Immunosuppression following surgical and traumatic injury

Surgery Today

Volumn 40, Issue 9, 2010, Pages 793-808

  Kimura, Fumio ^a   Shimizu, Hiroaki ^a   Yoshidome, Hiroyuki ^a   Ohtsuka, Masayuki ^a   Miyazaki, Masaru ^a  

^a CHIBA UNIVERSITY   (Japan)

Author keywords

Monocytes macrophages; Organ failure; Pattern recognition receptors; Polymorphonuclear neutrophils; Sepsis; Surgery; T lymphocytes; Trauma

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; NITRIC OXIDE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; PURINERGIC RECEPTOR; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ACUTE LUNG INJURY; ADAPTIVE IMMUNITY; ADULT RESPIRATORY DISTRESS SYNDROME; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; CELL FUNCTION; CELLULAR IMMUNITY; COMPENSATORY ANTIINFLAMMATORY RESPONSE SYNDROME; HUMAN; IMMUNE DEFICIENCY; IMMUNOREGULATION; INCIDENCE; INFLAMMATION; INJURY; INNATE IMMUNITY; LYMPHOCYTE; MACROPHAGE; MONOCYTE; MULTIPLE ORGAN FAILURE; NEUTROPHIL; PHAGOCYTOSIS; PNEUMONIA; POSTOPERATIVE COMPLICATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; SEPSIS; SURGERY; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TH1 CELL; TH17 CELL; TH2 CELL;

ACUTE LUNG INJURY; ADAPTIVE IMMUNITY; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; MULTIPLE ORGAN FAILURE; NEUTROPHILS; POSTOPERATIVE COMPLICATIONS; RECEPTORS, PATTERN RECOGNITION; SEPSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TOLL-LIKE RECEPTORS; WOUNDS AND INJURIES;

EID: 77956940456     PISSN: 09411291     EISSN: 14362813     Source Type: Journal    
DOI: 10.1007/s00595-010-4323-z     Document Type: Review

References (160)

1. E. Dixon C.M. Vollmer Jr A. Sahajpal M. Cattral D. Grant C. Doig, et al. 2005 An aggressive surgical approach leads to improved survival in patients with gallbladder cancer: a 12-year study at a North American Center Ann Surg 241 385 394 15729060
2. H. Shigeta M. Nagino J. Kamiya K. Uesaka T. Sano H. Yamamoto, et al. 2002 Bacteremia after hepatectomy: an analysis of a singlecenter, 10-year experience with 407 patients Langenbecks Arch Surg 387 117 124 12172855
3. C.M. Schmidt E.S. Powell C.T. Yiannoutsos T.J. Howard E.A. Wiebke C.A. Wiesenauer, et al. 2004 Pancreaticoduodenectomy: a 20-year experience in 516 patients Arch Surg 139 718 725 15249403
4. C.J. Yeo J.L. Cameron K.D. Lillemoe T.A. Sohn K.A. Campbell P.K. Sauter, et al. 2002 Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality Ann Surg 236 355 366 12192322
5. J. Busquets J. Fabregat F.G. Borobia R. Jorba C. Valls T. Serrano, et al. 2010 Organ-preserving surgery for benign lesions and low-grade malignancies of the pancreatic head: a matched case-control study Surg Today 40 125 131 20107951
6. M.K. Angele I.H. Chaudry 2005 Surgical trauma and immunosuppression: pathophysiology and potential immunomodulatory approaches Langenbecks Arch Surg 390 333 341 15995884
7. N. Ni Choileain H.P. Redmond 2006 Cell response to surgery Arch Surg 141 1132 1140 17116807
8. N. Ni Choileain H.P. Redmond 2006 The immunological consequences of injury Surgeon 4 23 31 16459497
9. A. Lenz G.A. Franklin W.G. Cheadle 2007 Systemic inflammation after trauma Injury 38 1336 1345 18048040
10. R.C. Bone 1996 Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS) Ann Intern Med 125 680 687 8849154
11. F.A. Moore E.E. Moore 1995 Evolving concepts in the pathogenesis of postinjury multiple organ failure Surg Clin North Am 75 257 277 7899997
12. S.K. Tschoeke M. Hellmuth A. Hostmann W. Ertel A. Oberholzer 2007 The early second hit in trauma management augments the proinflammatory immune response to multiple injuries J Trauma 62 1396 1403 17563655
