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February 17, 1989, Vol 261, No. 7 >
ARTICLE | February 17, 1989

Reperfusion Pulmonary Edema FREE

Joseph M. Klausner, MD; Ian S. Paterson, MB, FRCS; John A. Mannick, MD; C. Robert Valeri, MD; David Shepro, PhD; Herbert B. Hechtman, MD
[+] Author Affiliations

Reprint requests to Brigham and Women's Hospital, 75 Francis St, Boston, MA 02115 (Dr Hechtman).


JAMA. 1989;261(7):1030-1035. doi:10.1001/jama.1989.03420070080035
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References

Reperfusion following lower-torso ischemia in humans leads to respiratory failure manifest by pulmonary hypertension, hypoxemia, and noncardiogenic pulmonary edema. The mechanism of injury has been studied in the sheep lung lymph preparation, where it has been demonstrated that the reperfusion resulting in pulmonary edema is due to an increase in microvascular permeability of the lung to protein. This respiratory failure caused by reperfusion appears to be an inflammatory reaction associated with intravascular release of the chemoattractants leukotriene B4 and thromboxane. Histological studies of the lung in experimental animals revealed significant accumulation of neutrophils but not platelets in alveolar capillaries. We conclude that thromboxane generated and released from the ischemic tissue is responsible for the transient pulmonary hypertension. Second, it is likely that the chemoattractants are responsible for leukosequestration, and, third, neutrophils, oxygen-derived free radicals, and thromboxane moderate the altered lung permeability.

(JAMA 1989;261:1030-1035)

