The effect of age on susceptibility to brain damage in a model of global hemispheric hypoxia-ischemia

Developmental Brain Research

Volumn 93, Issue 1-2, 1996, Pages 143-154

  Yager, Jerome Y ^a,b   Shuaib, Ashfaq ^a,b   Thornhill, Jim ^a,b  

^a ROYAL UNIVERSITY HOSPITAL   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Age; Brain damage; Development; Hypoxia ischemia; Stroke

Indexed keywords

ADOLESCENT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN DEVELOPMENT; BRAIN ISCHEMIA; CONTROLLED STUDY; DOPPLER FLOWMETRY; HIPPOCAMPUS; HISTOLOGY; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; STROKE;

EID: 0029888215     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/0165-3806(96)00026-0     Document Type: Article

References (92)

1. Andine, P., Sandberg, M., Bagenholm, R., Lehmann, A. and Hagberg, H., Intra-and extracellular changes of amino acids in the cerebral cortex of the neonatal rat during hypoxia-ischemia, Dev. Brain Res., 64 (1991) 115-120.
2. Auer, R.N., Excitotoxic mechanisms, and age-related susceptibility to brain damage in ischemia, hypoglycemia and toxic mussel poisoning, Neurotoxicology, 12 (1991) 541-546.
3. Benveniste, H., Drejer, J., Schousboe, A. and Diemer, N.H., Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis, J. Neurochem., 43 (1984) 1369-1374.
4. Bickler, P., E., Gallego, S.M. and Hansen, B.M., Developmental changes in intracellular calcium regulation in rat cerebral cortex during hypoxia, J. Cereb. Blood Flow Metab., 13 (1993) 811-819.
5. Bogousslavsky, J. and Pierre, P., Ischemic stroke in patients under age 45. In H.J.M. Barnett and V. Hachinski (Eds.), Neurologic Clinics: Cerebral Ischemia: Treatment and Prevention, 1992, Vol. 10, pp. 113-124.
6. Bogousslavsky, J., Van Melle, G. and Regli, F., The Lausanne Stroke Registry: analysis of 1000 consecutive patients with first stroke, Stroke, 19 (1988) 1083-1092.
7. Buchli, R., Martin, E., Boesiger, P. and Rumpel, H., Developmental changes of phosphorus metabolite concentrations in the human brain: a 31 P magnetic resonance spectroscopy study in vivo, Pediatr. Res., 35 (1994) 431-435.
8. Busto, R., Dietrich, D., Globus, MY-T. and Ginsberg, M., D., The importance of brain temperature in cerebral ischemic injury, Stroke, 20 (1989) 1113-1114.
9. Busto, R., Dietrich, W., D., Globus, MY-T., Valdes, I., Schenberg. P. and Ginsberg, M.D., Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury, J. Cereb. Blood Flow Metab., 7 (1987) 729-738.
10. Chugani, H.T. and Phelps, M.E., Maturational changes in cerebral function in infants determined by 5184FDG positron emission tomography. Science, 231 (1986) 840-843.
11. Chugani, H., T., Hovda. D.A., Villablanca, J.R., Phelps, M.E. and Xu, W-F., Metabolic maturation of the brain: a study of local cerebral glucose utilization in the developing cat, J. Cereb. Blood Flow Metab., 11 (1991) 35-47.
12. Chugani, H., T., Phelps, M.E. and Mazziotta, J.C., Positron emission tomography study of human brain functional development, Ann. Neurol., 22 (1987) 487-497.
13. Combs, D.J., Dempsey, R.J., Maley, M., Donaldson, D. and Smith, C., Relationship between plasma glucose, brain lactate and intracellular pH during cerebral ischemia in gerbils, Stroke, 21 (1990) 936-942.
