Animal models for the study of perinatal hypoxic-ischemic encephalopathy: A critical analysis

Early Human Development

Volumn 47, Issue 2, 1997, Pages 115-146

  Roohey, Tabasam ^a   Raju, Tonse N K ^a   Moustogiannis, Anastasia N ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Birth asphyxia; Brain damage; Brain protection; Hypoxia; Newborn; Newborn animals

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; GUINEA PIG; NEWBORN HYPOXIA; NONHUMAN; PRIMATE; SHEEP; SWINE; TIME;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; ASPHYXIA NEONATORUM; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HUMANS; INFANT, NEWBORN;

EID: 0031579263     PISSN: 03783782     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-3782(96)01773-2     Document Type: Article

References (105)

1. [1] Ashwal, S., Majcher, J.S. and Longo, L.D. (1981): Patterns of fetal lamb regional cerebral blood flow during and after prolonged hypoxia: studies during the posthypoxic recovery period. Am. J. Obstet. Gynecol., 139, 365-372.
2. [2] Ba, A. and Seri, B.V. (1995): Psychomotor functions in developing rats: ontogenetic approach to structure-function relationships. Neurosci. Biobehav. Reviews, 19, 413-425.
3. [3] Bailey, C.J. and Windle, W.F. (1959): Neurological, psychological and neurohistological defects following asphyxia neonatorum in the guinea pig. Exp. Neurol., 1, 467-482.
4. [4] Barks, J.D., Post, M. and Tuor, U.I. (1991): Dexamethasone prevents hypoxic-ischemic brain damage in neonatal rat. Pediatr. Res., 29, 558-563.
5. [5] Becker, R.F. and Donnell, W. (1952): Learning behavior in guinea pigs subjected to asphyxia at birth. J. Comp. Physiol. Psychol., 45, 153-162.
6. [6] Beilharz, E.J., Klempt, N.D., Klempt, M., Sirimanne, E., Dragunow, M. and Gluckman, P.D. (1993): Differential expression of insulin like growth gactor binding proteins (IGFBP) 4 and 5 mRNA in rat brain after transient hypoxic-ischemic injury. Mol. Brain. Res., 18, 209-215.
7. [7] Berman, D., Karalitzky, A.R. and Berman, A.J. (1971): Auditory thresholds in monkeys asphyxiated at birth. Exp. Neurol., 31, 140-149.
8. [8] Boksa P, Krishnamurthy A and Brooks W. Effects of a period of asphyxia during birth on spatial learning in the rat. Pediatr. Res., 37, 4, 1995.
9. [9] Brann, A.W. and Myers, R.E. (1975): Central nervous system findings in the newborn monkey following severe in utero partial asphyxia. Neurology, 25, 327-338.
10. [10] Burke, R.E., Franklin, S.O. and Inturrisi, C.E. (1994): Acute and persistent suppression of preproenkephalin mRNA expression in the striatum following developmental hypoxic-ischemic injury. J. Neurochem., 62, 1878-1886.
11. [11] Burtrum, D. and Silverstein, F.S. (1994): Hypoxic-ischemic brain injury stimulates Glial Fibrillary Acidic Protein mRNA and protein expression in neonatal rats. Exp. Neurol., 126, 112-118.
12. [12] Chumas, P.D., Del Bigio, M.R., Drake, J.M. and Tuor, U.I. (1993): A comparison of the protective effect of dexamethasone to other potential prophylactic agents in a neonatal rat model of cerebral hypoxia ischemia. J. Neurosurg., 79, 414-420.
13. [13] Cockburn, F., Daniel, S.S., Dawes, G.S., James, L.S., Myers, R.E., Niemann, W., Rodriguez de Curet, H. and Ross, B.B. (1969): The effect of pentobarbital anesthesia on resuscitation and brain damage in fetal rhesus monkeys asphyxiated at delivery. J. Peds., 75, 281-291.
14. [14] Dawes, G.S., Hibbard, E. and Windell, W.F. (1964): The effect of alkali and glucose infusion on permanent brain damage in rhesus monkeys asphyxiated at birth. J. Peds., 65, 801-806.