13. W.L. Biffl E.E. Moore F.A. Moore V.M. Peterson 1996 Interleukin-6 in the injured patient. Marker of injury or mediator of inflammation? Ann Surg 224 647 664 8916880
14. R.J. Baigrie P.M. Lamont D. Kwiatkowski M.J. Dallman P.J. Morris 1992 Systemic cytokine response after major surgery Br J Surg 79 757 760 1393463
15. L.M. Gale S.R. McColl 1999 Chemokines: extracellular messengers for all occasions? Bioessays 21 17 28 10070251
16. M. Strüber J.T. Cremer B. Gohrbandt C. Hagl M. Jankowski B. Völker, et al. 1999 Human cytokine responses to coronary artery bypass grafting with and without cardiopulmonary bypass Ann Thorac Surg 68 1330 1335 10543502
17. A.K. Lehmann A. Halstensen S. Sørnes O. Røkke A. Waage 1995 High levels of interleukin 10 in serum are associated with fatality in meningococcal disease Infect Immun 63 2109 2112 7768588
18. A. Marchant M.L. Alegre A. Hakim G. Piérard G. Marécaux G. Friedman, et al. 1995 Clinical and biological significance of interleukin-10 plasma levels in patients with septic shock J Clin Immunol 15 266 273 8537471
19. M. Howard T. Muchamuel S. Andrade S. Menon 1993 Interleukin 10 protects mice from lethal endotoxemia J Exp Med 177 1205 1208 8459215
20. S. Florquin Z. Amraoui D. Abramowicz M. Goldman 1994 Systemic release and protective role of IL-10 in staphylococcal enterotoxin B-induced shock in mice J Immunol 153 2618 2623 7915740 (Pubitemid 24278131)
21. J.T. DiPiro T.R. Howdieshell J.K. Goddard D.B. Callaway R.G. Hamilton A.R. Mansberger Jr 1995 Association of interleukin-4 plasma levels with traumatic injury and clinical course Arch Surg 130 1159 1162 7487457
22. C. Wanidworanun W. Strober 1993 Predominant role of tumor necrosis factor-alpha in human monocyte IL-10 synthesis J Immunol 151 6853 6861 8258695
23. N.C. Riedemann R.F. Guo P.A. Ward 2003 Novel strategies for the treatment of sepsis Nat Med 9 517 524 12724763
24. P.J. Offner E.E. Moore D. Ciesla 2002 The adrenal response after severe trauma Am J Surg 184 649 653 12488202
25. D. Keh T. Boehnke S. Weber-Cartens C. Schulz O. Ahlers S. Bercker, et al. 2003 Immunologic and hemodynamic effects of "low-dose" hydrocortisone in septic shock: a double-blind, randomized, placebo-controlled, crossover study Am J Respir Crit Care Med 167 512 520 12426230
26. T. Roger M.P. Glauser T. Calandra 2001 Macrophage migration inhibitory factor (MIF) modulates innate immune responses induced by endotoxin and Gram-negative bacteria J Endotoxin Res 7 456 460 11753217
27. Z.N. Kain Z. Zimolo G. Heninger 1999 Leptin and the perioperative neuroendocrinological stress response J Clin Endocrinol Metab 84 2438 2442 10404818
28. V. Sánchez-Margalet C. Martín-Romero J. Santos-Alvarez R. Goberna S. Najib C. Gonzalez-Yanes 2003 Role of leptin as an immunomodulator of blood mononuclear cells: mechanisms of action Clin Exp Immunol 133 11 19 12823272
29. F. Kimura H. Shimizu H. Yoshidome M. Ohtsuka A. Kato H. Yoshitomi, et al. 2006 Circulating cytokines, chemokines, and stress hormones are increased in patients with organ dysfunction following liver resection J Surg Res 133 102 112 16386757
30. F. Kimura M. Miyazaki T. Suwa T. Sugiura T. Shinoda H. Itoh, et al. 1998 Plasma concentration of cytokine antagonists in patients with infection following liver resection Br J Surg 85 1631 1635 9876064
31. M.F. Osuchowski K. Welch J. Siddiqui D.G. Remick 2006 Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality J Immunol 177 1967 1974 16849510
32. F. Martinon J. Tschopp 2005 NLRs join TLRs as innate sensors of pathogens Trends Immunol 26 447 454 15967716
33. F.Y. Liew D. Xu E.K. Brint L.A. O'Neill 2005 Negative regulation of toll-like receptor-mediated immune responses Nat Rev Immunol 5 446 458 15928677
