Background Review and Current Concepts of Reperfusion Injury

Archives of Neurology

Volumn 47, Issue 11, 1990, Pages 1245-1254

  Hallenbeck, John M ^a   Dutka, Andrew J ^a  

^a WALTER REED ARMY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOT LYSIS; BRAIN ISCHEMIA; HUMAN; ISCHEMIC HEART DISEASE; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW;

CALCIUM; CHOLESTEROL; FREE RADICALS; HUMAN; LEUKOCYTES; OXYGEN; REPERFUSION INJURY; SUPPORT, U.S. GOV'T, NON-P.H.S.; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0025165826     PISSN: 00039942     EISSN: 15383687     Source Type: Journal    
DOI: 10.1001/archneur.1990.00530110107027     Document Type: Article

References (132)

1. Heiss W-D, Rosner G. Functional recovery of cortical neurons as related to degree and duration of ischemia. Ann Neurol. 1983;14:294-301.
2. Reimer KA, Jennings RB. The ‘wavefront phenomenon’ of myocardial ischemic cell death, II: transmural progression of necrosis within the framework of ischemic bed size (myocardium at risk) and collateral flow. Lab Invest. 1979;40:633-644.
3. Braunwald E, Kloner RA. Myocardial reperfusion: a double-edged sword? J Clin Invest. 1985;76:1713-1719.
4. Weisfeldt ML. Reperfusion and reperfusion injury. Clin Res. 1987;35:13-20.
5. Jennings RB, Sommers HM, Smyth GA, Flack HA, Linn H. Myocardial necrosis induced by temporary occlusion of a coronary artery in the dog. Pathology. 1960;70:68-78.
6. Bulkley BH, Hutchins GM. Myocardial consequences of coronary artery bypass graft surgery: the paradox of necrosis in areas of revascularization. Circulation. 1977;56:906-913.
7. Greene HL, Weisfeldt ML. Determinants of hypoxic and post-hypoxic myocardial contracture. Am J Physiol. 1977;232:H526-H533.
8. Shine KI, Douglas AM. Low calcium reperfusion of ischemic myocardium. J Mol Cell Cardiol. 1983;15:251-260.
9. DiBona DR, Powell WJ Jr. Quantitative correlation between cell swelling and necrosis in myocardial ischemia in dogs. Circ Res. 1980;47:653-665.
10. Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA, Lucchesi BR. Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation. 1983;67:1016-1023.
11. Rowe GT, Manson NH, Caplan M, Hess ML. Hydrogen peroxide and hydroxyl radical mediation of activated leukocyte depression of cardiac sarcoplasmic reticulum. Circ Res. 1983;53:584-591.
12. Ames A, Wright RL, Kowada M, et al. Cerebral ischemia, II: the no-reflow phenomenon. Am J Pathol. 1968;52:437-447.
13. Leaf A. Regulation of intracellular fluid volume and disease. Am J Med. 1970;49:291-295.
14. Fischer EG. Impaired perfusion following cerebrovascular stasis: a review. Arch Neurol. 1972;29:361-366.
15. Ginsberg MD, Myers RE. The topography of impaired microvascular perfusion in the primate brain following total circulatory arrest. Neurology. 1972;22:998-1011.
16. Hossmann KA, Sato K. Recovery of neuronal function after prolonged cerebral ischemia. Science. 1970;168:375-376.
17. Hossmann KA, Kleihues P. Reversibility of ischemic brain damage. Arch Neurol. 1973;29:375-384.
18. Brierley JB, Meldrum BS, Brown AW. The threshold and neuropathology of cerebral ‘anoxic-ischemic’ cell change. Arch Neurol. 1973;29:367-374.
19. Levy DE, Brierley JB, Plum F. Ischaemic brain damage in the gerbil in the absence of ‘no-reflow.’ J Neurol Neurosurg Psychiatry. 1975;38:1197-1205.
20. Harrison MJG, Sedal L, Arnold J, Russell RWR. No-reflow phenomenon in the cerebral circulation of the gerbil. J Neurol Neurosurg Psychiatry. 1975;38:1190-1193.
