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January 1984, Vol 119, No. 1 >
ARTICLE | January 1984

Role of Oxygen Radicals in Endotoxin-Induced Lung Injury FREE

Catherine Wong, MD; John Flynn, PhD; Robert H. Demling, MD
[+] Author Affiliations

Accepted for publication Sept 7, 1983.

Read before the Third Annual Meeting of the Surgical Infection Society, Fort Lauderdale, Fla, May 10, 1983.

Reprint requests to Longwood Area Trauma Center, 75 Francis St, Boston, MA 02115 (Dr Demling).


Arch Surg. 1984;119(1):77-82. doi:10.1001/archsurg.1984.01390130059011
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• We tested the hypothesis that the increased permeability in the pulmonary microcirculation seen with endotoxin is caused by the release of oxygen radicals from activated neutrophils. We first compared the pulmonary injury in sheep caused by low-dose endotoxin with that produced by phorbol myristate acetate, an agent that selectively causes the release of oxygen radicals from neutrophils. We then determined the degree of lung tissue lipid peroxidation, a reflection of direct oxygen radical damage after endotoxin and phorbol myristate acetate. Both agents produced a nearly identical increase in protein permeability; however, peroxidation was only evident with phorbol myristate acetate. Higher doses of endotoxin did result in increased lung peroxidation as well as a more severe physiologic injury. We can conclude that oxygen radical release, most likely from neutrophils, occurs with endotoxin. However, the permeability injury may not be the direct result of increased lipid peroxidation, as increased permeability can be seen without measurable increases in this parameter.

(Arch Surg 1984;119:77-82)