34. M. Lamkanfi T.D. Kanneganti L. Franchi G. Nunez 2007 Caspase-1 inflammasomes in infection and inflammation J Leukoc Biol 82 220 225 17442855
35. T. Kawai S. Akira 2006 Innate immune recognition of viral infection Nat Immunol 7 131 137 16424890 (Pubitemid 43135878)
36. L. Härter L. Mica R. Stocker O. Trentz M. Keel 2004 Increased expression of toll-like receptor-2 and -4 on leukocytes from patients with sepsis Shock 22 403 409 15489631
37. S. Shalhub C.E. Junker S.D. Imahara M.N. Mindrinos S. Dissanaike G.E. O'Keefe 2009 Variation in the TLR4 gene influences the risk of organ failure and shock posttrauma: a cohort study J Trauma 66 115 122 19131814
38. L.A. Carneiro J.G. Magalhaes I. Tattoli D.J. Philpott L.H. Travassos 2008 Nod-like proteins in inflammation and disease J Pathol 214 136 148 18161746
39. F. Martinon 2007 Orchestration of pathogen recognition by inflammasome diversity: Variations on a common theme Eur J Immunol 37 3003 3006 17960661
40. F.S. Sutterwala Y. Ogura R.A. Flavell 2007 The inflammasome in pathogen recognition and inflammation J Leukoc Biol 82 259 264 17470531
41. D.K. Podolsky 2002 Inflammatory bowel disease N Engl J Med 347 417 429 12167685
42. R.J. Fahy M.C. Exline M.A. Gavrilin N.Y. Bhatt B.Y. Besecker A. Sarkar, et al. 2008 Inflammasome mRNA expression in human monocytes during early septic shock Am J Respir Crit Care Med 177 983 988 18263805
43. A. Rubartelli M.T. Lotze 2007 Inside, outside, upside down: damageassociated molecular-pattern molecules (DAMPs) and redox Trends Immunol 28 429 436 17845865
44. M.E. Bianchi 2007 DAMPs, PAMPs and alarmins: all we need to know about danger J. Leukoc. Biol 81 1 5 17032697
45. T. Bonaldi F. Talamo P. Scaffidi D. Ferrera A. Porto A. Bachi, et al. 2003 Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion EMBO J 22 5551 5560 14532127
46. H. Wang H. Yang K.J. Tracey 2004 Extracellular role of HMGB1 in inflammation and sepsis J Intern Med 255 320 331 14871456
47. E. Abraham J. Arcaroli A. Carmody H. Wang K.J. Tracey 2000 HMG-1 as a mediator of acute lung inflammation J Immunol 165 2950 2954 10975801
48. J.Y. Kim J.S. Park D. Strassheim I. Douglas F. Diaz del Valle K. Asehnoune, et al. 2005 HMGB1 contributes to the development of acute lung injury after hemorrhage Am J Physiol Lung Cell Mol Physiol 288 L958 965 15640285
49. A. Tsung R. Sahai H. Tanaka A. Nakao M.P. Fink M.T. Lotze, et al. 2005 The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion J Exp Med 201 1135 1143 15795240
50. H. Wang O. Bloom M. Zhang J.M. Vishnubhakat M. Ombrellino J. Che, et al. 1999 HMG-1 as a late mediator of endotoxin lethality in mice Science 285 5425 248 251 10398600
51. M. Ombrellino H. Wang M.S. Ajemian A. Talhouk L.A. Scher S.G. Friedman, et al. 1999 Increased serum concentrations of high-mobility-group protein 1 in haemorrhagic shock Lancet 354 9188 1446 1447 10543678
52. H. Ueno T. Matsuda S. Hashimoto F. Amaya Y. Kitamura M. Tanaka, et al. 2004 Contributions of high mobility group box protein in experimental and clinical acute lung injury Am J Respir Crit Care Med 170 1310 1316 15374839
53. J. Sundén-Cullberg A. Norrby-Teglund A. Rouhiainen H. Rauvala G. Herman K.J. Tracey, et al. 2005 Persistent elevation of high mobility group box-1 protein (HMGB1) in patients with severe sepsis and septic shock Crit Care Med 33 564 573 15753748
54. W. Chen U. Syldath K. Bellmann V. Burkart H. Kolb 1999 Human 60-kDa heat-shock protein: a danger signal to the innate immune system J Immunol 162 3212 3219 10092772
55. K. Ohashi V. Burkart S. Flohe H. Kolb 2000 Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex J Immunol 164 558 561 10623794