14. Corbett, R., J.T., Laptook, A.R., Garcia, D. and Ruley, J.I., Cerebral acid buffering capacity at different ages measured in vivo by 31P and 1H nuclear magnetic resonance spectroscopy, J. Neurochem., 59 (1992) 216-226.
15. Dawes, G.S., Jacobson, H.M., Mott, J.C., Shelley, H.J., Some observations on foetal and newborn rhesus monkeys, J. Physiol., 152 (1960) 271-298.
16. Dirnagl, U., Kaplan, B., Jacewicz, M., Pulsinelli, W., Continuous measurement of cerebral cortical blood flow by laser-doppler flowmetry in a rat stroke model. J. Cereb. Blood Flow Metab., 9 (1989) 589-596.
17. Duffy, T.E., Kohle, S.J. and Vannucci, R.C., Carbohydrate and energy metabolism in perinatal rat brain: relation to survival in anoxia, J. Neurochem., 24 (1975) 271-276.
18. Duverger, D. and MacKenzie, E.T., The quantification of cerebral infarction following focal ischemia in the rat: influence of strain, arterial pressure, blood glucose concentration and age, J. Cereb. Blood Flow Metab., 8 (1988) 449-461.
19. Fazekas, J.F., Alexander, A.D. and Himich, H.E., Tolerance of the newborn to anoxia, Am. J. Physiol., 134 (1941) 281-287.
20. Gallyas, F., Wolff, J.R., Bottcher, H. and Zaborszky, L., A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol., 55 (1980) 299-306.
21. Gallyas, F., Wolff, J.R., Bottcher, H. and Zaborszky, L., A reliable method to localize axonal damage after axotomy, Stain Technol., 55 (1980) 291-297.
22. Glass, H., G., Snyder, F.F. and Webster, E., The rate of decline in resistance to anoxia of rabbits, dogs and guinea pigs from the onset of viability to adult life. Am. J. Physiol., 140 (1944) 609-615.
23. Haberl, R.L., Villringer, A. and Dirnagl, U., Applicability of Laser-Doppler flowmetry for cerebral blood flow monitoring in neurological intensive care, Acta Neurochir., 59 (1993) 64-68.
24. Hamon, B. and Heinemann, U., Developmental changes in neuronal sensitivity to excitatory amino acids in area CA1 of the rat hippocampus, Dev. Brain Res., 38 (1988) 286-290.
25. Harris, K.S. and Teyler, T.J., Developmental onset of long-term potentiation in area CA1 of the rat hippocampus, J. Physiol., 346 (1984) 27-48.
26. Hattori, H. and Wasterlain. C.G., Excitatory amino acids in the developing brain: ontogeny, plasticity, and excitotoxicity, Ped. Neurol., 6 (1990) 219-228.
27. Hattori, H. and Wasterlain, C.G., Post-hypoxic glucose supplement reduces hypoxic-ischemic brain damage in the neonatal rat, Ann. Neurol., 28 (1990) 122-128.
28. Himwich, H.E. and Fazekas, J.F., Comparative studies of the metabolism of brain in infant and adult dog, Am. J. Physiol., 132 (1941) 454-458.
29. Holler, T., Cappel, E., Klein, J. and Loffelholz, K., Glutamate activates phospholipase D in hippocampal slices of newborn and adult rats, J. Neurochem., 61 (1993) 1569-1572.
30. Ikonomidou, C., Mosinger, J.L. and Salles, S.K., Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-D-aspartate neurotoxicity, J. Neurosci., (1989) 2809-2818.
31. Jacobson, H.N. and Widdle, W.F., Responses of fetal and newborn monkeys to asphyxia, J. Physiol., 153 (1960) 447.
32. Jilek, L., Fischer, J., Virulich, L., Trojan, S., The reaction of the brain to stagnant hypoxia and anoxia during ontogeny, Prog. Brain Res., 9 (1964) 113-131.
33. Johnston, M.V., Cellular alterations associated with perinatal asphyxia. Clin. Invest. Med., 16 (1993) 122-132.
34. Juurlink, B.H.J., Hertz, L. and Yager, J.Y., Astrocyte maturation and susceptibility to ischemia or substrate deprivation, NeuroReport, 3 (1992) 1135-1137.
