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Published in: European Journal of Trauma and Emergency Surgery 2/2011

Open Access 01-04-2011 | Original Article

Isolated blunt chest injury leads to transient activation of circulating neutrophils

Authors: T. Visser, F. Hietbrink, K. M. Groeneveld, L. Koenderman, L. P. H. Leenen

Published in: European Journal of Trauma and Emergency Surgery | Issue 2/2011

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Abstract

Introduction

The acute respiratory distress syndrome (ARDS) is a severe and frequently seen complication in multi-trauma patients. ARDS is caused by an excessive innate immune response with a clear role for neutrophils. As ARDS is more frequently seen in trauma patients with chest injury, we investigated the influence of chest injury on the systemic neutrophil response and the development of ARDS.

Materials and methods

Thirteen patients with isolated blunt chest injury [abbreviated injury score (AIS) 2–5] were included. To avoid systemic inflammation caused by tissue damage outside the thorax, injuries to other regions than the chest did not exceed an AIS of 2. At 3, 9 and 24 h after injury, the expression of circulating activating molecules on neutrophils and levels of circulating interleukine (IL)-6 were determined. Blood samples from eight healthy volunteers were used as control.

Results

Blunt chest injury resulted in the activation of circulating neutrophils, as characterized by a decreased expression of l-selectin (CD62L), CXCR2 (CD182b) and C5aR (CD88) compared to control (p < 0.05). Expression of l-selectin, CXCR2 and C5aR was partially restored at 24 h after injury. In addition, the mean expression of FcγRIII (CD16) dropped (p < 0.001), indicating the recruitment of young neutrophils into the circulation. IL-6 levels increased to a maximum mean concentration of 86 ± 31 pg/ml at 24 h postinjury. None of the patients developed ARDS.

