Abstract
During cardiopulmonary bypass (CPB), neutrophils (PMNs) may be stimulated by shear stress which could contribute to the pulmonary injury that occurs after CPB. To elucidate whether mechanically stimulated PMNs increase pulmonary vascular permeability, measured as the pulmonary filtration coefficient (K) and pulmonary vascular resistance, and to elucidate whether superoxide anion mediates this increase, we assessed the effects of stimulated and unstimulated PMNs, and of superoxide dismutase (SOD) on K and resistance in isolated perfused lungs from Sprague-Dawley rats. PMNs were stimulated by gentle agitation in a glass vial for 10s. Lungs perfused with the stimulated PMNs, being the stimulated group (n=6), elicited a 5-fold increase in the filtration coefficient compared with lungs perfused with unstimulated cells, being the unstimulated group (n=6). This increase in filtration was completely blocked by the pre-incubation of stimulated PMNs with CD18 monoclonal antibody, being the Ab group (n=6), and also by superoxide dismutase, being the SOD group (n=6). Pulmonary vascular resistance was not increased by stimulated PMNs, and the accumulation of stimulated PMNs was not blocked by SOD. These findings suggest that stimulated PMNs increaseK and that superoxide anion may injure the pulmonary vascular endothelial cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Demling RH (1995) The modern version of adult respiratory distress syndrome. Annu Rev Med 46(193):193–202
Elliott MJ, Finn AH (1993) Interaction between neutrophils and endothelium. Ann Thorac Surg 56(6):1503–1508
Dreyer WJ, Michael LH, Millman EE, Berens KL, Geske RS (1995) Neutrophil sequestration and pulmonary dysfunction in a canine model of open heart surgery with cardiopulmonary bypass. Evidence for a CD18-dependent mechanism. Circulation 92(8):2276–2283
Finn A, Morgan BP, Rebuck N, Klein N, Rogers CA, Hibbs M, Elliott M, Shore DF, Evans TW, Strobel S, Moat N (1996) Effects of inhibition of complement activation using recombinant soluble complement receptor 1 on neutrophil CD11b/CD18 and L-selectin expression and release of interleukin-8 and elastase in simulated cardiopulmonary bypass. J Thorac Cardiovasc Surg 111(2):451–459
Naess A, Halstensen A, Solberg CO (1986) Enhancement of leukocyte membrane receptor expression after mechanical agitation. Int Arch Allergy Appl Immunol 81(3):235–237
West JB, Dollery CT, Naimark A (1964) Distribution of blood flow in isolated lung; relation to vascular and alveolar pressures. J Appl Physiol 19:713–742
Dawson CA, Linehan JH, Rickaby DA (1982) Pulmonary microcirculatory hemodynamics. Ann NY Acad Sci 384:90–106
Tanita T, Koike K, Ono S, Fujimura S (1996) Simultaneous estimation of filtration variables in isolated rat lungs in zone 3 conditions. Tohoku J Exp Med 179:193–203
Drake RE, Smith JH, Gabel JC (1980) Estimation of the filtration coefficient in intact dog lungs. Am J Physiol 238(4):H430-H438
Perry M, Taylor AE (1988) Phorbol myristate acetate-induced injury of isolated perfused rat lungs: neutrophil dependence. J Appl Physiol 65(5):2164–2169
Perry ML, Kayes SG, Barnard JW, Taylor AE (1990) Effects of phorbol Myristate acetate-stimulated human leukocytes on rat lung. J Appl Physiol 68(1):235–240
Onizuka M, Tanita T, Staub NC (1989) Erythrocytes reduce liquid filtration in injured dog lungs. Am J Physiol 256(2 Pt 2):H515-H519
Nakata M, Nasuda-Kouyama A, Isogai Y, Kanegasaki S, Iizuka T (1997) Effect of aromatic nitroso-compounds on superoxide-generating activity in neutrophils. J Biochem 122(1):188–192
Liochev SL (1996) The role of iron-sulfur clusters in in vivo hydroxyl radical production. Free Radic Res 25(5):369–384
Liochev SI, Fridovich I (1997) How does superoxide dismutase protect against tumor necrosis factor: a hypothesis informed by effect of superoxide on “free” iron. Free Radic Biol Med 23(4):668–671
Hiraishi H, Terano A, Razandi M, Sugimoto T, Harada T, Ivey KJ (1992) Role of cellular superoxide dismutase against reactive oxygen metabolite injury in cultured bovine aortic endothelial cells. J Biol Chem 267(21):14812–14817
Entman ML, Youker K, Shoji T, Kukielka G, Shappell SB, Taylor AA, Smith CW (1992) Neutrophil induced oxidative injury of cardiac myocytes. A compartmented system requiring CD11b/CD18-ICAM-1 adherence. J Clin Invest 90(4):1335–1345
Yoshida N, Granger DN, Anderson DC, Rothlein R, Lane C, Kvietys PR (1992) Anoxia/reoxygenation-induced neutrophil adherence to cultured endothelial cells. Am J Physiol 262:H1891–1898
Staub NC (1987) Lung liquid and protein exchange: the four inhomogeneities. Ann Biomed Eng 15(2):115–126
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Tanita, T., Song, C., Kubo, H. et al. Superoxide anion mediates pulmonary vascular permeability caused by neutrophils in cardiopulmonary bypass. Surg Today 29, 755–761 (1999). https://doi.org/10.1007/BF02482321
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02482321