) Hypoxic preconditioning and hypoxic-ischemic brain damage in the immature rat: pathologic and metabolic correlates. J. Neurochem. 71, 1215-1220 (Pubitemid 28390276)
17. Mujsce, D.J., Christensen, M.A. and Vannucci, R.C. (1990) Cerebral blood flow and edema in perinatal hypoxic-ischemic brain damage. Pediatr Res 27, 450-453 (Pubitemid 20152792)
18. Blue, M.E. and Parnavelas, J.G. (1983) The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J. Neurocytol. 12, 697-712 (Pubitemid 13043553)
19. Huttenlocher, P.R. and de Courten, C. (1987) The development of synapses in striate cortex of man. Hum. Neurobiol. 6, 1-9 (Pubitemid 17058539)
20. Romijn, H.J., Hofman, M.A. and Gramsbergen, A. (1991) At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum. Dev. 26, 61-67
21. Miller, S.P. and Ferriero, D.M. (2009) From selective vulnerability to connectivity: insights from newborn brain imaging. Trends Neurosci. 32, 496-505
22. Back, S.A., Han, B.H., Luo, N.L., Chricton, C.A., Xanthoudakis, S., Tam, J., Arvin, K.L. and Holtzman, D.M. (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci. 22, 455-463 (Pubitemid 34049083)
23. Gerstner, B., DeSilva, T.M., Genz, K., Armstrong, A., Brehmer, F., Neve, R.L., Felderhoff-Mueser, U., Volpe, J.J. and Rosenberg, P.A. (2008) Hyperoxia causes maturation-dependent cell death in the developing white matter. J. Neurosci. 28, 1236-1245 (Pubitemid 351186357)
24. Towfighi, J., Mauger, D., Vannucci, R.C. and Vannucci, S.J. (1997) Influence of age on the cerebral lesions in an immature rat model of cerebral hypoxia-ischemia: a light microscopic study. Brain Res. Dev. Brain Res. 100, 149-160 (Pubitemid 27286387)
25. Tucker, A.M., Aquilina, K., Chakkarapani, E., Hobbs, C.E. and Thoresen, M. (2000) Development of amplitude-integrated electroencephalography and interburst interval in the rat. Pediatr. Res. 65, 62-66
26. Cuaycong, M., Engel, M., Weinstein, S.L., Salmon, E., Perlman, J.M., Sunderam, S. and Vannucci, S.J. (2011) A novel approach to the study of hypoxia-ischemia-induced clinical and subclinical seizures in the neonatal rat. Dev. Neurosci. 33, 241-250
27. Vannucci, R.C., Yager, J.Y. and Vannucci, S.J. (1994) Cerebral glucose and energy utilization during the evolution of hypoxic-ischemic brain damage in the immature rat. J. Cereb. Blood Flow Metab. 14, 279-288
28. Iadecola, C. and Anrather, J. (2011) The immunology of stroke: from mechanisms to translation. Nat. Med. 17, 796-808
29. Sanders, R.D., Manning, H.J., Robertson, N.J., Ma, D., Edwards, A.D., Hagberg, H. and Maze, M. (2010) Preconditioning and postinsult therapies for perinatal hypoxic-ischemic injury at term. Anesthesiology 113, 233-249
30. Blumberg, R.M., Cady, E.B., Wigglesworth, J.S., McKenzie, J.E. and Edwards, A.D. (1997) Relation between delayed impairment of cerebral energy metabolism and infarction following transient focal hypoxia-ischaemia in the developing brain. Exp. Brain Res. 113, 130-137 (Pubitemid 27039298)
31. Palmer, C., Brucklacher, R.M., Christensen, M.A. and Vannucci, R.C. (1990) Carbohydrate and energy metabolism during the evolution of hypoxic-ischemic brain damage in the immature rat. J. Cereb. Blood Flow Metab. 10, 227-235 (Pubitemid 20096194)
32. Vannucci, R.C. (1992) Cerebral carbohydrate and energy metabolism in perinatal hypoxic-ischemic brain damage. Brain Pathol. 2, 229-234
33. Vannucci, R.C., Towfighi, J. and Vannucci, S.J. (2004) Secondary energy failure after cerebral hypoxia-ischemia in the immature rat. J. Cereb. Blood Flow Metab. 24, 1090-1097 (Pubitemid 39332148)
34. Brucklacher, R.M., Vannucci, R.C. and Vannucci, S.J. (2002) Hypoxic preconditioning increases brain glycogen and delays energy depletion from hypoxia-ischemia in the immature rat. Dev. Neurosci. 24, 411-417 (Pubitemid 36359373)