Conclusion

Blunt chest trauma caused a systemic inflammatory reaction with transient activation of neutrophils and mobilization of young neutrophils into the circulation. Isolated chest injury, however, was not abundant enough to cause ARDS, so a second hit appears crucial.
Literature
1.
go back to reference Miller PR, Croce MA, Kilgo PD, Scott J, Fabian TC. Acute respiratory distress syndrome in blunt trauma: identification of independent risk factors. Am Surg. 2002; 68(10):845–850; discussion 850–841. Miller PR, Croce MA, Kilgo PD, Scott J, Fabian TC. Acute respiratory distress syndrome in blunt trauma: identification of independent risk factors. Am Surg. 2002; 68(10):845–850; discussion 850–841.
2.
go back to reference Vecsei V, Arbes S, Aldrian A, Nau T. Chest injury in polytrauma. Eur J Trauma. 2005;31:239–43.CrossRef Vecsei V, Arbes S, Aldrian A, Nau T. Chest injury in polytrauma. Eur J Trauma. 2005;31:239–43.CrossRef
3.
go back to reference Miller PR, Croce MA, Bee TK, Qaisi WG, Smith CP, Collins GL, et al. ARDS after pulmonary contusion: accurate measurement of contusion volume identifies high-risk patients. J Trauma, 2001; 51(2):223–228; discussion 229–230. Miller PR, Croce MA, Bee TK, Qaisi WG, Smith CP, Collins GL, et al. ARDS after pulmonary contusion: accurate measurement of contusion volume identifies high-risk patients. J Trauma, 2001; 51(2):223–228; discussion 229–230.
4.
go back to reference Maier M, Geiger EV, Wutzler S, Lehnert M, Wiercinski A, Buurman WA, et al. Role of lung contusions on posttraumatic inflammatory response and organ dysfunction in traumatized patients. Eur J Trauma Emerg Surg. 2009;35(5):463–9.CrossRef Maier M, Geiger EV, Wutzler S, Lehnert M, Wiercinski A, Buurman WA, et al. Role of lung contusions on posttraumatic inflammatory response and organ dysfunction in traumatized patients. Eur J Trauma Emerg Surg. 2009;35(5):463–9.CrossRef
5.
go back to reference Henson PM, Johnston RB Jr. Tissue injury in inflammation oxidants, proteinases, and cationic proteins. J Clin Invest. 1987;79(3):669–74.PubMedCrossRef Henson PM, Johnston RB Jr. Tissue injury in inflammation oxidants, proteinases, and cationic proteins. J Clin Invest. 1987;79(3):669–74.PubMedCrossRef
6.
go back to reference Tellado JM, Christou NV. Activation state of polymorphonuclear leukocytes in surgical patients: characterization of surface receptor expression. Surgery. 1993;113(6):624–30.PubMed Tellado JM, Christou NV. Activation state of polymorphonuclear leukocytes in surgical patients: characterization of surface receptor expression. Surgery. 1993;113(6):624–30.PubMed
7.
go back to reference Rosenbloom AJ, Pinsky MR, Bryant JL, Shin A, Whiteside T. Leukocyte activation in the peripheral blood of patients with cirrhosis of the liver and SIRS. Correlation with serum interleukin-6 levels and organ dysfunction. JAMA. 1995;274(1):58–65.PubMedCrossRef Rosenbloom AJ, Pinsky MR, Bryant JL, Shin A, Whiteside T. Leukocyte activation in the peripheral blood of patients with cirrhosis of the liver and SIRS. Correlation with serum interleukin-6 levels and organ dysfunction. JAMA. 1995;274(1):58–65.PubMedCrossRef
8.
go back to reference Muller Kobold AC, Tulleken JE, Zijlstra JG, Sluiter W, Hermans J, Kallenberg CG, et al. Leukocyte activation in sepsis—correlations with disease state and mortality. Intensive Care Med. 2000;26(7):883–92.PubMedCrossRef Muller Kobold AC, Tulleken JE, Zijlstra JG, Sluiter W, Hermans J, Kallenberg CG, et al. Leukocyte activation in sepsis—correlations with disease state and mortality. Intensive Care Med. 2000;26(7):883–92.PubMedCrossRef
9.
go back to reference Russwurm S, Vickers J, Meier-Hellmann A, Spangenberg P, Bredle D, Reinhart K, et al. Platelet and leukocyte activation correlate with the severity of septic organ dysfunction. Shock. 2002;17(4):263–8.PubMedCrossRef Russwurm S, Vickers J, Meier-Hellmann A, Spangenberg P, Bredle D, Reinhart K, et al. Platelet and leukocyte activation correlate with the severity of septic organ dysfunction. Shock. 2002;17(4):263–8.PubMedCrossRef
10.
