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Hemorrhage Without Tissue Trauma Produces Immunosuppression and Enhances Susceptibility to Sepsis

Hemorrhage Without Tissue Trauma Produces Immunosuppression and Enhances Susceptibility to Sepsis Abstract • To determine whether hemorrhage without major tissue trauma can itself produce immunosuppression, the effect of hemorrhage on the lymphocyte response to T-cell mitogen in endotoxin-resistant C3H/HEJ mice was measured. The mice were bled to achieve a mean blood pressure of 35 mm Hg, maintained at that level for one hour, and then adequately resuscitated. On days 1 through 10 thereafter, the proliferative responses of the splenocytes to concanavalin A were measured and allogeneic mixed lymphocyte reaction was performed. The proliferative responses to mitogen stimulation as well as the results of mixed lymphocyte reaction studies indicated that marked immunosuppression occurred at day 1. Immunosuppression persisted for at least five days following hemorrhage, as evidenced by mitogen stimulation assay. Another group of mice was subjected to sepsis three days after hemorrhage and resuscitation. The mortalities in the sham-hemorrhage and hemorrhage groups following sepsis were 58% and 100%, respectively. Thus, a significant depression of cellular immunity occurred following simple hemorrhage despite adequate resuscitation, and this immunosuppression enhanced the susceptibility to sepsis. (Arch Surg 1987;122:62-68) References 1. Miller SE, Miller CL, Trunkey DD: The immune consequences of trauma . Surg Clin North Am 1982;62:167-181. 2. Antonacci AC, Calvano SE, Reaves LE, et al: Autologous and allogeneic mixed-lymphocyte responses following thermal injury in man: The immunomodulatory effects of interleukin-1, interleukin-2 and a prostaglandin inhibitor, WY-18251 . Clin Immunol Immunopathol 1984;30: 304-320.Crossref 3. Hamid J, Bancewicz J, Brown R, et al: The significance of changes in blood lymphocyte populations following surgical operations . Clin Exp Immunol 1984;56:49-57. 4. Winkelstein A: What are the immunological alterations induced by burn injury? J Trauma 1984;24:S72-S83.Crossref 5. Meakins JL, McLean APH, Kelly R, et al: Delayed hypersensitivity and neutrophil chemotaxis: Effect of trauma . J Trauma 1978;18:240-242.Crossref 6. Deitch EA, Gelder F, McDonald JC: Prognostic significance of abnormal neutrophil chemotaxis after thermal injury . J Trauma 1982;22:199-204.Crossref 7. Wang BS, Heacock EH, Wu AVO, et al: Generation of suppressor cells in mice after surgical trauma . J Clin Invest 1980;66:200-209.Crossref 8. Munster AM: Post-traumatic immunosuppression is due to activation of suppressor T-cells . Lancet 1976;7973:1329.Crossref 9. Ninnemann JL, Condie T, Davis SE, et al: Isolation of immunosuppressive serum components following thermal injury . J Trauma 1982;22: 837-844.Crossref 10. Kupper TS, Green DR, Durum SK, et al: Defective antigen presentation to a cloned T helper cell by macrophages from burned mice can be restored with interleukin-1 . Surgery 1985;98:199-206. 11. Kaplan JE, Saba TM: Humoral deficiency and reticuloendothelial depression after traumatic shock . Am J Physiol 1976;230:7-14. 12. Chaudry IH, Kupper TS, Schleck S, et al: Impairment of reticuloendothelial function following thermal injury and its restoration with ATP-MgCl2 administration . Circ Shock 1982;9:297-305. 13. Watson J, Riblet R: Genetic control of responses to bacterial lipopolysaccharides in mice . J Exp Med 1974;140:1147-1161.Crossref 14. Mittermayer C, Riede VN: Human pathology of the gastrointestinal tract in shock, ischemia and hypoxemia , in Cowley RA, Trump BE (eds): Pathophysiology of Shock, Anoxia and Ischemia . Baltimore, Williams & Wilkins, 1982, pp 301-308. 