35. Kagstrom, E., Smith, M.L. and Siesjo, B.K., Local cerebral blood flow in the recovery period following complete cerebral ischemia in the rat, J. Cereb. Blood Flow Metab., 3 (1983) 170-182.
36. Kass, I.S. and Lipton, P., Protection of hippocampal slices from young rats against anoxic transmission damage is due to better maintenance of ATP, J. Physiol., 413 (1989) 1-11.
37. Kolb, B. and Gibb, R., Possible anatomical basis of recovery of function after neonatal frontal lesions rats, Behav. Neurosci., 107 (1993) 799-811.
38. Kolb, B. and Whishaw, I.Q., Earlier is not always better: behavioral dysfunction and abnormal cerebral morphogenesis following neonatal cortical lesions in the rat, Behav. Brain Res., 17 (1985) 25-43.
39. Kolb, B., Holmes, C., and Whishaw, I.Q., Recovery from early cortical lesions in rats. III. Neonatal removal of posterior parietal cortex has greater behavioral and anatomical effects than similar removals in adulthood, Behav. Brain Res., 26 (1987) 119-137.
40. Kolb, B. and Whishaw, I.Q., Plasticity in the neocortex: mechanisms underlying recovery from early brain damage, Prog. Neurobiol., 32 (1989) 235-276.
41. Kostic, V., Przedborski, S., Jackson-Lewis, V., Cadet, J.L. and Burke, R.E., Effect of unilateral perinatal hypoxic-ischemic brain injury in the rat on striatal muscarinic cholinergic receptors and high-affinity choline uptake sites: a quantitative autoradiographic study, J. Neurochem., 57 (1991) 1962-1970.
42. LeMay, D.R., Gehua, L., Zelenock, G.B. and D'Alecy, L.G., Insulin administration protects neurologic function in cerebral ischemia in rats. Stroke, 19 (1988) 1411-1419.
43. Levine, S., Anoxic-ischemic encephalopathy in rats, Am. J. Pathol., 36 (1960) 1-17.
44. Levy, D.E., Van Uitert, R.L., Pike, C.L., Delayed postischemic hypoperfusion: a potential damaging consequence of stroke, Neurology, 29 (1979) 1245-1252.
45. Lowry, O.H. and Passonneau, J. V., A Flexible System of Enzymatic Analysis, Academic Press. New York, 1972.
46. Marie, C. and Bralet, J., Blood glucose level and morphological brain damage following cerebral ischemia. Cerebrovasc. Brain Metabol. Rev., 3 (1991) 29-38.
47. McDonald, J.W. and Johnston, M.V., Physiological and pathophysiological roles of excitatory amino acids during central nervous system development, Brain Res. Rev., 15 (1990) 41-70.
48. McDonald, J.W., Silverstein, F.S. and Johnston, M.V., Neurotoxicity of N-methyl-D-aspartate is markedly enhanced in developing rat central nervous system. Brain Res., 459 (1988) 200-203.
49. McIlwain, H. and Bachelard, H.S., Chemical and enzymic make-up of the brain during development and ageing. In Biochemistry and the Central Nervous System, Williams and Wilkins, Baltimore, MD, 1971, pp. 371-412.
50. Meibach, R.C., Ross, D.A., Cox, R.D. and Glick, S.D., The ontogeny of hippocampal energy metabolism, Brain Res., 204 (1981) 431-435.
51. Myers, R.E., A unitary theory of causation of anoxic and hypoxic brain pathology. In S. Fahn, J.N. Davis, L.P. Rowland (Eds.), Cerebral Hypoxia and Its Consequences, Raven Press, New York, 1979, pp. 195-213.
52. Myers, R.E. and Yamaguchi, S., Nervous system effects of cardiac arrest in monkeys. Preservation of vision, Arch. Neurol., 34 (1977) 65-74.