go back to reference Garcia-Vicuna R, Diaz-Gonzalez F, Gonzalez-Alvaro I, del Pozo MA, Mollinedo F, Cabanas C, et al. Prevention of cytokine-induced changes in leukocyte adhesion receptors by nonsteroidal antiinflammatory drugs from the oxicam family. Arthritis Rheum. 1997;40(1):143–53.PubMedCrossRef Garcia-Vicuna R, Diaz-Gonzalez F, Gonzalez-Alvaro I, del Pozo MA, Mollinedo F, Cabanas C, et al. Prevention of cytokine-induced changes in leukocyte adhesion receptors by nonsteroidal antiinflammatory drugs from the oxicam family. Arthritis Rheum. 1997;40(1):143–53.PubMedCrossRef
11.
go back to reference Hietbrink F, Oudijk EJ, Braams R, Koenderman L, Leenen L. Aberrant regulation of polymorphonuclear phagocyte responsiveness in multitrauma patients. Shock. 2006;26(6):558–64.PubMedCrossRef Hietbrink F, Oudijk EJ, Braams R, Koenderman L, Leenen L. Aberrant regulation of polymorphonuclear phagocyte responsiveness in multitrauma patients. Shock. 2006;26(6):558–64.PubMedCrossRef
12.
13.
go back to reference McGill SN, Ahmed NA, Hu F, Michel RP, Christou NV. Shedding of l-selectin as a mechanism for reduced polymorphonuclear neutrophil exudation in patients with the systemic inflammatory response syndrome. Arch Surg. 1996; 131(11):1141–1146; discussion 1147. McGill SN, Ahmed NA, Hu F, Michel RP, Christou NV. Shedding of l-selectin as a mechanism for reduced polymorphonuclear neutrophil exudation in patients with the systemic inflammatory response syndrome. Arch Surg. 1996; 131(11):1141–1146; discussion 1147.
14.
go back to reference Botha AJ, Moore FA, Moore EE, Kim FJ, Banerjee A, Peterson VM. Postinjury neutrophil priming and activation: an early vulnerable window. Surgery. 1995; 118(2):358–364; discussion 364–355. Botha AJ, Moore FA, Moore EE, Kim FJ, Banerjee A, Peterson VM. Postinjury neutrophil priming and activation: an early vulnerable window. Surgery. 1995; 118(2):358–364; discussion 364–355.
15.
go back to reference Giannoudis PV, Smith RM. The effects of trauma and sepsis on soluble l-selectin and cell surface expression on l-selectin and CD11b on leukocytes. J Trauma. 1999;46(5):984.PubMedCrossRef Giannoudis PV, Smith RM. The effects of trauma and sepsis on soluble l-selectin and cell surface expression on l-selectin and CD11b on leukocytes. J Trauma. 1999;46(5):984.PubMedCrossRef
16.
go back to reference Giannoudis PV, Smith RM, Banks RE, Windsor AC, Dickson RA, Guillou PJ. Stimulation of inflammatory markers after blunt trauma. Br J Surg. 1998;85(7):986–90.PubMedCrossRef Giannoudis PV, Smith RM, Banks RE, Windsor AC, Dickson RA, Guillou PJ. Stimulation of inflammatory markers after blunt trauma. Br J Surg. 1998;85(7):986–90.PubMedCrossRef
17.
go back to reference Seekamp A, van Griensven M, Hildebrandt F, Brauer N, Jochum M, Martin M. The effect of trauma on neutrophil l-selectin expression and sl-selectin serum levels. Shock. 2001;15(4):254–60.PubMedCrossRef Seekamp A, van Griensven M, Hildebrandt F, Brauer N, Jochum M, Martin M. The effect of trauma on neutrophil l-selectin expression and sl-selectin serum levels. Shock. 2001;15(4):254–60.PubMedCrossRef
18.
go back to reference van Griensven M, Barkhausen T, Hildebrand F, Grotz M, Mahlke L, Meier R, et al. l-Selectin shows time and gender dependency in association with MODS. Injury. 2004;35(11):1087–95. van Griensven M, Barkhausen T, Hildebrand F, Grotz M, Mahlke L, Meier R, et al. l-Selectin shows time and gender dependency in association with MODS. Injury. 2004;35(11):1087–95.
19.
go back to reference Fowler AA, Fisher BJ, Centor RM, Carchman RA. Development of the adult respiratory distress syndrome: progressive alteration of neutrophil chemotactic and secretory processes. Am J Pathol. 1984;116(3):427–35.PubMed Fowler AA, Fisher BJ, Centor RM, Carchman RA. Development of the adult respiratory distress syndrome: progressive alteration of neutrophil chemotactic and secretory processes. Am J Pathol. 1984;116(3):427–35.PubMed
20.
go back to reference Hietbrink F, Koenderman L, Althuizen M, Leenen LP. Modulation of the innate immune response after trauma visualised by a change in functional PMN phenotype. Injury. 2009;40(8):851–5.PubMedCrossRef Hietbrink F, Koenderman L, Althuizen M, Leenen LP. Modulation of the innate immune response after trauma visualised by a change in functional PMN phenotype. Injury. 2009;40(8):851–5.PubMedCrossRef
21.