15. [15] De Haan, H.H., Van Reempts, J.L.H., Borgers, M., De Haan, J., Vles, J.S.H. and Hasaart, T.H.M. (1993): Possible neuroprotective properties of flunarizine infused after asphyxia in fetal lambs are not explained by effects on cerebral blood flow or systemic blood pressure. Pediatr. Res., 34, 379-384.
16. [16] Dell'Anna, M.E., Luthman, J., Lindqvist, E. and Olson, L. (1993): Development of monoamine systems after neonatal anoxia in rats. Brain Res. Bull., 32, 159-170.
17. [17] Dobbing, J. and Sands, J. (1979): Comparative aspects of the brain growth suprt. Early Hum. Dev., 3, 79-83.
18. [18] Ferrara, A., Atakent, Y., Bhogal, M. and Klupsteen, M. (1984): Impact of intermittent prolonged asphyxia in rat sucklings on growth and development. Growth, 48, 120-133.
19. [19] Ferriero, D.M., Arcavi, L.J., Sagar, S.M., McIntosh, T.K. and Simon, R.P. (1988): Selective sparing of NADPH-diaphorase neurons in neonatal hypoxia ischemia. Ann. Neurol., 24, 670-676.
20. [20] Goddard, J. Lewis, R.M., Alcala, H. and Zeller, R.S. (1980): Intraventricular hemorrhage - an animal model. Biol. Neonate, 37, 39.
21. [21] Goodman, J.H., Wasterlain, C.G., Masserweh, M.F., Dean, E., Sollas, A.L. and Sloviter, R.S. (1993): Calbindin-D28K immunoreactivity and selective vulnerability to ischemia in the dentate gyrus of the developing rat. Brain Res., 606, 309-314.
22. [22] Gunn, A.J., Mydlar, T., Bennet, L., Faull, R.L.M., Gorter, S., Cook, C., Johnston, B.M. and Gluckman, P.D. (1989): The neuroprotective actions of a calcium channel antagonist flunarizine in the infant rat. Pediatr. Res., 25, 573-576.
23. [23] Gunn, A.J., Dragunow, M., Faull, R.L.M. and Gluckman, P.D. (1990): Effects of hypoxia-ischemia and seizures on neuronal and glial like c-fos protein levels in the infant rat. Pediatr. Res., 531, 105-16.
24. [24] 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.
25. [25] Haaland, K., Orderud, W.J. and Thoresen, M. (1995): The piglet model for cerebral ciruclation: an angiographic study. Biol. Neonate, 75-80.
26. [26] Habgood, M.D., Jones, S.E., Maroni, J.M., Pickard, J.D., Richards, H.K. and Saunders, N.R. (1991): Cerebral blood flow in the anesthetized immature sheep fetus and the response to hypercapnia. Exp. Physiol., 76, 495-505.
27. [27] Hamada, Y., Hayakawa, T., Hattori, H. and Mikawa, H. (1994): Inhibitor of nitric oxide synthesis reduces hypoxic-ischemic brain damage in the neonatal rat. Pediatr. Res., 35, 10-14.
28. [28] Hattori, H. and Wasterlain, C.G. (1990): Posthypoxic glucose supplement reduces hypoxic-ischemic brain damage in the neonatal rat. Ann. Neurol., 28, 122-128.
29. [29] Hattori, H., Morin, A.M., Schwartz, P.H., Fujikawa, D.G. and Wasterlain, C.G. (1989): Posthypoxic treatment with MK-801 reduces hypoxic ischemic damage in the neonatal rat. Neurology, 39, 713-718.
30. [30] Hayakawa, T., Higuchi, Y., Nigami, H. and Hattori, H. (1994): Zonisamide reduces hypoxic-ischemic brain damage in neonatal rats irrespective of its anticonvulsant effect. Eur. J. Pharmacol., 257, 131-136.
31. [31] Hayakawa, T., Hamada, Y., Maihara, T., Hattori, H. and Mikawa, H. (1994): Phenytoin reduces neonatal hypoxic-ischemic brain damage in rats. Life Sci., 54, 387-392.
32. [32] Heyser C.J., Spear N.E. and Spear L.P. Effects of prenatal exposure to cocaine on Morris water maze performance in adult rats. Behav. Neurosci., 109, 4:734-743, 1995.