REFERENCES

1 +
Haimovici H:  Metabolic complications of acute arterial occlusion . J Cardiovasc Surg 1979;;20:349-357.
2 +
Stallone RJ, Lim RC Jr, Blaisdell FW:  Pathogenesis of pulmonary changes following ischemia of the lower extremities . Ann Thorac Surg 1969;;7: 539-549.
3 +
Halushka PV, Lefer AM:  Thromboxane A2 in health and disease . Fed Proc 1987;;6:131-132.
4 +
Anner H, Kaufman RP Jr, Kobzik L, et al:  Pulmonary leukosequestration induced by hind limb ischemia . Ann Surg 1987;;206:162-167.
5 +
Paterson IS, Klausner JM, Pugatch R, et al:  Non-cardiogenic pulmonary edema after abdominal aortic aneurysm surgery . Ann Surg , in press.
6 +
Tranbaugh RF, Lewis FR:  Mechanisms and etiologic factors of pulmonary edema . Surg Gynecol Obstet 1984;;158:193-206.
7 +
Gee MH, Perkowski SZ, Havill AM, et al:  Role of prostaglandins and leukotrienes in complement-mediated lung vascular injury . Chest 1983;; 83( (suppl) ):83-85.
8 +
Anner H, Kaufman RP Jr, Valeri CR, et al:  Reperfusion of the ischemic lower limbs increases pulmonary microvascular permeability . J Trauma 1988;;28:607-610.
9 +
Anner H, Kaufman RP Jr, Kobzik L, et al:  Pulmonary hypertension and leukosequestration after lower torso ischemia . Ann Surg 1987;;206:642-648.
10 +
Klausner JM, Anner H, Paterson IS, et al:  Lower torso ischemia induced lung injury is leukocyte dependent . Ann Surg 1988;; 208:761-767.
11 +
Parker RE, Roselli RJ, Harris T, et al:  Effects of graded increases in pulmonary vascular pressures on lung fluid balance in unanesthetized sheep . Circ Res 1981;;49:1164-1172.
12 +
Endman J, Vaughan T, Brigham KL, et al:  Effects of increased vascular pressure on lung fluid balance in unanesthetized sheep . Circ Res 1975;;37:271-280.
13 +
Staub NC:  Pulmonary edema . Physiol Rev 1974;;54:678-811.
14 +
Huval WV, Lelcuk S, Allen PD, et al:  Determinants of cardiovascular stability during abdominal aortic aneurysmectomy . Ann Surg 1984;;199:216-222.
15 +
McLoughlin GA, Grindlinger GA, Manny J, et al:  Intrapulmonary clotting and fibrinolysis during abdominal aortic aneurysm surgery . Ann Surg 1979;;190:623-630.
16 +
Smith ME, Gunter R, Gee M, et al:  Leukocytes, platelets and thromboxane A2 in endotoxin induced lung injury . Surgery 1981;;90:102-106.
17 +
Tate RM, Repine JE:  Neutrophils and the adult respiratory distress syndrome . Am Rev Respir Dis 1983;;128:552-559.
18 +
Mullane KM, Salmon JA, Kramer R:  Leukocyte-derived metabolites of arachidonic acid in ischemia induced myocardial injury . Fed Proc 1987;;46:2422-2433.
19 +
Shasby DM, Shasby SS, Peach MJ:  Polymorphonuclear leukocyte: Arachidonate edema . J Appl Physiol 1985;;59:47-55.
20 +
Rinaldo JE, Bomovetz H:  Deterioration of oxygenation and abnormal lung microvascular permeability during resolution of leukopenia in patients with diffuse lung injury . Am Rev Respir Dis 1985;;131:579-583.
21 +
Winn R, Maunder R, Chi E, et al:  Neutrophil depletion does not prevent lung edema after endotoxin infusion in goats . J Appl Physiol 1987;;62:116-121.
22 +
Romson JL, Hook BG, Kinkel SL, et al:  Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog . Circulation 1983;;67:1016-1023.
23 +
Klausner JM, Paterson IS, Valeri CR, et al:  Leukocytes and leukotrienes mediate ischemia induced increase in permeability . Ann Surg 1988;;208:755-760.
24 +
Linas SL, Shanley PF, Whittemburg D, et al:  Neutrophils accentuate ischemia-reperfusion injury in isolated perfused rat kidney . Am J Physiol 1988;;255:728-735.