go back to reference Kanters D, ten Hove W, Luijk B, van Aalst C, Schweizer RC, Lammers JW, et al. Expression of activated Fc gamma RII discriminates between multiple granulocyte-priming phenotypes in peripheral blood of allergic asthmatic subjects. J Allergy Clin Immunol. 2007;120(5):1073–81.PubMedCrossRef Kanters D, ten Hove W, Luijk B, van Aalst C, Schweizer RC, Lammers JW, et al. Expression of activated Fc gamma RII discriminates between multiple granulocyte-priming phenotypes in peripheral blood of allergic asthmatic subjects. J Allergy Clin Immunol. 2007;120(5):1073–81.PubMedCrossRef
22.
go back to reference Baker SP, O’Neill B, Haddon W Jr, Long WB. The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. J Trauma. 1974;14(3):187–96.PubMedCrossRef Baker SP, O’Neill B, Haddon W Jr, Long WB. The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. J Trauma. 1974;14(3):187–96.PubMedCrossRef
23.
go back to reference Osler T, Baker SP, Long W A. Modification of the injury severity score that both improves accuracy and simplifies scoring. J Trauma. 1997; 43(6):922–925; discussion 925–926. Osler T, Baker SP, Long W A. Modification of the injury severity score that both improves accuracy and simplifies scoring. J Trauma. 1997; 43(6):922–925; discussion 925–926.
24.
go back to reference Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13(10):818–29.PubMedCrossRef Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13(10):818–29.PubMedCrossRef
25.
go back to reference Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, et al. Report of the American-European Consensus Conference on Acute Respiratory Distress Syndrome: definitions, mechanisms, relevant outcomes, and clinical trial coordination. Consensus Committee. J Crit Care. 1994;9:72–81. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, et al. Report of the American-European Consensus Conference on Acute Respiratory Distress Syndrome: definitions, mechanisms, relevant outcomes, and clinical trial coordination. Consensus Committee. J Crit Care. 1994;9:72–81.
26.
go back to reference Pillay J, Ramakers BP, Kamp VM, Loi AL, Lam SW, Hietbrink F, et al. Functional heterogeneity and differential priming of circulating neutrophils in human experimental endotoxemia. J Leukoc Biol. 2010; 88(1) 211–220. Pillay J, Ramakers BP, Kamp VM, Loi AL, Lam SW, Hietbrink F, et al. Functional heterogeneity and differential priming of circulating neutrophils in human experimental endotoxemia. J Leukoc Biol. 2010; 88(1) 211–220.
27.
go back to reference Koenderman L, Kanters D, Maesen B, Raaijmakers J, Lammers JW, de Kruif J, et al. Monitoring of neutrophil priming in whole blood by antibodies isolated from a synthetic phage antibody library. J Leukoc Biol. 2000;68(1):58–64.PubMed Koenderman L, Kanters D, Maesen B, Raaijmakers J, Lammers JW, de Kruif J, et al. Monitoring of neutrophil priming in whole blood by antibodies isolated from a synthetic phage antibody library. J Leukoc Biol. 2000;68(1):58–64.PubMed
28.
go back to reference Koenderman L, Hermans SW, Capel PJ, van de Winkel JG. Granulocyte-macrophage colony-stimulating factor induces sequential activation and deactivation of binding via a low-affinity IgG Fc receptor, hFc gamma RII, on human eosinophils. Blood. 1993;81(9):2413–9.PubMed Koenderman L, Hermans SW, Capel PJ, van de Winkel JG. Granulocyte-macrophage colony-stimulating factor induces sequential activation and deactivation of binding via a low-affinity IgG Fc receptor, hFc gamma RII, on human eosinophils. Blood. 1993;81(9):2413–9.PubMed
29.
go back to reference Scannell G, Waxman K, Vaziri ND, Zhang J, Kaupke CJ, Jalali M, et al. Effects of trauma on leukocyte intercellular adhesion molecule-1, CD11b, and CD18 expressions. J Trauma. 1995;39(4):641–4.PubMedCrossRef Scannell G, Waxman K, Vaziri ND, Zhang J, Kaupke CJ, Jalali M, et al. Effects of trauma on leukocyte intercellular adhesion molecule-1, CD11b, and CD18 expressions. J Trauma. 1995;39(4):641–4.PubMedCrossRef
30.
go back to reference White-Owen C, Alexander JW, Babcock GF. Reduced expression of neutrophil CD11b and CD16 after severe traumatic injury. J Surg Res. 1992;52(1):22–6.PubMedCrossRef White-Owen C, Alexander JW, Babcock GF. Reduced expression of neutrophil CD11b and CD16 after severe traumatic injury. J Surg Res. 1992;52(1):22–6.PubMedCrossRef
31.
go back to reference Doroshenko T, Chaly Y, Savitskiy V, Maslakova O, Portyanko A, Gorudko I, et al. Phagocytosing neutrophils down-regulate the expression of chemokine receptors CXCR1 and CXCR2. Blood. 2002;100(7):2668–71.PubMedCrossRef Doroshenko T, Chaly Y, Savitskiy V, Maslakova O, Portyanko A, Gorudko I, et al. Phagocytosing neutrophils down-regulate the expression of chemokine receptors CXCR1 and CXCR2. Blood. 2002;100(7):2668–71.PubMedCrossRef