33. [33] Hickey, R.W., Akino, M., Strausbaugh S. and De Courten-Myers, G.N. (1996): Use of the Morris water maze and acoustic startle chamber to evaluate neurologic injury after asphyxial arrest in rats. Pediatr. Res., 39, 77-84.
34. [34] Hyman, A., Berman, D. and Berman, A.J. (1971): Deficits in unsignalled avoidance behavior in rhesus monkeys asphyxiated at birth. Exp. Neurol., 30, 362-366.
35. [35] Hyman, A., Parker, B., Berman, D. and Berman, A.J. (1970): Delayed response deficits in neonatally asphyxiated rhesus monkeys. Exp. Neurol., 28, 420-425.
36. [36] Jacobson H.N., Windle W.F. (1960): Responses of fetal and newborn monkeys to asphyxia. J. Physiol., 153, 447-456.
37. [37] Jensen, F.E., Applegate, C.D., Holtzman, D., Belin, T.R. and Burchfiel, J.L. (1991): Epileptogenic effect of hypoxia in the immature rodent brain. Ann. Neurol., 29, 629-637.
38. [38] Johnston, M.V. (1983): Neurotransmitter alterations in a model of perinatal hypoxic-ischemic brain injury. Ann. Neurol., 13, 511-518.
39. [39] Johnston, M.V. and Hudson, C. (1987): Effects of postnatal hypoxia-ischemia on cholinergic neurons in the developing rat forebrain: choline acetyltransferase imunocytochemistry. Dev. Brain Res., 34, 41-50.
40. [40] Kaneko, K. (1985): The effect of perinatal anoxia on amino acid metabolism in the developing brain. Part I: The effect of experimental anoxia on the free amino acid patterns in the brain of neonatal rats. Brain Dev., 7, 392-399.
41. [41] Katz, L. Ebmeyer U, Safer P. Radovsky, A. and Neumar, R. (1995): Outcome model of asphyxial cardiac arrest in rats. J. Cereb. Blood Flow Metab., 15, 1032-1039.
42. [42] Klempt, M., Klempt, N.D. and Gluckman, P.D. (1993): Hypoxia and hypoxia/ischemia affect the expression of insulin-like growth factor binding protein 2 in the developing rat brain. Mol. Brain Res., 17, 347-350.
43. [43] LeBlanc, M.H., Farias, L.A., Markov, A.K., Evans, O.B., Smith, B., Smith, E.E. and Brown, E.G. (1991): Fructose 1-6 diphosphate, when given 5 min after injury, does not ameliorate hypoxic-ischemic injury to the central nervous system in the newborn pig. Biol. Neonate, 59, 98-108.
44. [44] LeBlanc, M.H., Vig, V., Smith, B., Parker, C.C., Evans, O.B. and Smith, E.E. (1991): MK-801 does not protect against hypoxic-ischemic brain injury in piglets. Stroke, 22, 1270-1275.
45. [45] LeBlanc, M.H., Farias, L.A., Evans, O.B., Vig, V., Smith, E.E. and Markov, A.K. (1991): Fructose 1-6 bisphosphate, when given immediately before reoxygenation or before injury, does not ameliorate hypoxic-ischemic injury to central nervous system in the newborn pig. Crit. Care Med., 19, 75-83.
46. [46] LeBlanc, M.H., Vig, V., Randhawa, T., Smith, E.E., Parker, C.C. and Brown, E.G. (1993): Use of polyethylene glycol-bound superoxide dismutase, PEG bound catalase and nimodipine to prevent hypoxic-ischemic injury to the brain of newborn pigs. Crit. Care Med., 21, 252-259.
47. [47] LeBlanc, M.H., Huang, M., Vig, V., Patel, D. and Smith, E.E. (1993): Glucose affects the severity of hypoxic-ischemic brain injury in newborn pigs. Stroke, 24, 1055-1062.
48. [48] LeBlanc, M.H., Huang, M., Patel, D., Smith, E.E. and Devidas, M. (1994): Glucose given after hypoxic-ischemia does not affect brain injury in piglets. Stroke, 25, 1443-1448.
49. [49] Lorek, A., Takei, Y., Cady, E.B., Wyatt, J.S., Penrice, J., Edwards, A.D., Peebles, D. and Wylezinska, M. (1994): Delayed ('secondary') cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-h studies by phosphorus magnetic resonance spectroscopy. Pediatr. Res., 36, 699-706.