21. Halsey JH Jr, Ganji S, Erdmann W, Mardis HM. Studies in cerebral ischemia. Microvasc Res. 1977;13:363-370.
22. Hallenbeck JM. Prevention of postischemic impairment of microvascular perfusion. Neurology. 1977;27:3-10.
23. Levy DE, van Uitert RL, Pike CL. Delayed postischemic hypoperfusion: a potentially damaging consequence of stroke. Neurology. 1979;29:1245-1252.
24. Pulsinelli WA, Levy DE, Duffy TE. Regional cerebral blood flow and glucose metabolism following transient forebrain ischemia. Ann Neurol. 1982;11:499-509.
25. Siesjo BK. Cell damage in the brain: a speculative synthesis. J Cereb Blood Flow Metab. 1981;1:155-185.
26. Schanne FAX, Kane AB, Young EE, Faber JL. Calcium dependence of toxic cell death: a final common pathway. Science. 1979;206:700-702.
27. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol. 1982;11:491-498.
28. Smith M-L, Auer RN, Siesjo BK. The density and distribution of ischemic brain injury in the rat following 2-10 min of forebrain ischemia. Acta Neuropathol (Berl). 1984;64:319-332.
29. Rothman SM, Olney JW. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol. 1986;19:105-111.
30. Novelli A, Reilly JA, Lysko PG, Henneberry RC. Glutamate becomes neurotoxic via the N-methyl D-aspartate receptor when intracellular energy levels are reduced. Brain Res. 1988;451:205-212.
31. DeWood MA, Spores J, Notske R. Prevalence of total coronary occlusion during the early hours of transmural myocardial infarction. N Engl J Med. 1980;303:897-902.
32. Laffel GL, Braunwald E. Thrombolytic therapy: a new strategy for the treatment of acute myocardial infarction. N Engl J Med. 1984;311:710-717.
33. The thrombolysis in myocardial infarction study group. N Engl J Med. 1985;312:932-936.
34. Del Zoppo GJ. Thrombolytic therapy in cerebrovascular disease. Stroke. 1988;19:1174-1179.
35. Ryan US, Ryan JW, Crutchley DJ. The pulmonary endothelial surface. FASEB J. 1985;44:2603-2609.
36. Ryan US, Ryan JW. Surface properties of pulmonary endothelial cells. Ann NY Acad Sci. 1983;416:441-456.
37. Dietrich WD, Busto R, Ginsberg MD. Cerebral endothelial microvilli: formation following global forebrain ischemia. J Neuropathol Exp Neurol. 1984;43:72-83.
38. Clouse LH, Comp PC. The regulation of hemostasis: the protein C system. N Engl J Med. 1986;314:1298-1304.
39. Esmon CT. The regulation of natural anticoagulant pathways. Science. 1987;235:1348-1352.
40. Bachmann F, Egbert IR, Kruithof KO. Tissue plasminogen activator: chemical and physiological aspects. Semin Thromb Hemost. 1984;10:6-17.
41. Verstraete M, Collen D. Thrombolytic therapy in the 80's. Blood. 1986;67:1529-1541.
42. Stern D, Nawroth P, Marcum J, et al. Interaction of antithrombin III with bovine aortic segments: role of heparin in binding and enhanced anticoagulant activity. J Clin Invest. 1985;75:272-279.
43. Moncada S. Prostacyclin and arterial wall biology. Arteriosclerosis. 1982;2:193-207.
44. Crutchley DJ, Ryan US, Ryan JW. Effects of aspirin and dipyridamole on the degradation of adenosine diphosphate by cultured cells derived from bovine pulmonary artery. J Clin Invest. 1980;66:29-35.
45. Becker CG, Harpel PC. Alpha 2-macroglobulin on human vascular endothelium. J Exp Med. 1976;144:1-9.
46. Rosenblum WI. Biology of disease: aspects of endothelial malfunction and function in cerebral microvessels. Lab Invest. 1986;55:252-268.