56. B. Dybdahl A. Wahba E. Lien T.H. Flo A. Waage N. Qureshi, et al. 2002 Inflammatory response after open heart surgery: release of heat-shock protein 70 and signaling through toll-like receptor-4 Circulation 105 685 690 11839622
57. F. Kimura H. Itoh S. Ambiru H. Shimizu A. Togawa H. Yoshidome, et al. 2004 Circulating heat-shock protein 70 is associated with postoperative infection and organ dysfunction after liver resection Am J Surg 187 777 784 15191875
58. M.J. Bours E.L. Swennen F. Di Virgilio B.N. Cronstein P.C. Dagnelie 2006 Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation Pharmacol Ther 112 358 404 16784779
59. M.V. Sitkovsky A. Ohta 2005 The "danger" sensors that STOP the immune response: the A2 adenosine receptors? Trends Immunol 26 299 304 15922945
60. S. Deaglio K.M. Dwyer W. Gao D. Friedman A. Usheva A. Erat, et al. 2007 Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression J Exp Med 204 1257 1265 17502665
61. W.W. van Maren J.F. Jacobs I.J. de Vries S. Nierkens G.J. Adema 2008 Toll-like receptor signalling on Tregs: to suppress or not to suppress? Immunology 124 445 452 18540962
62. A.J. Seely J.L. Pascual N.V. Christou 2003 Science review: Cell membrane expression (connectivity) regulates neutrophil delivery, function and clearance Crit Care 7 291 307 12930553
63. L. Fialkow Y. Wang G.P. Downey 2007 Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function Free Radic Biol Med 42 153 164 17189821
64. C.H. Wakefield P.D. Carey S. Foulds J.R. Monson P.J. Guillou 1993 Polymorphonuclear leukocyte activation. An early marker of the postsurgical sepsis response Arch Surg 128 390 395 8096129
65. M.F. Jimenez R.W. Watson J. Parodo D. Evans D. Foster M. Steinberg, et al. 1997 Dysregulated expression of neutrophil apoptosis in the systemic inflammatory response syndrome Arch Surg 132 1263 1269 9403528
66. K. Maekawa S. Futami M. Nishida T. Terada H. Inagawa S. Suzuki, et al. 1998 Effects of trauma and sepsis on soluble L-selectin and cell surface expression of L-selectin and CD11b J Trauma 44 460 468 9529172
67. G. Quaid C. Cave M.A. Williams R.F. Hennigan G. Bokoch J.S. Solomkin 2001 Mechanisms of human neutrophil oxidant production after severe injury Surgery 130 669 675 11602898
68. S. Foulds M. Mireskandari P. Kalu W. Jackson N.J. Cheshire A.O. Mansfield, et al. 1998 Visceral ischemia and neutrophil activation in sepsis and organ dysfunction J Surg Res 75 170 176 9655091
69. S. Foulds N.J. Cheshire M. Schachter J.H. Wolfe A.O. Mansfield 1997 Endotoxin related early neutrophil activation is associated with outcome after thoracoabdominal aortic aneurysm repair Br J Surg 84 172 177 9052426
70. D.A. Partrick E.E. Moore D.A. Fullerton C.C. Barnett Jr D.R. Meldrum C.C. Silliman 1999 Cardiopulmonary bypass renders patients at risk for multiple organ failure via early neutrophil priming and late neutrophil disability J Surg Res 86 42 49 10452867
71. R. Bhatia C. Dent N. Topley I. Pallister 2006 Neutrophil priming for elastase release in adult blunt trauma patients J Trauma 60 590 596 16531859
72. S. Gando T. Kameue N. Matsuda A. Sawamura M. Hayakawa H. Kato 2004 Systemic inflammation and disseminated intravascular coagulation in early stage of ALI and ARDS: role of neutrophil and endothelial activation Inflammation 28 237 244 15673166
73. Y. Inoue H. Tanaka H. Ogura I. Ukai K. Fujita H. Hosotsubo, et al. 2006 A neutrophil elastase inhibitor, sivelestat, improves leukocyte deformability in patients with acute lung injury J Trauma 60 936 943 16688053 (Pubitemid 43778617)