35. Thoresen, M., Penrice, J., Lorek, A., Cady, E.B., Wylezinska, M., Kirkbride, V., Cooper, C.E., Brown, G.C., Edwards, A.D., Wyatt, J.S. et al. (1995) Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr. Res. 37, 667-670
36. Shankaran, S., Pappas, A., McDonald, S.A., Vohr, B.R., Hintz, S.R., Yolton, K., Gustafson, K.E., Leach, T.M., Green, C., Bara, R. et al. (2012) Childhood outcomes after hypothermia for neonatal encephalopathy. N. Engl. J. Med. 366, 2085-2092
37. Azzopardi, D.V., Strohm, B., Edwards, A.D., Dyet, L., Halliday, H.L., Juszczak, E., Kapellou, O., Levene, M., Marlow, N., Porter, E. et al. (2009) Moderate hypothermia to treat perinatal asphyxial encephalopathy. N. Engl. J. Med. 361, 1349-1358
38. Gunn, A.J., Gunn, T.R., de Haan, H.H., Williams, C.E. and Gluckman, P.D. (1997) Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J. Clin. Invest. 99, 248-256 (Pubitemid 27053465)
39. Bona, E., Hagberg, H., Loberg, E.M., Bagenholm, R. and Thoresen, M. (1998) Protective effects of moderate hypothermia after neonatal hypoxia-ischemia: short- and long-term outcome. Pediatr. Res. 43, 738-745 (Pubitemid 28243643)
40. Barks, J.D., Liu, Y.Q., Shangguan, Y. and Silverstein, F.S. (2010) Phenobarbital augments hypothermic neuroprotection. Pediatr. Res. 67, 532-537
41. Fang, A.Y., Gonzalez, F.F., Sheldon, R.A. and Ferriero, D.M. (2013) Effects of combination therapy using hypothermia and erythropoietin in a rat model of neonatal hypoxia-ischemia. Pediatr. Res. 73, 12-17
42. Pierce, L., Patel, S., Ciardiello, A., Vannucci, S. and Perlman, J.M. (2013) Therapeutic hypothermia reduces progression of hypoxic ischemic brain damage in the term-equivalent (P10) rat pup. Child Neurology Society Conference, Austin, TX, U.S.A. 30 October-2 November 2013, Abstract 167
43. Vannucci, S.J. and Hagberg, H. (2004) Hypoxia-ischemia in the immature brain. J. Exp. Biol. 207, 3149-3154 (Pubitemid 39275289)
44. Dirnagl, U., Iadecola, C. and Moskowitz, M.A. (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391-397 (Pubitemid 29453643)
45. Gonzalez, F.F. and Ferriero, D.M. (2008) Therapeutics for neonatal brain injury. Pharmacol. Ther. 120, 43-53
46. Jin, Y., Silverman, A.J. and Vannucci, S.J. (2007) Mast cell stabilization limits hypoxic-ischemic brain damage in the immature rat. Dev. Neurosci. 29, 373-384 (Pubitemid 47343691)
47. Jin, Y., Silverman, A.J. and Vannucci, S.J. (2009) Mast cells are early responders after hypoxia-ischemia in immature rat brain. Stroke 40, 3107-3112
48. Biran, V., Cochois, V., Karroubi, A., Arrang, J.M., Charriaut-Marlangue, C. and Heron, A. (2008) Stroke induces histamine accumulation and mast cell degranulation in the neonatal rat brain. Brain Pathol. 18, 1-9
49. Strbian, D., Karjalainen-Lindsberg, M.L., Tatlisumak, T. and Lindsberg, P.J. (2006) Cerebral mast cells regulate early ischemic brain swelling and neutrophil accumulation. J. Cereb. Blood Flow Metab. 26, 605-612
50. Silver, R. and Curley, J.P. (2013) Mast cells on the mind: new insights and opportunities. Trends Neurosci. 36, 513-521
51. Michaloudi, H., Grivas, I., Batzios, C., Chiotelli, M. and Papadopoulos, G.C. (2003) Parallel development of blood vessels and mast cells in the lateral geniculate nuclei. Brain Res. Dev. Brain Res. 140, 269-276 (Pubitemid 36173983)
52. Khalil, M., Ronda, J., Weintraub, M., Jain, K., Silver, R. and Silverman, A.J. (2007) Brain mast cell relationship to neurovasculature during development. Brain Res. 1171, 18-29 (Pubitemid 47404533)
53. Degos, V., Favrais, G., Kaindl, A.M., Peineau, S., Guerrot, A.M., Verney, C. and Gressens, P. (2010) Inflammation processes in perinatal brain damage. J. Neural Transm. 117, 1009-1017