47. Brox JH, Osterud B, Bjorklid E, Fenton JW II. Production and availability of thromboplastin in endothelial cells: the effects of thrombin, endotoxin and platelets. Br J Haematol. 1984;57:239-246.
48. Bevilacqua MP, Pober JS, Majeau GR, Cotran RS, Gimbrone MA Jr. Interleukin-1 (IL-1) induces biosynthesis and cell surface expression of procoagulant activity in human vascular endothelial cells. J Exp Med. 1984;160:618-623.
49. Lyberg T, Galdal KS, Evensen SA, Prydz H. Cellular cooperation in endothelial cell thromboplastin synthesis. Br J Haematol. 1983;53:85-95.
50. Libby P, Ordovas JM, Auger KR, Robbins AH, Birinyi LK, Dinarello CA. Endotoxin and tumor necrosis factor induce interleukin-1 gene expression in adult human vascular endothelial cells. Am J Pathol. 1986;124:179-185.
51. Bussolino F, Brevario F, Tetta C, Aglietta M, Mantouani A, Dejana E. Interleukin-1 stimulates platelet-activating factor production in cultured human endothelial cells. J Clin Invest. 1986;77:2027-2033.
52. Nawroth PP, Handley DA, Esmon CT, Stern DM. Interleukin-1 induces endothelial cell procoagulant while suppressing cell surface anticoagulant activity. Proc Natl Acad Sci U S A. 1986;83:3460-3464.
53. Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA Jr. Interleukin-1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes and related leukocyte cell lines. J Clin Invest. 1985;76:2003-2011.
54. Bevilacqua MP, Wheeler ME, Pober JS, et al. Endothelial-dependent mechanisms of leukocyte adhesion: regulation by interleukin-1 and tumor necrosis factor. In: Movat HZ, ed. Leukocyte Emigration and Its Sequelae, Satellite Symposium: Sixth International Congress on Immunology, Toronto, Ontario. Basel, Switzerland: S. Karger; 1986:79-93.
55. Pober JS, Lapierre LA, Stolpen AH, et al. Activation of cultured human endothelial cells by recombinant lymphotoxin: comparison with tumor necrosis factor and interleukin 1 species. J Immunol. 1987;138:3319-3324.
56. Marks RM, Todd RF III, Ward PA. Rapid induction of neutrophil-endothelial adhesion by endothelial complement fixation. Nature. 1989;339:314-317.
57. Strieter RM, Kunkel SL, Showell HJ, et al. Endothelial cell gene expression of a neutrophil chemotactic factor by TNF-α, LPS, and IL-1β. Science. 1989;243:1467-1469.
58. Wiggins RC, Loskutoff DJ, Cochrane CJ, Griffin JH, Edgington TS. Activation of rabbit Hageman Factor by homogenates of cultured rabbit endothelial cells. J Clin Invest. 1980;65:197-206.
59. Loesberg C, Gonsalves MD, Zandbergen J, et al. The effect of calcium on the secretion of factor VIII-related antigen by cultured human endothelial cells. Biochim Biophys Acta. 1983;763:160-168.
60. Levine JD, Harlan JM, Harker LA, Joseph ML, Counts RB. Thrombin-mediated release of factor VIII antigen from human umbilical vein endothelial cells in culture. Blood. 1982;60:531-534.
61. Ingerman-Wojenski C, Silver MJ, Smith JV, Macarak E. Bovine endothelial cells in culture produce thromboxane as well as prostacyclin. J Clin Invest. 1981;67:1292-1296.
62. Piper PJ, Galton SA. Generation of leukotriene B-4 and leukotriene E-4 from porcine pulmonary artery. Prostaglandins. 1984;28:905-914.
63. Samuelsson B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation. Science. 1983;220:568-575.
64. Braquet P, Touqui L, Shen TY, Vargaftig BB. Perspectives in platelet-activating factor research. Pharmacol Rev. 1987;39:97-145.
65. McIntyre TM, Zimmerman GA, Satoh K, Prescott SM. Cultured endothelial cells synthesize both platelet-activating factor and prostacyclin in response to histamine, bradykinin, and adenosine triphosphate. J Clin Invest. 1985;76:271-280.