74. S. Gando T. Kameue N. Matsuda M. Hayakawa T. Ishitani Y. Morimoto, et al. 2002 Combined activation of coagulation and inflammation has an important role in multiple organ dysfunction and poor outcome after severe trauma Thromb Haemost 88 943 949 12529743
75. D. Rittirsch M.A. Flierl P.A. Ward 2008 Harmful molecular mechanisms in sepsis Nat Rev Immunol 8 776 787 18802444
76. T.S. Olson K. Ley 2002 Chemokines and chemokine receptors in leukocyte trafficking Am J Physiol Regul Integr Comp Physiol 283 R7 28 12069927
77. J. Reutershan K. Ley 2004 Bench-to-bedside review: acute respiratory distress syndrome-how neutrophils migrate into the lung Crit Care 8 453 461 15566616
78. J. Villard F. Dayer-Pastore J. Hamacher J.D. Aubert S. Schlegel-Haueter L.P. Nicod 1995 GRO alpha and interleukin-8 in Pneumocystis carinii or bacterial pneumonia and adult respiratory distress syndrome Am J Respir Crit Care Med 152 1549 1554 7582292
79. W.C. Tsai R.M. Strieter B. Mehrad M.W. Newstead X. Zeng T.J. Standiford 2000 CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia Infect Immun 68 4289 4296 10858247
80. J.M. Adams C.J. Hauser D.H. Livingston R.F. Lavery Z. Fekete E.A. Deitch 2001 Early trauma polymorphonuclear neutrophil responses to chemokines are associated with development of sepsis, pneumonia, and organ failure J Trauma 51 452 456 11535890
81. M.H. Tarlowe A. Duffy K.B. Kannan K. Itagaki R.F. Lavery D.H. Livingston, et al. 2005 Prospective study of neutrophil chemokine responses in trauma patients at risk for pneumonia Am J Respir Crit Care Med 171 753 759 15618463
82. K.A. Brown S.D. Brain J.D. Pearson J.D. Edgeworth S.M. Lewis D.F. Treacher 2006 Neutrophils in development of multiple organ failure in sepsis Lancet 368 9530 157 169 16829300
83. C.A. Terregino C.L. Lubkin S.R. Thom 1997 Impaired neutrophil adherence as an early marker of systemic inflammatory response syndrome and severe sepsis Ann Emerg Med 29 400 403 9055781
84. S.M. Arraes M.S. Freitas S.V. da Silva H.A. de Paula Neto J.C. Alves-Filho M. Auxiliadora Martins, et al. 2006 Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation Blood 108 2906 29013 16849637
85. A. Rot U.H. von Andrian 2004 Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells Annu Rev Immunol 22 891 928 15032599
86. P.S. Martins E.G. Kallas M.C. Neto M.A. Dalboni S. Blecher R. Salomão 2003 Upregulation of reactive oxygen species generation and phagocytosis, and increased apoptosis in human neutrophils during severe sepsis and septic shock Shock 20 208 212 12923490
87. I. Kaufmann A. Hoelzl F. Schliephake T. Hummel A. Chouker K. Peter, et al. 2006 Polymorphonuclear leukocyte dysfunction syndrome in patients with increasing sepsis severity Shock 26 254 261 16912650
88. D.D. Danikas M. Karakantza G.L. Theodorou G.C. Sakellaropoulos C.A. Gogos 2008 Prognostic value of phagocytic activity of neutrophils and monocytes in sepsis. Correlation to CD64 and CD14 antigen expression Clin Exp Immunol 154 87 97 18727624
89. W. van der Meer P. Pickkers C.S. Scott J.G. van der Hoeven J.K. Gunnewiek 2007 Hematological indices, inflammatory markers and neutrophil CD64 expression: comparative trends during experimental human endotoxemia J Endotoxin Res 13 94 100 17621550
90. R. Taneja A.P. Sharma M.B. Hallett G.P. Findlay M.R. Morris 2008 Immature circulating neutrophils in sepsis have impaired phagocytosis and calcium signaling Shock 30 618 622 18496237
91. N.V. Serbina T. Jia T.M. Hohl E.G. Pamer 2008 Monocyte-mediated defense against microbial pathogens Annu Rev Immunol 26 421 452 18303997
92. S. Gordon P.R. Taylor 2005 Monocyte and macrophage heterogeneity Nat Rev Immunol 5 953 964 16322748
93. M. Benoit B. Desnues J.L. Mege 2008 Macrophage polarization in bacterial infections J Immunol 181 3733 3739 18768823