15. Bruce DL: Halothane inhibition of phytohemagglutinin-induced transformation of lymphocytes . Anesthesiology 1972;36:201-206.Crossref 16. Jubert AV, Lee ET, Hersh EM, et al: Effects of surgery, anesthesia and intraoperative blood loss on immunocompetence . J Surg Res 1973;15: 399-405.Crossref 17. Schenkein HA, Genco RJ: Inhibition of lymphocyte blastogenesis by C3c and C3d . J Immunol 1979;122:1126-1133. 18. Needleman BW, Weiler JM, Feldbush TL: The third component of complement inhibits human lymphocyte blastogenesis . J Immunol 1981;128: 1586-1591. 19. Roitt I, Brostoff J, Male D: Hypersensitivity-type III , in Roitt I (ed): Immunology . St Louis, CV Mosby Co, 1985, pp 21.1-21.10. 20. Waymack JP, Rapien J, Garnett D, et al: Effect of transfusion on immune function in a traumatized animal model . Arch Surg 1986;121:50-55.Crossref 21. Hume DM, Nelson DH: Adrenal cortical function in surgical shock . Surg Forum 1954;5:568-575. 22. Cleman H: Corticosteroid and lymphoid cells . N Engl J Med 1972;287: 388-397.Crossref 23. Gillis S, Crabtree GR, Smith KA: Glucocorticoid-induced inhibition of T-cell growth factor production: I. The effect on mitogen-induced lymphocyte proliferation . J Immunol 1979;123:1624-1631. 24. Cantrell DA, Smith KA: The interleukin-2 T cell system: A new cell growth model . Science 1984;224:1312-1316.Crossref 25. Stephan RN, Conrad PJ, Janeway CA, et al: Decreased interleukin-2 production following simple hemorrhage . Surg Forum 1986;37:73-75. 26. Trachte G: Endocrinology of shock , in Altura BM, Lefer AM, Schumer W (eds): Handbook of Shock and Trauma . New York, Raven Press, 1983, vol 1: Basic Science, pp 337-354. 27. Watts DT: Adrenergic mechanisms in hypovolemic shock , in Mills LC, Moyer JH (eds): Shock and Hypotension . New York, Grune & Stratton, 1965, pp 385-391. 28. Crary B, Borysenko M, Sutherland DC, et al: Decrease in mitogen responsiveness of mononuclear cells from peripheral blood after epinephrine administration in humans . J Immunol 1983;130:694-697. 29. Crary B, Hauser SL, Borysenko M, et al: Epinephrine-induced changes in the distribution of lymphocyte subsets in peripheral blood of humans . J Immunol 1983;131:1178-1181. 30. Beck L, Dontas AS: Vasomotor activity in hemorrhagic shock . Fed Proc 1955;14:318. 31. Lefer AM: Role of prostaglandins and thromboxanes in shock states , in Altura BM, Lefer AM, Schumer W (eds): Handbook of Shock and Trauma . New York, Raven Press, 1983, vol 1: Basic Science, pp 355-376. 32. Smith J, Steiner A, Parker C: Human lymphocyte metabolism: Effects of cyclic and noncyclic adenosine monophosphate on stimulation by phytohemagglutinin . J Clin Invest 1971;50:442-448.Crossref 33. Rogers TJ, Nowowiejski I, Webb DR: Partial characterization of a prostaglandin-induced suppressor factor . Cell Immunol 1980;50:82-93.Crossref 34. Kupper TS, Green DR: Immunoregulation after thermal injury: Sequential appearance of IJ+, Ly 1 T-suppressor inducer cells and Ly 2 T-suppressor effector cells following thermal trauma in mice . J Immunol 1984;135:3047-3053. 35. Constantian MB: Association of sepsis with immunosuppressive polypeptide in the serum of burn patients . Ann Surg 1978;188:209-215.Crossref 36. McLoughlin GA, Wu AVO, Saporoschetz I, et al: Correlation between anergy and a circulating immunosuppressive factor following major surgical trauma . Ann Surg 1979;190:297-304.Crossref 37. Wolfe JHN, Saporoschetz I, Young AE, et al: Suppressive serum, suppressor lymphocytes and death from burns . Ann Surg 1981;193:513-520. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Surgery American Medical Association

Hemorrhage Without Tissue Trauma Produces Immunosuppression and Enhances Susceptibility to Sepsis