REFERENCES

1 +
Ley K, Arfors K:  Changes in macromolecular permeability by intravascular generation of oxygen-derived free radicals . Microvasc Res 1982;;24:25-33.
2 +
Martin W, Gadek J, Hunninghake G, et al:  Oxidant injury of lung parenchymal cells . J Clin Invest 1981;;68:1277-1288.
3 +
Mustafa M, Tierney D:  Biochemical and metabolic changes in the lung with oxygen, ozone, and nitrogen dioxide toxicity . Am Rev Respir Dis 1978;;118:1061-1073.
4 +
Shasby DM, Van Bethingsen KM, Tato RM, et al:  Granulocytes mediate acute edematous lung injury in rabbits and in isolated rabbit lungs perfused with PMA: Role of O2 radicals . Am Rev Respir Dis 1982;;125: 443-447.
5 +
Fong KL, McCay P, Poyer J, et al:  Evidence that peroxidation of lysosomal membranes is initiated by hydroxyl free radicals produced during flavin enzyme activity . J Biol Chem 1973;;248:7792-7797.
6 +
Chow CK, Tappel AL:  An enzymatic protective mechanism against lipid peroxidation damage to lungs of ozone-exposed rats . Lipids 1972;;7: 518-524.
7 +
Sakaguchi S, Kanda N, Hsu C, et al:  Lipid peroxide formation and membrane damage in endotoxin-poisoned mice . Microbiol Immunol 1981;; 25:229-244.
8 +
Brown RE, Craver R, Drake RM:  Lipid peroxidation and pulmonary hyaline membranes of the newborn . Ann Clin Lab Sci 1981;;11:25-34.
9 +
Yasaka T, Ohya I, MatsumotoJ, et al:  Acceleration of lipid peroxidation in human paraquat poisoning . Arch Intern Med 1981;;141:1169-1171.
10 +
Heflin C, Brigham KL:  Prevention by granulocyte depletion of increased lung vascular permeability of sheep lung after endotoxemia . J Clin Invest 1981;;68:1253-1262.
11 +
Smith ME, Gunther R, Demling RH:  Leukocytes, platelets, and thromboxane A2 in endotoxin induced lung injury . Surgery 1981;;90:102-107.
12 +
Demling RH, Proctor R, Starling J:  Lung injury and lung lysosomal enzyme release during endotoxemia . J Surg Res 1981;;30:135-141.
13 +
Sacks T, Moldow F, Craddock PR:  Oxygen radicals mediate endothelial cell damage by complement stimulated granulocytes: An in vitro model of immune vascular damage . J Clin Invest 1978;;61:1161-1167.
14 +
O'Flaherty J, Cousant S, Lineberger S, et al:  Phorbol myristate acetate: In vivo effects upon neutrophils, platelets, and lung . Am J Pathol 1980;;101:79-92.
15 +
Loyd J, Newman J, English D, et al:  Lung vascular effects of phorbol myristate acetate in awake sheep . J Appi Physiol 1983;;54:267-276.
16 +
Demling RH:  Role of prostaglandins in acute microvascular injury . Ann NY Acad Sci 1982;;284:517-534.
17 +
Demling RH, Smith M, Gunther R, et al:  Pulmonary injury and prostaglandin production during endotoxemia in conscious sheep . Am J Physiol 1981;;240:348-353.
18 +
Erdmann JA, Vaughn TR, Brigham KL, et al:  Effect of increased vascular pressure on lung fluid balance in unanesthetized sheep . Circ Res 1975;;28:271-276.
19 +
VreimCE, SnashallPD, DemlingRH, et al:  Lung and free interstitial fluid protein composition in sheep with edema . Am J Physiol 1976;;230: 1650-1653.
20 +
Staub NC, Bland RD, Brigham KL, et al:  Preparation of chronic lung lymph fistulas in sheep . J Surg Res 1975;;19:315-321.
21 +
Unger WC, Stanford TF, Benett H:  Extraction of prostaglandins from human blood . Nature 1971;;233:336-337.
22 +
Pearce ML, Yamashita J, Beasell J:  Measurement of pulmonary edema . Circ Res 1965;;16:482-488.
23 +
Brigham KL, Bowers RE, Haynes J:  Increased sheep lung vascular permeability caused by Escherichia coli endotoxin . Circ Res 1979;;45: 292-297.
24 +
Sibbald WT, Peterson M, Halliday RL, et al:  Pulmonary hypertension in sepsis . Chest 1978;;75:583-593.
25 +
Anderson RR, Holliday RL, Driedger AA, et al:  Documentation of pulmonary capillary permeability in the adult respiratory distress syndrome accompanying human sepsis . Am Rev Respir Dis 1979;;119:869-878.
26 +
Brigham KL, Owen PJ, Bowers RE:  Increased permeability of sheep lung vessels to proteins after pseudomonas bacteremia . Microvasc Res 1976;;11:415-421.
27 +
Parralt JR, Coker SJ, Hughes B:  The possible role of prostaglandins and thromboxanes in the pulmonary consequences of experimental endotoxin shock and clinical sepsis ; in McConn R (ed): Role of Chemical Mediators in the Pathophysiology of Acute Illness and Injury . New York, Raven Press, 1982;, pp 195-218.
28 +
Newman JH, Loyd J, Ogletree M, et al:  Effects of meclofenamate on the pulmonary vascular response to PMA , abstracted. Am Rev Respir Dis 1982;;124:282.
29 +
McCord JM:  Oxygen free radicals: Release and activities: A superoxide activated chemotactic factor and its role in the inflammatory process . Agents Actions 1980;;10:522-527.
30 +
Allen RC:  Free-radical production by reticulo endothelial cells , in Sharra A, Strauss R (eds): The Reticulo Endothelial System . New York, Plenum Publishing, 1980;, pp 309-337.