53. Paschen, W., Djuricic, B., Mies, G., Schmidt-Kastner, R. and Linn, F., Lactate and pH in the brain: association and dissociation in different pathophysiological states, J. Neurochem., 48 (1987) 154-159.
54. Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, 2nd Edn., Academic Press, Sydney, 1986.
55. Pettigrew, J.W., Panchalingam, K., Withers, G., et al. Changes in brain energy and phospholipid metabolism during development and aging in the Fischer 344 rat, J. Neuropathol. Exp. Neurol., 49 (1990) 237-249.
56. Pokorny, J. and Yamamoto, T., Postnatal ontogenesis of hippocampal CA1 area in rats. Development of dendritic arborisation in pyramidal neurons, Brain Res. Bull., 7 (1981) 113-120.
57. Raichle, M.E., The pathophysiology of brain ischemia, Ann. Neurol., 13 (1983) 2-10.
58. Reeves, I., Mujsce, D. and Vannucci, R.C., Extreme hyperglycemia (HG) protects the perinatal brain from hypoxic-ischemic (H-I) brain damage, Pediatr. Res., 31 (1992) 352A.
59. Rehncrona, S., Rosen, I. and Siesjo, B.K., Brain lactic acidosis and ischemic cell damage: 1. Biochemistry and neurophysiology, J. Cereb. Blood Flow Metab., 1 (1981) 297-311.
60. Rehncrona, S., Rosen, I. and Siesjo, B.K., Excessive cellular acidosis: an important mechanism of neuronal damage in the brain?, Acta Physiol. Scand., 110 (1980) 435-437.
61. Rehncrona, S., Rosen. I. and Smith, M-L., Effect of different degrees of brain ischemia and tissue lactic acidosis on the short-term recovery of neurophysiologic and metabolic variables, Exp. Neurol., 87 (1985) 458-473.
62. Represa, A., Tremblay, E. and Ben-Ari, Y., Transient increase of NMDA binding sites in human hippocampal during development. Neurosci. Lett., 99 (1989) 61-66.
63. Rice, J.E., Vannucci, R.C. and Brierley, J.B., The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol., 9 (1981) 131-141.
64. Ridenour, T.R., Warner, D.S., Todd, M.M. and McAllister, A.C., Mild hypothermia reduces infarct size resulting from temporary but not permanent focal ischemia in rats, Stroke, 23 (1992) 733-738.
65. Rothman, S.M., Olney, J.W., Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol., 19 (1986) 105-111.
66. Salford, L.G., Plum, F. and Brierley, J.B., Graded hypoxia-oligemia in rat brain: neurological alterations and their implications, Arch. Neurol., 29 (1973) 234-238.
67. Schoenberg, B.S., Mellinger, J.F. and Schoenberg, D.G., Cerebrovascular disease in infants and children: A study of incidence, clinical features and survival, Neurology, 28 (1978) 763-768.
68. Sherwood, N.M. and Timiras, P.S. (Eds.), A Stereotaxic Atlas of the Developing Rat Brain, University of California Press, Los Angeles, CA, 1970.
69. Shuaib, A., Xu, K., Crain, B., Siren, A-L., Feuerstein, G., Hallenbeck, J. and Davis, J.N., Assessment of damage from implantation of microdialysis probes in the rat hippocampus with silver degeneration staining, Neurosci. Lett., 112 (1990) 149-154.
70. Siesjo, B., K., Agardh, C-D. and Bengtsson, F., Free radicals and brain damage, Cerebrovasc. Brain Metab. Rev., 1 (1989) 165-211.
71. Siesjo, B.K., Cell damage in the brain: a speculative synthesis, J. Cereb. Blood Flow Metab., 1 (1981) 155-185,.
72. Silverstein. F.S., Naik, B. and Simpson, J., Hypoxia-Ischemia stimulates hippocampal glutamate efflux in perinatal rat brain: an in vivo microdialysis study, Pediatr. Res., 30 (1991) 587-590.