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Publisher
American Medical Association
Copyright
Copyright © 1987 American Medical Association. All Rights Reserved.
ISSN
0004-0010
eISSN
1538-3644
DOI
10.1001/archsurg.1987.01400130068010
Publisher site
See Article on Publisher Site

Abstract

Abstract • To determine whether hemorrhage without major tissue trauma can itself produce immunosuppression, the effect of hemorrhage on the lymphocyte response to T-cell mitogen in endotoxin-resistant C3H/HEJ mice was measured. The mice were bled to achieve a mean blood pressure of 35 mm Hg, maintained at that level for one hour, and then adequately resuscitated. On days 1 through 10 thereafter, the proliferative responses of the splenocytes to concanavalin A were measured and allogeneic mixed lymphocyte reaction was performed. The proliferative responses to mitogen stimulation as well as the results of mixed lymphocyte reaction studies indicated that marked immunosuppression occurred at day 1. Immunosuppression persisted for at least five days following hemorrhage, as evidenced by mitogen stimulation assay. Another group of mice was subjected to sepsis three days after hemorrhage and resuscitation. The mortalities in the sham-hemorrhage and hemorrhage groups following sepsis were 58% and 100%, respectively. Thus, a significant depression of cellular immunity occurred following simple hemorrhage despite adequate resuscitation, and this immunosuppression enhanced the susceptibility to sepsis. (Arch Surg 1987;122:62-68) References 1. Miller SE, Miller CL, Trunkey DD: The immune consequences of trauma . Surg Clin North Am 1982;62:167-181. 2. Antonacci AC, Calvano SE, Reaves LE, et al: Autologous and allogeneic mixed-lymphocyte responses following thermal injury in man: The immunomodulatory effects of interleukin-1, interleukin-2 and a prostaglandin inhibitor, WY-18251 . Clin Immunol Immunopathol 1984;30: 304-320.Crossref 3. Hamid J, Bancewicz J, Brown R, et al: The significance of changes in blood lymphocyte populations following surgical operations . Clin Exp Immunol 1984;56:49-57. 4. Winkelstein A: What are the immunological alterations induced by burn injury? J Trauma 1984;24:S72-S83.Crossref 5. Meakins JL, McLean APH, Kelly R, et al: Delayed hypersensitivity and neutrophil chemotaxis: Effect of trauma . J Trauma 1978;18:240-242.Crossref 6. Deitch EA, Gelder F, McDonald JC: Prognostic significance of abnormal neutrophil chemotaxis after thermal injury . J Trauma 1982;22:199-204.Crossref 7. Wang BS, Heacock EH, Wu AVO, et al: Generation of suppressor cells in mice after surgical trauma . J Clin Invest 1980;66:200-209.Crossref 8. Munster AM: Post-traumatic immunosuppression is due to activation of suppressor T-cells . Lancet 1976;7973:1329.Crossref 9. Ninnemann JL, Condie T, Davis SE, et al: Isolation of immunosuppressive serum components following thermal injury . J Trauma 1982;22: 837-844.Crossref 10. Kupper TS, Green DR, Durum SK, et al: Defective antigen presentation to a cloned T helper cell by macrophages from burned mice can be restored with interleukin-1 . Surgery 1985;98:199-206. 11. Kaplan JE, Saba TM: Humoral deficiency and reticuloendothelial depression after traumatic shock . Am J Physiol 1976;230:7-14. 12. Chaudry IH, Kupper TS, Schleck S, et al: Impairment of reticuloendothelial function following thermal injury and its restoration with ATP-MgCl2 administration . Circ Shock 1982;9:297-305. 13. Watson J, Riblet R: Genetic control of responses to bacterial lipopolysaccharides in mice . J Exp Med 1974;140:1147-1161.Crossref 14. Mittermayer C, Riede VN: Human pathology of the gastrointestinal tract in shock, ischemia and hypoxemia , in Cowley RA, Trump BE (eds): Pathophysiology of Shock, Anoxia and Ischemia . Baltimore, Williams & Wilkins, 1982, pp 301-308. 