66. Camussi G, Aglietta M, Malavasi F, et al. The release of platelet-activating factor from human endothelial cells in culture. J Immunol. 1983;131:2397-2403.
67. Dubois C, Bissonnette E, Rola-Pleszczynski M. Platelet-activating factor (PAF) enhances tumor necrosis factor production by alveolar macrophages: prevention by PAF receptor antagonists and lipoxygenase inhibitors. J Immunol. 1989;143:964-970.
68. Rodgers GM, Shuman MA. Prothrombin is activated on vascular endothelial cells by Factor Xa and calcium. Proc Natl Acad Sci U S A. 1983;80:7001-7005.
69. Stern DM, Drillings M, Kisiel W, Nawroth P, Nossel HL, LaGamma KS. Activation of Factor IX bound to cultured bovine aortic endothelial cells. Proc Natl Acad Sci USA. 1984;81:913-917.
70. Cerveny TJ, Fass DN, Mann KG. Synthesis of coagulation factor V by cultured aortic endothelium. Blood. 1984;63:1467-1474.
71. Van Mourik JA, Lawrence DA, Loskutoff DJ. Purification of an inhibitor of plasminogen activator (antiactivator) synthesized by endothelial cells. J Biol Chem. 1984;259:14914-14921.
72. Juhan-Vague I, Moerman B, De Cock F, Aillaud MF, Collen D. Plasma levels of a specific inhibitor of tissue-type plasminogen activator (and urokinase) in normal and pathological conditions. Thromb Res. 1984;33:523-530.
73. Angleton P, Chandler WL, Schmer G. Diurnal variation in tissue plasminogen activator and its rapid inhibitor. Circulation. 1987;76(suppl 4):339.
74. Matsubara T, Ziff M. Superoxide anion release by human endothelial cells: synergism between a phorbol ester and a calcium ionophore. J Cell Physiol. 1986;127:207-210.
75. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980;288:373-376.
76. Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524-526.
77. Radomski MW, Palmer RMJ, Moncada S. Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium. Lancet. 1987;2:1057-1058.
78. Yanagisawa M, Kurihara H, Kimura S, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332:411-415.
79. Zimmerman ANE, Hulsmann WC. Paradoxical influence of calcium ions on the permeability of cell membranes of the isolated rat heart. Nature. 1966;211:646-647.
80. Young W. Ca paradox in neural injury: a hypothesis. Central Nervous System Trauma. 1986;3:235-251.
81. Braunwald E. Mechanism of action of calcium-channel-blocking agents. N Engl J Med. 1982;307:1618-1627.
82. White BC, Winegar CD, Wilson RF, Hoehner PJ, Trombley JH Jr. Possible role of calcium blockers in cerebral resuscitation: a review of the literature and synthesis for future studies. Crit Care Med. 1983;11:202-207.
83. Murphy JG, Marsh JD, Smith TW. The role of calcium in ischemic myocardial injury. Circulation. 1987;75(suppl 5):V15-V24.
84. Siesjo BK, Bengtsson F. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J Cereb Blood Flow Metab. 1989;9:127-140.
85. Uematsu D, Greenberg JH, Reivich M, Karp A. In vivo measurement of cytosolic free calcium during cerebral ischemia and reperfusion. Ann Neurol. 1988;24:420-428.
86. Steenbergen C, Murphy E, Levy L, London RE. Elevation in cytosolic free calcium concentration early in myocardial ischemia in perfused rat heart. Circ Res. 1987;60:700-707.
87. Nakayami H, Ginsberg MD, Dietrich WD. (S-emopamil), a novel calcium channel blocker and serotonin S2 antagonist, markedly reduces infarct size following middle cerebral artery occlusion in the rat. Neurology. 1988;38:1667-1673.
88. Grotta JC, Pettigrew LC, Rosenbaum D, Reid C, Rhoades H, McCandless D. Efficacy and mechanism of action of a calcium channel blocker after global cerebral ischemia in rats. Stroke. 1988;19:447-454.
