Do leukocytes contribute to impaired microvascular tissue perfusion after arterial repair?
Frank-W. Peter M.D.
Division of Plastic and Reconstructive Surgery, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorDale A. Schuschke Ph.D.
Center for Applied Microcirculation Research, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorWei Z. Wang M.D.
Center for Applied Microcirculation Research, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorGary L. Anderson Ph.D.
Department of Physiology, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorRalph J.P.M. Franken M.D.
Division of Plastic and Reconstructive Surgery, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorSilvia Pierangeli Ph.D.
Departments of Medicine, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorCorresponding Author
John H. Barker M.D., Ph.D.
Division of Plastic and Reconstructive Surgery, University of Louisville School of Medicine, Louisville, KY
332 MDR Building, 511 South Floyd Street, Louisville, KY 40292Search for more papers by this authorFrank-W. Peter M.D.
Division of Plastic and Reconstructive Surgery, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorDale A. Schuschke Ph.D.
Center for Applied Microcirculation Research, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorWei Z. Wang M.D.
Center for Applied Microcirculation Research, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorGary L. Anderson Ph.D.
Department of Physiology, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorRalph J.P.M. Franken M.D.
Division of Plastic and Reconstructive Surgery, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorSilvia Pierangeli Ph.D.
Departments of Medicine, University of Louisville School of Medicine, Louisville, KY
Search for more papers by this authorCorresponding Author
John H. Barker M.D., Ph.D.
Division of Plastic and Reconstructive Surgery, University of Louisville School of Medicine, Louisville, KY
332 MDR Building, 511 South Floyd Street, Louisville, KY 40292Search for more papers by this authorAbstract
Impaired capillary perfusion may result in flap failure. Platelet emboli, polymorphonuclear leukocytes (PMNs), and/or vasospasm have been identified as possible causes. This study investigates the role of PMNs in causing impaired capillary perfusion in a free flap model. PMN concentrations were depleted using antineutrophil serum. The cremaster muscles of 20 Sprague-Dawley rats were isolated on a single neurovascular pedicle and after a simulated technically poor arterial anastomosis upstream and reperfusion, capillary perfusion was measured each hour for 6 hours. Even though the number of PMNs was significantly reduced in the animals treated with antineutrophil serum, capillary perfusion was not changed compared with controls. These results demonstrate that depleting circulating PMNs does not protect capillary perfusion in our model. These findings suggest that reduced capillary perfusion downstream from an anastomotic repair is not mediated by the presence of PMNs in the microcirculation. © 1998 Wiley-Liss, Inc. MICROSURGERY 18:23–28, 1998.
References
- 1 Shaw WW: Microvascular free flaps: Survival, donor sites and application, in H Buncke, D Furnas (eds): Symposium on Clinical Frontiers in Reconstructive Microsurgery. St. Louis, Mosby, 1984.
- 2 Khouri RK: Free flap surgery. The second decade. Clin Plast Surg 19: 757–761, 1992.
- 3 Anderson GL, Acland RD, Siemionow M, et al.: Vascular isolation of the rat cremaster muscle. Microvasc Res 36: 56–63, 1988.
- 4 Acland RD, Anderson GL, Siemionow M, et al.: Direct in vivo observation of embolic events in the microcirculation distal to a small-vessel anastomosis. Plast Reconstr Surg 84: 280–288, 1989.
- 5 Barker JH, Acland RD, Anderson GL, et al.: Microcirculatory disturbances following the passage of emboli in an experimental free-flap model. Plast Reconstr Surg 90: 95–102, 1992.
- 6 Barker JH, Gu JM, Anderson GL, et al.: The effects of heparin and dietary fish oil on embolic events and the microcirculation downstream from a small-artery repair. Plast Reconstr Surg 91: 335–343, 1993.
- 7 Weinzweig N, Gonzalez M: Free tissue failure is not an all-or-none phenomenon. Plast Reconstr Surg 96: 648–660, 1995.
- 8 Holtmann H, Resch K: Cytokines. Naturwissenschaften 82: 178–187, 1995.
- 9 Gamelli RL, He LK, Liu H: Marrow granulocyte-macrophage progenitor cell response to burn injury as modified by endotoxin and indomethacin. J Trauma 37: 339–346, 1994.
- 10 Faist E, Schinkel C, Zimmer S: Update on the mechanisms of immune suppression of injury and immune modulation. World J Surg 20: 454–459, 1996.
- 11 Schlag G, Redl H: Mediators of injury and inflammation. World J Surg 20: 406–410, 1996.
- 12
Messmer K,
Sack FU,
Menger MD, et al.:
White cell-endothelium interaction during post-ischemic reperfusion of skin and skeletal muscle, in
S Chien (ed):
Vascular Endothelium: Health and Disease.
New York,
Plenum Press,
1988,
p 95.
10.1007/978-1-4684-8935-4_11 Google Scholar
- 13 Smith JK, Grisham MB, Granger DN, et al.: Free radical defense mechanism and neutrophil infiltration in postischemic skeletal muscle. Am J Physiol 256: H789, 1989.
- 14 Kerrigan CL, Stotland MA: Ischemia reperfusion injury: A review. Microsurgery 14: 165–175, 1993.
- 15 Hallenbeck JM, Dutka AJ: Background review and current concepts of reperfusion injury. Arch Neurol 47: 1245–1254, 1990.
- 16 Zimmerman BJ, Granger DN: Reperfusion injury. Surg Clin North Am 72: 65–83, 1992.
- 17 Menger MD, Vollmar B: Adhesion molecules as determinants of disease: From molecular biology to surgical research. Br J Surg 83: 588–601, 1996.