50. [50] Levine, S. (1960): Anoxic-ischemic encephalopathy in rats. Am. J. Pathol., 36. 1-17.
51. [51] Lun, A., Szuencz, L., Gross, J., Horvath, G. and Nagy, I. (1989): Effect of mild postnatal hypoxia and L-DOPA administration on dopamine concentration in striata of newborn rat and long-term sequelae on dopamine turnover. Biomed. Biochim. Acta, 48, 231-236.
52. [52] Lun, A., Dominick, B. and Gross, J. (1990): An animal model of perinatal hypoxic brain damage: behavioral aspects. Biomed. Biochim. Acta, 49, 1021-1026.
53. [53] Mallard, E.C., Williams, C.E., Gunn, A.J., Gunning, M.I. and Gluckman, RD. (1993): Frequent episodes of brief ischemia sensitize the fetal sheep brain to neuronal loss and induce striatal injury. Pediatr. Res., 33, 61-65.
54. [54] Martin, R. and Day, M.H. (1992): Primate Reproduction. In: Jones, S., Martin, R., Philbeam, D. (eds). The Cambridge Encyclopedia of Human Evolution. Cambridge, Cambridge University Press, 88-94.
55. [55] McCulloch, K.M., Raju, T.N.K., Burt, C.T., Roohey, T., Moustogiannis, A., Zachary, J.F. and Shankarrao, R. (1993): A long-term surviving animal model of neonatal hypoxic ischemic encephalopathy (HIE). Pediatr. Res., 33, 373A (Abstract).
56. [56] Mirsky, A.F., Orren, M.M., Stanton, L., Fullerton, B.C., Harris, H. and Myers, R.E. (1979): Auditory evoked potentials and auditory behavior following prenatal and perinatal asphyxia in rhesus monkeys. Dev. Psychobiology, 12, 369-379.
57. [57] Musjsce, 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.
58. [58] Myers, R.E. (1977): Experimental models of perinatal brain damage. Relevance to human pathology. In: L Gluck (ed) Intrauterine Asphyxia and the Developing Fetal Brain. Year Book Publishing Co. New York, pp 37-97.
59. [59] Myers, R.E. (1969): Atrophic cortical sclerosis associated with status marmoratus in perinatally damaged monkeys. Neurology, 19, 1177-1188.
60. [60] Myers, R.E. (1975): Fetal asphyxia due to umbilical cord compression. Biol. Neonate, 26, 21-43.
61. [61] Nelson, C. and Silverstein, F.S. and (1994): Acute disruption of cytochrome oxidase activity in brain in a perinatal rat stroke model. Pediatr. Res., 36, 12-19.
62. [62] Nozaki, K., Finklestein, S.P. and Beal, M.F. (1993): Basic fibroblast growth factor protects against hypoxia-ischemia and NMDA neurotoxicity in neonatal rats. J. Cereb. Blood Flow Metabol., 13, 221-228.
63. [63] Palmer, C., Vannucci, R.C. and Towfighi, J. (1990): Reduction of perinatal hypoxic ischemic brain damage with allopurinol. Pediatr. Res., 27, 332-336.
64. [64] 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 immature rat. J. Cereb. Blood Flow Metabol. 10: 227-235.
65. [65] Palmer, C., Towfighi, J., Roberts, R.L. and Heitjan, D.F. (1993): Allopurinol administered after inducing hypoxia ischemia reduces brain injury in 7-day-old rats. Pediatr. Res., 33, 405-411.
66. [66] Raju, T.N.K. (1992): Some animal models for the study of perinatal asphyxia. Biol. Neonate, 62, 202-214.
67. [67] Ranck, J.B. and Windle, W.F. (1959): Brain damage in the monkey, Macaca mulatta, by asphyxia neonatorum. Exp. Neurol., 1, 130-154.
68. [68] Rice, 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.
69. [69] Romijn, H.J., Hofman, M.A. and Gramsbergen, A. (1991): At what age is the developing cellular cortex of the rat comaparable to that of full-term newborn human fetus? 26, 61-67.