89. Cheung JY, Bonventre JV, Malis CD, Leaf A. Calcium and ischemic injury. N Engl J Med. 1986;314:1670-1676.
90. Del Maestro RF. An approach to free radicals in medicine and biology. Ada Physiol Scand Suppl. 1980;492:153-168.
91. Halliwell B, Gudteridge JMC. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J. 1984;219:1-14.
92. Southorn PA, Powis G. Free radicals in medicine, I: chemical nature and biologic reactions. Mayo Clin Proc. 1988;63:381-389.
93. McCord JM. Oxygen-derived radicals: a link between reperfusion injury and inflammation. FASEB J. 1987;6:2402-2406.
94. Fantone JC, Ward PA. Role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. Am J Pathol. 1982;107:397-418.
95. Kinuta Y, Kimura M, Itokawa Y, Ishikawa M, Kikuchi H. Changes in xanthine oxidase in ischemic rat brain. J Neurosurg. 1989;71:417-420.
96. Patt A, Harken AH, Burton LK, et al. Xanthine oxidase-derived hydrogen peroxide contributes to ischemia reperfusion-induced edema in gerbil brains. J Clin Invest. 1988;81:1556-1562.
97. Kontos HA. Oxygen radicals in cerebral vascular injury. Circ Res. 1985;57:508-516.
98. Harlan JM. Neutrophil-mediated vascular injury. Acta Med Scand. 1987;715(suppl):123-129.
99. Schmid-Schonbein GW. Capillary plugging by granulocytes and the no-reflow phenomenon in the microcirculation. FASEB J. 1987;46:2397-2401.
100. Engler RL, Schmid-Schonbein GW, Pavelec RS. Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog. Am J Pathol. 1983;111:98-111.
101. Weissmann G, Smolen JE, Korghak HM. Release of inflammatory mediators from stimulated neurophils. N Engl J Med. 1980;303:27-34.
102. Moncada S, Higgs EA. Arachidonate metabolism in blood cells and the vessel wall. Clin Haematol. 1986;15:273-292.
103. Berenberg JL, Ward PA. Chemotactic factor inactivator in normal human serum. J Clin Invest. 1973;52:1200-1206.
104. Wright DG, Gallin JI. A functional differentiation of human neutrophil granules: generation of C5a by a specific (secondary) granule product and inactivation of C5a by azurophil (primary) granule products. J Immunol. 1977;119:1068-1076.
105. Clark RA, Klebanoff SJ. Chemotactic factor inactivation by the myeloperoxidase-hydrogen peroxide-halide system. J Clin Invest. 1979;64:913-920.
106. Blank ML, Lee T, Fitzgerald V, Snyder F. A specific acetylhydrolase for 1-alkyl-2-acetylsn-glycero-3-phosphocholine (a hypotensive and platelet-activating lipid). J Biol Chem. 1981;256:175-178.
107. Travis J, Giles PJ, Porcelli L, Reilly CF, Baugh R, Powers J. Human leucocyte elastase and cathepsin G: structural and functional characteristics. Ciba Found Symp. 1979;75:51-68.
108. Goldstein IM, Kaplan HB, Edelson HS, Weissmann G. Ceruloplasmin: a scavenger of superoxide anion radicals. J Biol Chem. 1979;254:4040-4045.
109. Stroncek DF, Vercellotti GM, Huh PW, Jacob HS. Neutrophil oxidants inactivate alpha-1 protease inhibitor and promote PMN-mediated detachment of cultured endothelium: protection by free methionine. Arteriosclerosis. 1986;6:332-340.
110. Seeger W, Suttorp N, Schmidt F, Neuhof H. The glutathione redox cycle as a defense system against hydrogen-peroxide-induced prostanoid formation and vasoconstriction in rabbit lungs. Am Rev Respir Dis. 1986;133:1029-1036.
111. Harlan JN, Levine JD, Callahan KS, Schwartz BR. Glutathione redox cycle protects cultured endothelial cells against lysis by extracellularly generated hydrogen peroxide. J Clin Invest. 1984;73:706-713.