15. Bruce DL: Halothane inhibition of phytohemagglutinin-induced transformation of lymphocytes . Anesthesiology 1972;36:201-206.Crossref 16. Jubert AV, Lee ET, Hersh EM, et al: Effects of surgery, anesthesia and intraoperative blood loss on immunocompetence . J Surg Res 1973;15: 399-405.Crossref 17. Schenkein HA, Genco RJ: Inhibition of lymphocyte blastogenesis by C3c and C3d . J Immunol 1979;122:1126-1133. 18. Needleman BW, Weiler JM, Feldbush TL: The third component of complement inhibits human lymphocyte blastogenesis . J Immunol 1981;128: 1586-1591. 19. Roitt I, Brostoff J, Male D: Hypersensitivity-type III , in Roitt I (ed): Immunology . St Louis, CV Mosby Co, 1985, pp 21.1-21.10. 20. Waymack JP, Rapien J, Garnett D, et al: Effect of transfusion on immune function in a traumatized animal model . Arch Surg 1986;121:50-55.Crossref 21. Hume DM, Nelson DH: Adrenal cortical function in surgical shock . Surg Forum 1954;5:568-575. 22. Cleman H: Corticosteroid and lymphoid cells . N Engl J Med 1972;287: 388-397.Crossref 23. Gillis S, Crabtree GR, Smith KA: Glucocorticoid-induced inhibition of T-cell growth factor production: I. The effect on mitogen-induced lymphocyte proliferation . J Immunol 1979;123:1624-1631. 24. Cantrell DA, Smith KA: The interleukin-2 T cell system: A new cell growth model . Science 1984;224:1312-1316.Crossref 25. Stephan RN, Conrad PJ, Janeway CA, et al: Decreased interleukin-2 production following simple hemorrhage . Surg Forum 1986;37:73-75. 26. Trachte G: Endocrinology of shock , in Altura BM, Lefer AM, Schumer W (eds): Handbook of Shock and Trauma . New York, Raven Press, 1983, vol 1: Basic Science, pp 337-354. 27. Watts DT: Adrenergic mechanisms in hypovolemic shock , in Mills LC, Moyer JH (eds): Shock and Hypotension . New York, Grune & Stratton, 1965, pp 385-391. 28. Crary B, Borysenko M, Sutherland DC, et al: Decrease in mitogen responsiveness of mononuclear cells from peripheral blood after epinephrine administration in humans . J Immunol 1983;130:694-697. 29. Crary B, Hauser SL, Borysenko M, et al: Epinephrine-induced changes in the distribution of lymphocyte subsets in peripheral blood of humans . J Immunol 1983;131:1178-1181. 30. Beck L, Dontas AS: Vasomotor activity in hemorrhagic shock . Fed Proc 1955;14:318. 31. Lefer AM: Role of prostaglandins and thromboxanes in shock states , in Altura BM, Lefer AM, Schumer W (eds): Handbook of Shock and Trauma . New York, Raven Press, 1983, vol 1: Basic Science, pp 355-376. 32. Smith J, Steiner A, Parker C: Human lymphocyte metabolism: Effects of cyclic and noncyclic adenosine monophosphate on stimulation by phytohemagglutinin . J Clin Invest 1971;50:442-448.Crossref 33. Rogers TJ, Nowowiejski I, Webb DR: Partial characterization of a prostaglandin-induced suppressor factor . Cell Immunol 1980;50:82-93.Crossref 34. Kupper TS, Green DR: Immunoregulation after thermal injury: Sequential appearance of IJ+, Ly 1 T-suppressor inducer cells and Ly 2 T-suppressor effector cells following thermal trauma in mice . J Immunol 1984;135:3047-3053. 35. Constantian MB: Association of sepsis with immunosuppressive polypeptide in the serum of burn patients . Ann Surg 1978;188:209-215.Crossref 36. McLoughlin GA, Wu AVO, Saporoschetz I, et al: Correlation between anergy and a circulating immunosuppressive factor following major surgical trauma . Ann Surg 1979;190:297-304.Crossref 37. Wolfe JHN, Saporoschetz I, Young AE, et al: Suppressive serum, suppressor lymphocytes and death from burns . Ann Surg 1981;193:513-520.

Journal

Archives of SurgeryAmerican Medical Association

Published: Jan 1, 1987

References