32.
go back to reference Pillay J, Hietbrink F, Koenderman L, Leenen LP. The systemic inflammatory response induced by trauma is reflected by multiple phenotypes of blood neutrophils. Injury. 2007;38(12):1365–72.PubMedCrossRef Pillay J, Hietbrink F, Koenderman L, Leenen LP. The systemic inflammatory response induced by trauma is reflected by multiple phenotypes of blood neutrophils. Injury. 2007;38(12):1365–72.PubMedCrossRef
33.
go back to reference Morris AC, Kefala K, Wilkinson TS, Dhaliwal K, Farrell L, Walsh T, et al. C5a mediates peripheral blood neutrophil dysfunction in critically ill patients. AJRCCM. 2009;180:19–28. Morris AC, Kefala K, Wilkinson TS, Dhaliwal K, Farrell L, Walsh T, et al. C5a mediates peripheral blood neutrophil dysfunction in critically ill patients. AJRCCM. 2009;180:19–28.
34.
go back to reference Richardson RM, Marjoram RJ, Barak LS, Snyderman R. Role of the cytoplasmic tails of CXCR1 and CXCR2 in mediating leukocyte migration, activation, and regulation. J Immunol. 2003;170(6):2904–11.PubMed Richardson RM, Marjoram RJ, Barak LS, Snyderman R. Role of the cytoplasmic tails of CXCR1 and CXCR2 in mediating leukocyte migration, activation, and regulation. J Immunol. 2003;170(6):2904–11.PubMed
35.
go back to reference Elghetany MT. Surface antigen changes during normal neutrophilic development: a critical review. Blood Cells Mol Dis. 2002;28(2):260–74.PubMedCrossRef Elghetany MT. Surface antigen changes during normal neutrophilic development: a critical review. Blood Cells Mol Dis. 2002;28(2):260–74.PubMedCrossRef
36.
go back to reference Biffl WL, West KE, Moore EE, Gonzalez RJ, Carnaggio R, Offner PJ, et al. Neutrophil apoptosis is delayed by trauma patients’ plasma via a mechanism involving proinflammatory phospholipids and protein kinase C. Surg Infect (Larchmt). 2001; 2(4):289–293; discussion 294–285. Biffl WL, West KE, Moore EE, Gonzalez RJ, Carnaggio R, Offner PJ, et al. Neutrophil apoptosis is delayed by trauma patients’ plasma via a mechanism involving proinflammatory phospholipids and protein kinase C. Surg Infect (Larchmt). 2001; 2(4):289–293; discussion 294–285.
37.
go back to reference Nolan B, Collette H, Baker S, Duffy A, De M, Miller C, et al. Inhibition of neutrophil apoptosis after severe trauma is NFkappabeta dependent. J Trauma. 2000; 48(4):599–604; discussion 604–595. Nolan B, Collette H, Baker S, Duffy A, De M, Miller C, et al. Inhibition of neutrophil apoptosis after severe trauma is NFkappabeta dependent. J Trauma. 2000; 48(4):599–604; discussion 604–595.
38.
go back to reference Pepe PE, Potkin RT, Reus DH, Hudson LD, Carrico CJ. Clinical predictors of the adult respiratory distress syndrome. Am J Surg. 1982;144(1):124–30.PubMedCrossRef Pepe PE, Potkin RT, Reus DH, Hudson LD, Carrico CJ. Clinical predictors of the adult respiratory distress syndrome. Am J Surg. 1982;144(1):124–30.PubMedCrossRef
39.
go back to reference Wind J, Versteegt J, Twisk J, van der Werf TS, Bindels AJ, Spijkstra JJ, et al. Epidemiology of acute lung injury and acute respiratory distress syndrome in The Netherlands: a survey. Respir Med. 2007;101(10):2091–8.PubMedCrossRef Wind J, Versteegt J, Twisk J, van der Werf TS, Bindels AJ, Spijkstra JJ, et al. Epidemiology of acute lung injury and acute respiratory distress syndrome in The Netherlands: a survey. Respir Med. 2007;101(10):2091–8.PubMedCrossRef
40.
go back to reference Hoth JJ, Martin RS, Yoza BK, Wells JD, Meredith JW, McCall CE. Pulmonary contusion primes systemic innate immunity responses. J Trauma. 2009; 67(1):14–21; discussion 21–12. Hoth JJ, Martin RS, Yoza BK, Wells JD, Meredith JW, McCall CE. Pulmonary contusion primes systemic innate immunity responses. J Trauma. 2009; 67(1):14–21; discussion 21–12.
Metadata
Title
Isolated blunt chest injury leads to transient activation of circulating neutrophils
Authors
T. Visser
F. Hietbrink
K. M. Groeneveld
L. Koenderman
L. P. H. Leenen
Publication date
01-04-2011
Publisher
Springer-Verlag
Published in
European Journal of Trauma and Emergency Surgery / Issue 2/2011
Print ISSN: 1863-9933
Electronic ISSN: 1863-9941
DOI
https://doi.org/10.1007/s00068-010-0041-x

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