112. Smith CW, Rothlein R, Hughes BJ, et al. Recognition of an endothelial determinant for CD 18-dependent human neutrophil adherence and transendothelial migration. J Clin Invest. 1988;82:1746-1756.
113. Dustin ML, Staunton DE, Springer TA. Supergene families meet in the immune system. Immunol Today. 1988;9:213-215.
114. Harlan JM, Schwartz BR, Wallis WJ, Pohlman TH. The role of neutrophil membrane proteins in neutrophil emigration. In: Movat HZ, ed. Leukocyte Emigration and Its Sequelae, Satellite Symposium: Sixth International Congress on Immunology, Toronto, Ontario. Basel, Switzerland: S. Karger; 1986;94-104.
115. Engler RL, Dahlgren MD, Morris DD, Peterson MA, Schmid-Schönbein GW. Role of leukocytes in response to acute myocardial ischemia and reflow in dogs. Am J Physiol. 1986;251(Heart Circ Physiol 20):H314-H322.
116. Engler RL, Dahlgren MD, Peterson MA, Dobbs A, Schmid-Schönbein GW. Accumulation of polymorphonuclear leukocytes during 3-h experimental myocardial ischemia. Am J Physiol. 1986;251(Heart Circ Physiol 20):H93-H100.
117. Engler R. Consequences of activation and adenosine-mediated inhibition of granulocytes during myocardial ischemia. FASEB J. 1987;46:2407-2412.
118. Hallenbeck JM, Dutka AJ, Tanishima T, et al. Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke. 1986;17:246-253.
119. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med. 1989;320:365-376.
120. Test ST, Lampert MB, Ossanna PJ, Thoene JG, Weiss SJ. Generation of nitrogen-chlorine oxidants by human phagocytes. J Clin Invest. 1984;74:1341-1349.
121. Smith JL, Drennan AM, Rettie T, Campbell W. Experimental observations on the antiseptic action of hypochlorous acid and its application to wound treatment. BMJ. 1915;2:129-136.
122. Janoff A. Elastase in tissue injury. Ann Rev Med. 1985;36:207-216.
123. Travis J, Salvesen GS. Human plasma proteinase inhibitors. Annu Rev Biochem. 1983;52:655-709.
124. Weiss SJ, Peppin GJ. Collagenolytic metalloenzymes of the human neutrophil: characteristics, regulation and potential function in vivo. Biochem Pharmacol. 1986;35:3189-3197.
125. Weiss SJ, Peppin G, Ortiz X, Ragsdale C, Test ST. Oxidative autoactivation of latent collagenase by human neutrophils. Science. 1985;227:747-749.
126. Glauser FL, Fairman RP. The uncertain role of the neutrophil in increased permeability pulmonary edema. Chest. 1985;88:601-607.
127. Tilton RG, Cole PA, Zions JD, et al. Increased ischemia-reperfusion injury to the heart associated with short-term diet-induced hypercholesterolemia in rabbits. Circ Res. 1987;60:551-559.
128. Golino P, Maroko PR, Carew TE. The effect of acute hypercholesterolemia on myocardial infarct size and the no-reflow phenomenon during coronary occlusion-reperfusion. Circulation. 1987;75:292-298.
129. Golino P, Maroko PR, Carew TE. Efficacy of platelet depletion in counteracting the detrimental effect of acute hypercholesterolemia on infarct size and the no-reflow phenomenon in rabbits undergoing coronary artery occlusionreperfusion. Circulation. 1987;76:173-180.
130. Joris I, Zand T, Nunnari JJ, Krolikowski FJ, Majno G. Studies on the pathogenesis of atherosclerosis, I: adhesion and emigration of mononuclear cells in the aorta of hypercholesterolemic rats. Am J Pathol. 1983;113:341-358.
131. Ratnoff OD. Some relationships among hemostasis, fibrinolytic phenomena, immunity, and the inflammatory response. Adv Immunol. 1969;10:145-227.
132. Siesjo BK. Historical overview: calcium, ischemia, and death of brain cells. Ann NY Sci. 1988;522:638-661.