73. 31P] NMR studies on the influence of age on rat brain hypoxia, Brain Res., 482 (1989) 1-11.
74. Thornhill, J. and Halvorson, I., Intrascapular brown adipose tissue (IBAT) temperature and blood flow responses following ventromedial hypothalamic stimulation to sham and IBAT-denervated rats, Brain Res., 615 (1993) 289-294.
75. Towfighi, J., Housman, C., Heitjan, D.F., Vannucci, R.C. and Yager J.Y., The effect of focal cerebral cooling on perinatal hypoxicischemic brain damage, Acta Neuropathol., 87 (1994) 598-604.
76. Towfighi, J., Yager, J.Y., Housman, C. and Vannucci, R.C., Neuropathology of remote hypoxic-ischemic damage in the immature rat, Acta Neuropathol., 81 (1991) 578-587.
77. Tremblay, E., Roisin, M.P., Represa, A., Charriaut-Marlangue, C. and Ben-Ari, Y., Transient increased density of NMDA binding sites in the developing rat hippocampus. Brain Res., 461 (1988) 393-396.
78. United States Department of Health, Education and Welfare, National Survey of Stroke. NIH publication No. 80-2069, 1980.
79. Vannucci, R.C., Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage, Pediatr. Res., 27 (1990) 317-326.
80. Vannucci, R.C. and Yager, J.Y., Glucose, lactic acid and perinatal hypoxic-ischemic brain damage, Ped. Neurol., 8 (1992) 3-12.
81. Voll, C.L. and Auer, R.N., Insulin attenuates ischemic brain damage independent of its hypoglycemic effect. J. Cereb. Blood Flow Metab., 11 (1991) 1006-1014.
82. Voll, C.L., Whishaw, I.Q. and Auer, R.N., Post-ischemic insulin reduces spatial learning deficit following transient forebrain ischemia. Stroke, 20 (1989) 646-651.
83. Volpe, J.J., Brain injury in the premature infant: is it preventable?, Pediatr. Res., 21 (1990) 528-533.
84. Voorhies, T.M., Rawlinson, D. and Vannucci, R.C., Glucose and perinatal hypoxic-ischemic brain damage in the rat, Neurology, 36 (1986) 1115-1118.
85. Welsh, F.A., Ginsberg, M.D., Rieder, W. and Budd, W.W., Deleterious effect of glucose pretreatment on recovery from diffuse cerebral ischemia in the cat. II. Regional metabolite levels. Stroke, 11 (1980) 355-363.
86. Welsh, F.A., Sims, R.E. and Harris, V.A., Mild hypothermia prevents ischemic injury in gerbil hippocampus, J. Cereb. Blood Flow Metab., 10 (1990) 557-563.
87. Welsh, F.A., Vannucci, R.C. and Brierley, J.B., Columnar alterations of NADH fluorescence during hypoxia-ischemia in immature rat brain, J. Cereb. Blood Flow Metab., 2 (1982) 221-228.
88. Yager, J.Y., Brucklacher, R.M. and Vannucci, R.C., Cerebral oxidative metabolism and redox state during hypoxia-ischemia and early recovery in the immature rat, Am. J. Physiol., 262 (1991) H1 102-H1 108.
89. Yager, J.Y., Heitjan, D.F., Towfighi, J. and Vannucci, R.C., Effect of insulin induced and fasting hypoglycemia on perinatal hypoxicischemic brain damage, Pediatr. Res., 31 (1992) 138-142.
90. Yager, J.Y., Towfighi, J. and Vannucci, R.C., Influence of mild hypothermia on hypoxic-ischemic brain damage in the immature rat, Pediatr. Res., 34 (1993) 525-529.
91. Young, R.S.K., Petroff, O.A.C., Chen, B., Aquila, W.J. and Gore, J.C., Preferential utilization of lactate in neonatal dog brain: in vivo and in vitro proton NMR study, Biol. Neonate, 59 (1991) 46-53.
92. Zhang, J-R., Andrus, P.K. and Hall, E.D., Age-related regional changes in hydroxyl radical stress and antioxidants in gerbil brain, J. Neurochem., 61 (1993) 1640-1647.