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1 +
Ley K, Arfors K:  Changes in macromolecular permeability by intravascular generation of oxygen-derived free radicals . Microvasc Res 1982;;24:25-33.
2 +
Martin W, Gadek J, Hunninghake G, et al:  Oxidant injury of lung parenchymal cells . J Clin Invest 1981;;68:1277-1288.
3 +
Mustafa M, Tierney D:  Biochemical and metabolic changes in the lung with oxygen, ozone, and nitrogen dioxide toxicity . Am Rev Respir Dis 1978;;118:1061-1073.
4 +
Shasby DM, Van Bethingsen KM, Tato RM, et al:  Granulocytes mediate acute edematous lung injury in rabbits and in isolated rabbit lungs perfused with PMA: Role of O2 radicals . Am Rev Respir Dis 1982;;125: 443-447.
5 +
Fong KL, McCay P, Poyer J, et al:  Evidence that peroxidation of lysosomal membranes is initiated by hydroxyl free radicals produced during flavin enzyme activity . J Biol Chem 1973;;248:7792-7797.
6 +
Chow CK, Tappel AL:  An enzymatic protective mechanism against lipid peroxidation damage to lungs of ozone-exposed rats . Lipids 1972;;7: 518-524.
7 +
Sakaguchi S, Kanda N, Hsu C, et al:  Lipid peroxide formation and membrane damage in endotoxin-poisoned mice . Microbiol Immunol 1981;; 25:229-244.
8 +
Brown RE, Craver R, Drake RM:  Lipid peroxidation and pulmonary hyaline membranes of the newborn . Ann Clin Lab Sci 1981;;11:25-34.
9 +
Yasaka T, Ohya I, MatsumotoJ, et al:  Acceleration of lipid peroxidation in human paraquat poisoning . Arch Intern Med 1981;;141:1169-1171.
10 +
Heflin C, Brigham KL:  Prevention by granulocyte depletion of increased lung vascular permeability of sheep lung after endotoxemia . J Clin Invest 1981;;68:1253-1262.
11 +
Smith ME, Gunther R, Demling RH:  Leukocytes, platelets, and thromboxane A2 in endotoxin induced lung injury . Surgery 1981;;90:102-107.
12 +
Demling RH, Proctor R, Starling J:  Lung injury and lung lysosomal enzyme release during endotoxemia . J Surg Res 1981;;30:135-141.
13 +
Sacks T, Moldow F, Craddock PR:  Oxygen radicals mediate endothelial cell damage by complement stimulated granulocytes: An in vitro model of immune vascular damage . J Clin Invest 1978;;61:1161-1167.
14 +
O'Flaherty J, Cousant S, Lineberger S, et al:  Phorbol myristate acetate: In vivo effects upon neutrophils, platelets, and lung . Am J Pathol 1980;;101:79-92.
15 +
Loyd J, Newman J, English D, et al:  Lung vascular effects of phorbol myristate acetate in awake sheep . J Appi Physiol 1983;;54:267-276.
16 +
Demling RH:  Role of prostaglandins in acute microvascular injury . Ann NY Acad Sci 1982;;284:517-534.
17 +
Demling RH, Smith M, Gunther R, et al:  Pulmonary injury and prostaglandin production during endotoxemia in conscious sheep . Am J Physiol 1981;;240:348-353.
18 +
Erdmann JA, Vaughn TR, Brigham KL, et al:  Effect of increased vascular pressure on lung fluid balance in unanesthetized sheep . Circ Res 1975;;28:271-276.
19 +
VreimCE, SnashallPD, DemlingRH, et al:  Lung and free interstitial fluid protein composition in sheep with edema . Am J Physiol 1976;;230: 1650-1653.
20 +
Staub NC, Bland RD, Brigham KL, et al:  Preparation of chronic lung lymph fistulas in sheep . J Surg Res 1975;;19:315-321.
21 +
Unger WC, Stanford TF, Benett H:  Extraction of prostaglandins from human blood . Nature 1971;;233:336-337.
22 +
Pearce ML, Yamashita J, Beasell J:  Measurement of pulmonary edema . Circ Res 1965;;16:482-488.
23 +
Brigham KL, Bowers RE, Haynes J:  Increased sheep lung vascular permeability caused by Escherichia coli endotoxin . Circ Res 1979;;45: 292-297.
24 +
Sibbald WT, Peterson M, Halliday RL, et al:  Pulmonary hypertension in sepsis . Chest 1978;;75:583-593.
25 +
Anderson RR, Holliday RL, Driedger AA, et al:  Documentation of pulmonary capillary permeability in the adult respiratory distress syndrome accompanying human sepsis . Am Rev Respir Dis 1979;;119:869-878.
26 +
Brigham KL, Owen PJ, Bowers RE:  Increased permeability of sheep lung vessels to proteins after pseudomonas bacteremia . Microvasc Res 1976;;11:415-421.
27 +
Parralt JR, Coker SJ, Hughes B:  The possible role of prostaglandins and thromboxanes in the pulmonary consequences of experimental endotoxin shock and clinical sepsis ; in McConn R (ed): Role of Chemical Mediators in the Pathophysiology of Acute Illness and Injury . New York, Raven Press, 1982;, pp 195-218.
28 +
Newman JH, Loyd J, Ogletree M, et al:  Effects of meclofenamate on the pulmonary vascular response to PMA , abstracted. Am Rev Respir Dis 1982;;124:282.
29 +
McCord JM:  Oxygen free radicals: Release and activities: A superoxide activated chemotactic factor and its role in the inflammatory process . Agents Actions 1980;;10:522-527.
30 +
Allen RC:  Free-radical production by reticulo endothelial cells , in Sharra A, Strauss R (eds): The Reticulo Endothelial System . New York, Plenum Publishing, 1980;, pp 309-337.

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