94. D.M. Mosser J.P. Edwards 2008 Exploring the full spectrum of macrophage activation Nat Rev Immunol 8 958 969 19029990
95. J.S. Gerber D.M. Mosser 2001 Reversing lipopolysaccharide toxicity by ligating the macrophage Fc? receptors J Immunol 166 6861 6868 11359846
96. Z. Spolarics M. Siddiqi J.H. Siegel Z.C. Garcia D.S. Stein T. Denny, et al. 2003 Depressed interleukin-12-producing activity by monocytes correlates with adverse clinical course and a shift toward Th2-type lymphocyte pattern in severely injured male trauma patients Crit Care Med 31 1722 1729 12794411
97. H. Weighardt C.D. Heidecke A. Westerholt K. Emmanuilidis S. Maier M. Veit, et al. 2002 Impaired monocyte IL-12 production before surgery as a predictive factor for the lethal outcome of postoperative sepsis Ann Surg 235 560 567 11923613
98. M. Ditschkowski E. Kreuzfelder V. Rebmann S. Ferencik M. Majetschak E.N. Schmid, et al. 1999 HLA-DR expression and soluble HLA-DR levels in septic patients after trauma Ann Surg 229 246 254 10024107
99. C.H. Wakefield P.D. Carey S. Foulds J.R. Monson P.J. Guillou 1993 Changes in major histocompatibility complex class II expression in monocytes and T cells of patients developing infection after surgery Br J Surg 80 205 209 8443652
100. C. Schinkel R. Sendtner S. Zimmer E. Faist 1998 Functional analysis of monocyte subsets in surgical sepsis J Trauma 44 743 748 9603073
101. F. Venet S. Tissot A.L. Debard C. Faudot C. Crampé A. Pachot, et al. 2007 Decreased monocyte human leukocyte antigen-DR expression after severe burn injury: Correlation with severity and secondary septic shock Crit Care Med 35 1910 1917 17568330
102. K. Tschaikowsky M. Hedwig-Geissing A. Schiele F. Bremer M. Schywalsky J. Schüttler 2002 Coincidence of pro- and anti-inflammatory responses in the early phase of severe sepsis: Longitudinal study of mononuclear histocompatibility leukocyte antigen-DR expression, procalcitonin, C-reactive protein, and changes in T-cell subsets in septic and postoperative patients Crit Care Med 30 1015 12006796
103. G. Monneret M.E. Finck F. Venet A.L. Debard J. Bohé J. Bienvenu, et al. 2004 The anti-inflammatory response dominates after septic shock: Association of low monocyte HLA-DR expression and high interleukin-10 concentration Immunol Lett 95 193 198 15388260
104. T. Fumeaux J. Pugin 2002 Role of interleukin-10 in the intracellular sequestration of human leukocyte antigen-DR in monocytes during septic shock Am J Respir Crit Care Med 166 1475 1482 12406851
105. A. Lekkou M. Karakantza A. Mouzaki F. Kalfarentzos C.A. Gogos 2004 Cytokine production and monocyte HLA-DR expression as predictors of outcome for patients with community-acquired severe infections Clin Diagn Lab Immunol 11 161 167 14715564
106. R. Abe H. Hirasawa S. Oda T. Sadahiro M. Nakamura E. Watanabe, et al. 2008 Up-regulation of interleukin-10 mRNA expression in peripheral leukocytes predicts poor outcome and diminished human leukocyte antigen-DR expression on monocytes in septic patients J Surg Res 147 1 8 17720196
107. R. de Waal Malefyt J. Haanen H. Spits M.G. Roncarolo A. te Velde C. Figdor, et al. 1991 Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via down-regulation of class II major histocompatibility complex expression J Exp Med 174 915 1655948
108. A.S. Morel G. Coulton M. Londei 2002 Regulation of major histocompatibility complex class II synthesis by interleukin-10 Immunology 106 229 236 12047752
109. M. Aste-Amezaga X. Ma A. Sartori G. Trinchieri 1998 Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10 J Immunol 160 5936 5944 9637507