25 +
Schmid-Schonbein GW:  Capillary plugging by granulocytes and the no-reflow phenomenon in the microcirculation . Fed Proc 1987;;46:2397-2401.
26 +
Utsunomiya T, Krausz MM, Mannick JA, et al:  Maintenance of cardiodynamics with aspirin during abdominal aortic aneurysmectomy . Ann Surg 1981;;194:602-608.
27 +
Lelcuk S, Huval WV, Valeri CR, et al:  Inhibition of ischemia induced thromboxane synthesis in man . J Trauma 1984;;24:393-396.
28 +
Lelcuk S, Alexander F, Valeri CR, et al:  Thromboxane A2 moderates permeability after limb ischemia . Ann Surg 1985;;202:642-646.
29 +
Klausner JM, Anner H, Kobzik L, et al:  Leg ischemia induced lung permeability requires thromboxane A2 and neutrophils, abstracted . Fed Proc 1987;;44:995.
30 +
Klausner JM, Alexander SJ, Anner H, et al:  Thromboxane (Tx) mediates microvascular permeability, abstracted . Fed Proc 1988;;2:A1870.
31 +
Welles SL, Shepro D, Hechtman HB:  Eicosanoid modulation of stress fibers in cultured bovine endothelial cells . Inflammation 1985;;9:439-450.
32 +
Sharbi DM, Sharbi SS, Sullivan JM, et al:  Role of endothelial cell cytoskeleton in control of endothelial permeability . Circ Res 1982;;51:657-661.
33 +
Doukas J, Hechtman HB, Shepro D:  Endothelial-secreted arachidonic acid metabolites modulate polymorphonuclear leukocyte chemotaxis and diapedesis in vitro . Blood 1988;;71:771-779.
34 +
Krausz MM, Utsunomiya T, Dunham B, et al:  Inhibition of permeability edema with imidazole . Surgery 1982;;92:299-308.
35 +
Garcia-Szabo R, Minnlar FL, Bizios R, et al:  Role of thromboxane in the pulmonary response to microembolization . Chest 1983;;83( (suppl) ):76-78.
36 +
Winn R, Harlan J, Nadir B, et al:  Thromboxane A2 mediates lung vasoconstriction but not permeability after endotoxin . J Clin Invest 1983;;72:911-918.
37 +
Spagnuolo PJ, Ellner JJ, Hassid A, et al:  Thromboxane A2 mediates augmented polymorphonuclear leukocyte adhesiveness . J Clin Invest 1980;;66:406-414.
38 +
Palder SB, Huval WV, Lelcuk S, et al:  Reduction of polymorphonuclear leukocyte accumulations by inhibition of cyclooxygenase and thromboxane synthetase in the rabbit . Surgery 1986;;99:72-80.
39 +
Klausner JM, Kobzik L, Valeri CR, et al:  Selective lung leukosequestration after complement activation . J Appl Physiol 1988;;65:80-88.
40 +
Ford-Hutchinson AW:  Leukotrienes: Their formation and role as inflammatory mediators . Fed Proc 1985;;44:25-29.
41 +
Klausner JM, Paterson IS, Kobzik L, et al:  Leukotrienes but not complement mediate limb ischemia induced lung injury . Ann Surg , in press.
42 +
Dunham B, Shepro D, Hechtman HB:  Leukotriene B4 induction of TxB2 in cultured bovine aortic endothelia cells . Inflammation 1984;;8:313-321.
43 +
Garcia JGN, Coonan TC, Jubiz W, et al:  Leukotrienes and the pulmonary microcirculation . Am Rev Respir Dis 1987;;136:161-169.
44 +
Worthen GS, Goins AJ, Mitchel BC, et al:  Platelet activating factor causes neutrophil accumulation and edema in rabbit lungs . Chest 1983;;83:135-155.
45 +
McCord JM:  Oxygen-derived free radicals in postischemic tissue injury . N Engl J Med 1985;; 312:159-163.
46 +
Klausner JM, Paterson IS, Kobzik L, et al:  Oxygen free radicals mediate ischemia induced lung injury . Surgery , in press.
47 +
Tate RM, Morris HG, Schroeder WR, et al:  Oxygen metabolites stimulate thromboxane production and vasoconstriction in isolated saline perfused rabbit lungs . J Clin Invest 1984;;74:608-613.