70. [70] Romijn, H.J., Janszen, A.W.J.W., van Voorst, M.J.D., Buijs, R.M., Balazs, R. and Swaab, D.F. (1992): Perinatal hypoxic-ischemic encephalopathy affects the proportion of GABA immunoreactive neurons in the cerebral cortex of the rat. Brain Res., 592, 17-28.
71. [71] Romijn, H.J., Marle, J. van and Janszen, A.W.J.W. (1993): Permanent increase of the GAD67/ synaptophysin ratio in rat cerebral cortex nerve endings as a result of hypoxic-ischemic encephalopathy sustained in early postnatal life: a confocal laser scanning microscope study. Pediatr. Res., 630, 315-329.
72. [72] Rootwelt, T., Løberg, E.M., Moen, A., Øyasæter, S. and Saugstad, O.D. (1992): Hypoxemia and reoxygenation with 21% or 100% oxygen in newborn pigs: changes in blood pressure, base deficit, and hypoxanthine and brain morphology. Pediatr. Res., 32, 107-113.
73. [73] Sato, K., Morimoto, K., Ujike, H., Yamada, T., Yamada, N., Kuroda, S. and Hayabara, T. (1994): The effects of perinatal anoxia or hypoxia on hippocampal kindling development in rats. Brain Res. Bull., 35,167-170.
74. [74] Saxson, S.V. (1961): Effects of asphyxia neonatorum on behavior in rhesus monkeys. J. Genet. Psychol., 99, 277-282.
75. [75] Saxson, S.V. (1961): Behavioral defects in monkeys asphyxiated during birth. Exp. Neurol., 4, 460-469.
76. [76] Schwartz, P.M., Massarweh, W.F., Vinters, H.V. and Wasterlain, C.G. (1992): A rat model of severe hypoxic ischemic brain injury. Stroke, 23, 539-546.
77. [77] Schwegler, A. and Crusio, W.E. (1995): Psychomotor function in developing rats. J. Cereb. Blood Flow Metab., 15, 1032-1039.
78. [78] Sechzer, J.A. (1969): Memory deficits in monkey brain damaged by asphyxia neonatorum. Exp. Neurol., 24, 497-507.
79. [79] Seidler, F.J. and Slotkin, T.A. (1990): Effects of acute hypoxia on neonatal rat brain: regionally selective long term alterations in catecholamine levels and turnover. Brain Res. Bull., 24, 157-161.
80. [80] Sheldon, R.A., Patridge, J.C. and Ferriero, D.M. (1992): Postischemic hyperglycemia is not protective to the neonatal rat brain. Pediatr. Res., 32, 489-493.
81. [81] Silverstein, F. and Johnston, M.V. (1984): Effects of hypoxia ischemia on monoamine metabolism in the immature brain. Ann. Neurol., 15, 342-347.
82. [82] Silverstein, F.S., Chen, R. and Johnston, M.V. (1986): The glutamate analogue of quisqualic acid is neurotoxic in striatum and hippocampus of immature rat brain. Neurosci. Letters, 71, 13-18.
83. [83] Silverstein, F.S., Buchanan, K., Hudson, C. and Johnston, M.V. (1986): Flunarizine limits hypoxia-ischemia induced morphologic injury in immature rat brain. Stroke, 17, 477-482.
84. [84] Speiser, Z., Korczyn, A.D., Teplitzky, J. and Gitter, S. (1983): Hyperactivity in rats following postnatal anoxia. Behav. Brain Res., 7, 379-382.
85. [85] Tan, W.K.M., Williams, C.E., Gunn, A.J., Mallard, E.C. and Gluckman, P.D. (1993): Pretreatment with monosialoganglioside GM1 protects the brain of fetal sheep against hypoxic-ischemic injury without causing systemic compromise. Pediatr. Res., 34,18-22.
86. [86] Tan, W.K.M., Williams, C.E., Gunn, A.J., Mallard, E.C. and Gluckman, P.D. (1992): Suppression of postischemic epileptiform activity with MK-801 improves neural outcome in fetal sheep. Ann. Neurol., 32, 677-682.
87. [87] Tan, W.K.M., Williams, C.E., Mallard, E.C. and Gluckman, P.D. (1994): Monosialoganglioside GM1 treatment after a hypoxic-ischemic episode reduces the vulnerability of fetal sheep brain to subsequent injuries. Am. J. Obstet. Gynecol., 170, 663-670.