- 18 Breidahl AF, Hickey MJ, Stewart AG, et al.: Effects of low dose intra-arterial monoclonal antibodies to ICAM-1 and CD11/CD18 on local and systemic consequences of ischemia-reperfusion injury in skeletal muscle. Br J Plast Surg 49: 202–209, 1996.
- 19 Siemionow M, Wang WZ, Anderson GL, et al.: Leukocyte-endothelial interaction and capillary perfusion in ischemia/reperfusion of the rat cremaster muscle. Microcirc Endothelium Lymphatics 7: 183–197, 1991.
- 20 Barker JH, Anderson GL, Gu JM, et al.: Experimental study of the relationship between alterations in tissue perfusion and anastomotic patency. Microsurgery 14: 409–415, 1993.
- 21 Barker JH, Acland RD, Wyllie F, et al.: Flow-dependent thromboembolic events in a free flap model. Eur Surg Res 23: 61, 1991.
- 22 Anderson GL, Barker JH, Acland RD, et al.: Cod liver oil, but not anti-neutrophil serum, improves microvascular perfusion in the rat cremaster after embolic insult from an arterial thrombus. Int J Microcirc 9: 119, 1990.
- 23 Breda MA, Drinkwater DC, Laks H, et al.: Prevention of reperfusion injury in the neonatal heart with leukocyte-depleted blood. J Thorac Cardiovasc Surg 97: 654–665, 1989.
- 24 Malatiali SA, Juggi JS: Role of polymorphonuclear leukocytes in reperfusion injury of globally ischemic rat heart. Can J Cardiol 11: 147–158, 1995.
- 25 Yuan Y, Chilian M: Heart Microcirculation, in JH Barker, GL Anderson, M Menger (eds): Clinically Applied Microcirculation Research. Boca Raton, CRC Press, 1995, pp 213–225.
- 26 Vollmar B, Menger MD, Glasz J, et al.: Impact of leukocyte-endothelial cell interaction in hepatic ischemia-reperfusion injury. Am J Physiol 267: G786–G793, 1994.
- 27 Marzi I, Knee J, Buhren V, et al.: Reduction by superoxide dismutase of leukocyte-endothelial adherence after liver transplantation. Surgery 111: 90–97, 1992.
- 28 Bilzer M, Lauterburg BH: Oxidant stress and potentiation of ischemia/reperfusion injury to the perfused rat liver by human polymorphonuclear leukocytes. J Hepatol 20: 473–477, 1994.
- 29 Chavez-Cartaya RE, Metcalfe S, Ramirez-Romero P, et al.: Rat liver blood flow after ischemia and reperfusion. The effects of the platelet-activating factor antagonist WEB-2170 and of removing circulating leukocytes. Transplantation 57: 1440–1444, 1994.
- 30 Zhuang J, Shackford SR, Schmoker JD, et al.: The association of leukocytes with secondary brain injury. J Trauma 35: 415–422, 1993.
- 31 Yokota J, Minei JP, Fantini GA, et al.: Role of leukocytes in reperfusion injury of skeletal muscle after partial ischemia. Am J Physiol 257: H1068–1075, 1989.
- 32 Menger MD, Pelikan S, Steiner D, et al.: Microvascular ischemiareperfusion injury in striated muscle: Significance of “reflow paradox.” Am J Physiol 263: H1901–H1906, 1992.
- 33 Hill MA, Meininger GA: Skeletal muscle microcirculation, in JH Barker, GL Anderson, M Menger (eds): Clinically Applied Microcirculation Research. Boca Raton, CRC Press, 1995, pp 297–314.
- 34 Lefer AM, Weyrich AS, Buerke M: Role of selectins, a new family of adhesion molecules in ischemia-reperfusion injury. Cardiovasc Res 28: 289–294, 1994.
- 35 Bevilacqua MP, Nelson RM, Mannori G, et al.: Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med 45: 361–378, 1994.
- 36 Dunn GD, Granger DN, Korthuis RJ: Leukocyte/endothelial cell adhesion and ischemia/reperfusion injury, in JH Barker, GL Anderson, MD Menger (eds): Clinically Applied Microcirculation Research. Boca Raton, CRC Press, 1995, pp 75–96.
- 37 Milazzo VJ, Ferrante RJ, Sabido F, et al.: Time course of leukocyte adhesion to endothelium in ischemia-reperfusion. J Surg Res 61: 139–142, 1996.
- 38 Springer TA: Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 57: 827–872, 1995.
- 39 Menger MD, Vollmar B: In vivo analysis of microvascular reperfusion injury in striated muscle and skin. Microsurgery 15: 383–389, 1994.
- 40 Menger MD, Messmer K: Die Mikrozirkulation des Skelettmuskels nach Ischämie und Reperfusion. Wien Med Wochenschr 143: 148–158, 1993.
- 41 O'Shaughnessy M, Gu JM, Wyllie FJ, et al.: Microcirculatory consequences of microvascular surgery. Microsurgery 15: 405–412, 1994.
- 42 Schroer K: The effect of prostaglandins and thromboxane A2 on coronary vessel tone—mechanisms of action and therapeutic implications. Eur Heart J 14: 34–41, 1993.
- 43 Pallapies D: [Vasoactive drugs with an effect on the prostaglandin system]. Wien Klin Wochenschr 104: 521–525, 1992.
- 44 Raymenants E, Yang B, Nicolini F, et al.: Verapamil and aspirin modulate platelet-mediated vasomotion in arterial segments with intact or disrupted endothelium. J Am Coll Cardiol 22: 684–689, 1993.
- 45 Zamboni WA, Stephenson LL, Suchy H, et al.: Mechanisms of ischemia-reperfusion injury in skeletal muscle: TXA2 dependent arteriole vasoconstriction. J Reconstr Microsurg 11: 384, 1995.
Citing Literature