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

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1 +
Haimovici H:  Metabolic complications of acute arterial occlusion . J Cardiovasc Surg 1979;;20:349-357.
2 +
Stallone RJ, Lim RC Jr, Blaisdell FW:  Pathogenesis of pulmonary changes following ischemia of the lower extremities . Ann Thorac Surg 1969;;7: 539-549.
3 +
Halushka PV, Lefer AM:  Thromboxane A2 in health and disease . Fed Proc 1987;;6:131-132.
4 +
Anner H, Kaufman RP Jr, Kobzik L, et al:  Pulmonary leukosequestration induced by hind limb ischemia . Ann Surg 1987;;206:162-167.
5 +
Paterson IS, Klausner JM, Pugatch R, et al:  Non-cardiogenic pulmonary edema after abdominal aortic aneurysm surgery . Ann Surg , in press.
6 +
Tranbaugh RF, Lewis FR:  Mechanisms and etiologic factors of pulmonary edema . Surg Gynecol Obstet 1984;;158:193-206.
7 +
Gee MH, Perkowski SZ, Havill AM, et al:  Role of prostaglandins and leukotrienes in complement-mediated lung vascular injury . Chest 1983;; 83( (suppl) ):83-85.
8 +
Anner H, Kaufman RP Jr, Valeri CR, et al:  Reperfusion of the ischemic lower limbs increases pulmonary microvascular permeability . J Trauma 1988;;28:607-610.
9 +
Anner H, Kaufman RP Jr, Kobzik L, et al:  Pulmonary hypertension and leukosequestration after lower torso ischemia . Ann Surg 1987;;206:642-648.
10 +
Klausner JM, Anner H, Paterson IS, et al:  Lower torso ischemia induced lung injury is leukocyte dependent . Ann Surg 1988;; 208:761-767.
11 +
Parker RE, Roselli RJ, Harris T, et al:  Effects of graded increases in pulmonary vascular pressures on lung fluid balance in unanesthetized sheep . Circ Res 1981;;49:1164-1172.
12 +
Endman J, Vaughan T, Brigham KL, et al:  Effects of increased vascular pressure on lung fluid balance in unanesthetized sheep . Circ Res 1975;;37:271-280.
13 +
Staub NC:  Pulmonary edema . Physiol Rev 1974;;54:678-811.
14 +
Huval WV, Lelcuk S, Allen PD, et al:  Determinants of cardiovascular stability during abdominal aortic aneurysmectomy . Ann Surg 1984;;199:216-222.
15 +
McLoughlin GA, Grindlinger GA, Manny J, et al:  Intrapulmonary clotting and fibrinolysis during abdominal aortic aneurysm surgery . Ann Surg 1979;;190:623-630.
16 +
Smith ME, Gunter R, Gee M, et al:  Leukocytes, platelets and thromboxane A2 in endotoxin induced lung injury . Surgery 1981;;90:102-106.
17 +
Tate RM, Repine JE:  Neutrophils and the adult respiratory distress syndrome . Am Rev Respir Dis 1983;;128:552-559.
18 +
Mullane KM, Salmon JA, Kramer R:  Leukocyte-derived metabolites of arachidonic acid in ischemia induced myocardial injury . Fed Proc 1987;;46:2422-2433.
19 +
Shasby DM, Shasby SS, Peach MJ:  Polymorphonuclear leukocyte: Arachidonate edema . J Appl Physiol 1985;;59:47-55.
20 +
Rinaldo JE, Bomovetz H:  Deterioration of oxygenation and abnormal lung microvascular permeability during resolution of leukopenia in patients with diffuse lung injury . Am Rev Respir Dis 1985;;131:579-583.
21 +
Winn R, Maunder R, Chi E, et al:  Neutrophil depletion does not prevent lung edema after endotoxin infusion in goats . J Appl Physiol 1987;;62:116-121.
22 +
Romson JL, Hook BG, Kinkel SL, et al:  Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog . Circulation 1983;;67:1016-1023.
23 +
Klausner JM, Paterson IS, Valeri CR, et al:  Leukocytes and leukotrienes mediate ischemia induced increase in permeability . Ann Surg 1988;;208:755-760.
24 +
Linas SL, Shanley PF, Whittemburg D, et al:  Neutrophils accentuate ischemia-reperfusion injury in isolated perfused rat kidney . Am J Physiol 1988;;255:728-735.
25 +
Schmid-Schonbein GW:  Capillary plugging by granulocytes and the no-reflow phenomenon in the microcirculation . Fed Proc 1987;;46:2397-2401.
26 +
Utsunomiya T, Krausz MM, Mannick JA, et al:  Maintenance of cardiodynamics with aspirin during abdominal aortic aneurysmectomy . Ann Surg 1981;;194:602-608.
27 +
Lelcuk S, Huval WV, Valeri CR, et al:  Inhibition of ischemia induced thromboxane synthesis in man . J Trauma 1984;;24:393-396.
28 +
Lelcuk S, Alexander F, Valeri CR, et al:  Thromboxane A2 moderates permeability after limb ischemia . Ann Surg 1985;;202:642-646.
29 +
Klausner JM, Anner H, Kobzik L, et al:  Leg ischemia induced lung permeability requires thromboxane A2 and neutrophils, abstracted . Fed Proc 1987;;44:995.
30 +
Klausner JM, Alexander SJ, Anner H, et al:  Thromboxane (Tx) mediates microvascular permeability, abstracted . Fed Proc 1988;;2:A1870.
31 +
Welles SL, Shepro D, Hechtman HB:  Eicosanoid modulation of stress fibers in cultured bovine endothelial cells . Inflammation 1985;;9:439-450.
32 +
Sharbi DM, Sharbi SS, Sullivan JM, et al:  Role of endothelial cell cytoskeleton in control of endothelial permeability . Circ Res 1982;;51:657-661.
33 +
Doukas J, Hechtman HB, Shepro D:  Endothelial-secreted arachidonic acid metabolites modulate polymorphonuclear leukocyte chemotaxis and diapedesis in vitro . Blood 1988;;71:771-779.
34 +
Krausz MM, Utsunomiya T, Dunham B, et al:  Inhibition of permeability edema with imidazole . Surgery 1982;;92:299-308.
35 +
Garcia-Szabo R, Minnlar FL, Bizios R, et al:  Role of thromboxane in the pulmonary response to microembolization . Chest 1983;;83( (suppl) ):76-78.
36 +
Winn R, Harlan J, Nadir B, et al:  Thromboxane A2 mediates lung vasoconstriction but not permeability after endotoxin . J Clin Invest 1983;;72:911-918.
37 +
Spagnuolo PJ, Ellner JJ, Hassid A, et al:  Thromboxane A2 mediates augmented polymorphonuclear leukocyte adhesiveness . J Clin Invest 1980;;66:406-414.
38 +
Palder SB, Huval WV, Lelcuk S, et al:  Reduction of polymorphonuclear leukocyte accumulations by inhibition of cyclooxygenase and thromboxane synthetase in the rabbit . Surgery 1986;;99:72-80.
39 +
Klausner JM, Kobzik L, Valeri CR, et al:  Selective lung leukosequestration after complement activation . J Appl Physiol 1988;;65:80-88.
40 +
Ford-Hutchinson AW:  Leukotrienes: Their formation and role as inflammatory mediators . Fed Proc 1985;;44:25-29.
41 +
Klausner JM, Paterson IS, Kobzik L, et al:  Leukotrienes but not complement mediate limb ischemia induced lung injury . Ann Surg , in press.
42 +
Dunham B, Shepro D, Hechtman HB:  Leukotriene B4 induction of TxB2 in cultured bovine aortic endothelia cells . Inflammation 1984;;8:313-321.
43 +
Garcia JGN, Coonan TC, Jubiz W, et al:  Leukotrienes and the pulmonary microcirculation . Am Rev Respir Dis 1987;;136:161-169.
44 +
Worthen GS, Goins AJ, Mitchel BC, et al:  Platelet activating factor causes neutrophil accumulation and edema in rabbit lungs . Chest 1983;;83:135-155.
45 +
McCord JM:  Oxygen-derived free radicals in postischemic tissue injury . N Engl J Med 1985;; 312:159-163.
46 +
Klausner JM, Paterson IS, Kobzik L, et al:  Oxygen free radicals mediate ischemia induced lung injury . Surgery , in press.
47 +
Tate RM, Morris HG, Schroeder WR, et al:  Oxygen metabolites stimulate thromboxane production and vasoconstriction in isolated saline perfused rabbit lungs . J Clin Invest 1984;;74:608-613.

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