88. [88] Thordstein, M., Bagenholm, R., Thiringer, K. and Kjellmer, I. (1993): Scavengers of free oxygen radicals in combination with magnesium ameliorate perinatal hypoxic ischemic brain damage in the rat. Pediatr. Res., 34(1), 23-26.
89. [89] Towfighi. J., Yager, J.Y., Housman, C. and Vannucci, R.C. (1991): Neuropathology of remote hypoxic-ischemic damage in the immature rat. Acta Neuropathol., 81, 578-587.
90. [90] Towfighi, J., Housman, C., Heitjan, D.F., Vannucci, R.C. and Yager, JY. (1994): The effect of focal cerebral cooling on perinatal hypoxic-ischemic brain damage. Acta Neuropathol. (Berl), 87, 598-604.
91. [91] Tuor, U.I., Simone, C.S., Arellano, R., Tanswell, K. and Post, M. (1993): Glucocorticoid prevention of neonatal hypoxic-ischemic damage: role of hyperglycemia and antioxidant enzymes. Brain Res., 604, 165-172.
92. [92] Vannucci, R.C. (1993): Experimental models of perinatal hypoxic ischemic brain damage. Acta Pathologica, Microbiologica, et Immunologica Scandinavica, 40, 89-95.
93. [93] Volpe, J.J. (1995): Hypoxic ischemic encephalopathy: biochemical and physioloigcal aspects. In: Neurology of the Newborn, Third Edition, Philadelphia, W. B. Saudners, 211-313.
94. [94] Waizer, J., Baumbach, D.T., Berman, D. and Berman, A.J. (1972): Visual stimulation as a reinforcer in neonatally asphyxiated monkeys. J. Compar. Physiologic Psychol., 78, 386-390.
95. [95] Wasterlain, C.G., Adams, L.M., Schwartz, P.H., Hattori, H., Sofia, R.D. and Wichmann, J.K. (1993): Posthypoxic treatment with felbamate is neuroprotective in a rat model of hypoxia-ischemia. Neurology, 43, 2303-2310.
96. [96] William, C.E., Gunn, A.J., Synek, B. and Gluckman, P.D. (1990): Delayed seizures occurring with hypoxic-ischemic encephalopathy in the fetal sheep. Pediatr. Res., 27, 561-565.
97. 31P-NMR study in anesthetized immature rats. Neurosci. Lett., 170, 31-34.
98. [98] Windle, W.F. (1943): Asphyxia neonatorum: an experimental study in guinea pig. Am. J. Obstet. Gynecol., 45, 183-200.
99. [99] Windle, W.F., Becker, R.F. and Weil, A. (1944): Alterations in brain structure after asphyxiation at birth. J. Neuropath. Exp. Neurol., 3, 224-237.
100. [100] Xia, Y., Eisenman, D. and Haddad, G.G. (1993): Sulfonylurea receptor expression in rat brain: effect of chronic hypoxia during development. Pediatr. Res., 34, 634-641.
101. + channels increase in number in newborn rat brain after in utero hypoxia. Brain Res., 635, 339-344.
102. [102] Yager, J.Y., Heitjan, D.F., Towfighi, J. and Vannucci, R.C. (1992): Effect of insulin induced and fasting hypoglycemia on perinatal hypoxic-ischemic brain damage. Pediatr. Res., 31, 138-142.
103. [103] Yoshioka, H., Yoshida, A., Ochi, M., Iino, S., Fujiwara, K., Ishimura, K., Kusunoki, T. (1986): Granule cell deficit in mouse cerebellum after total asphyxia. Ann. Neurol., 19, 356-359.
104. [104] Young, R.S.K., Olenginski, T.P., Yagel, S.K. and Towfighi, J. (1983): The effects of graded hypothermia on hypoxic-ischemic brain damage: a neuropathologic study in the neonatal rat. Stroke, 14, 929-934.
105. [105] Young, R.S.K., Hessen, T.R., Pritchard, G.A. and Yagel, S.K. (1984): Naloxone exacerbates hypoxic-ischemic brain injury in the neonatal rat. Am. J. Obstet. Gynecol., 150, 52-56.