110. F. Randow U. Syrbe C. Meisel D. Krausch H. Zuckermann C. Platzer, et al. 1995 Mechanism of endotoxin desensitization: involvement of interleukin 10 and transforming growth factor beta J Exp Med 181 1887 1892 7722463
111. W.D. Döcke F. Randow U. Syrbe D. Krausch K. Asadullah P. Reinke, et al. 1997 Monocyte deactivation in septic patients: restoration by IFN-gamma treatment Nat Med 3 678 681 9176497
112. M. Astiz D. Saha D. Lustbader R. Lin E. Rackow 1996 Monocyte response to bacterial toxins, expression of cell surface receptors, and release of anti-inflammatory cytokines during sepsis J Lab Clin Med 128 594 600 8960643
113. T. Sfeir D.C. Saha M. Astiz E.C. Rackow 2001 Role of interleukin-10 in monocyte hyporesponsiveness associated with septic shock Crit Care Med 29 129 133 11176172
114. H. Tsujimoto S. Ono T. Majima P.A. Efron M. Kinoshita H. Hiraide, et al. 2006 Differential toll-like receptor expression after ex vivo lipopolysaccharide exposure in patients with sepsis and following surgical stress Clin Immunol 119 180 187 16517212
115. B. Schaaf K. Luitjens T. Goldmann T. van Bremen F. Sayk C. Dodt, et al. 2009 Mortality in human sepsis is associated with downregulation of Toll-like receptor 2 and CD14 expression on blood monocytes Diagn Pathol 4 12 19371402
116. F. Re J.L. Strominger 2004 IL-10 Released by concomitant TLR2 stimulation blocks the induction of a subset of Th1 cytokines that are specifically induced by TLR4 or TLR3 in human dendritic cells J Immunol 173 7548 7555 15585882
117. D. Tamandl M. Bahrami B. Wessner G. Weigel M. Ploder W. Furst, et al. 2003 Modulation of toll-like receptor 4 expression on human monocytes by tumor necrosis factor and interleukin-6: tumor necrosis factor evokes lipopolysaccharide hyporesponsiveness, whereas interleukin-6 enhances lipopolysaccharide activity Shock 20 224 229 12923493
118. R. Salomao M.K. Brunialti N.E. Gomes M.E. Mendes R.S. Diaz S. Komninakis, et al. 2009 Toll-like receptor pathway signaling is differently regulated in neutrophils and peripheral mononuclear cells of patients with sepsis, severe sepsis, and septic shock Crit Care Med 37 132 139 19050613
119. P.S. Martins M.K. Brunialti L.S. Martos F.R. Machado M.S. Assunçao S. Blecher, et al. 2008 Expression of cell surface receptors and oxidative metabolism modulation in the clinical continuum of sepsis Crit Care 12 R25 18302745
120. S.M. Zughaier W.M. Shafer D.S. Stephens 2005 Antimicrobial peptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages Cell Microbiol 7 1251 1262 16098213
121. P.P. Wolkow 1998 Involvement and dual effects of nitric oxide in septic shock Inflamm Res 47 4 152 166 9628258
122. A. Cauwels P. Brouckaert 2007 Survival of TNF toxicity: dependence on caspases and NO Arch Biochem Biophys 462 132 139 17321482
123. J. Bultinck P. Sips L. Vakaet P. Brouckaert A. Cauwels 2006 Systemic NO production during (septic) shock depends on parenchymal and not on hematopoietic cells: in vivo iNOS expression pattern in (septic) shock FASEB J 20 2363 2365 17020927
124. D. Annane S. Sanquer V. Sébille A. Faye D. Djuranovic J.C. Raphaël, et al. 2000 Compartmentalised inducible nitric-oxide synthase activity in septic shock Lancet 355 9210 1143 1148 10791377
125. N. Hirabayashi H. Tanimura H. Yamaue 2005 Nitrite/nitrate oxide and cytokines changes in patients with surgical stress Dig Dis Sci 50 893 897 15906765
126. A.R. Novotny K. Emmanuel S. Maier A. Westerholt H. Weighardt J. Stadler, et al. 2007 Cytochrome P450 activity mirrors nitric oxide levels in postoperative sepsis: predictive indicators of lethal outcome Surgery 141 376 384 17349850
127. A. Kobayashi S. Hashimoto K. Kooguchi Y. Kitamura H. Onodera Y. Urata, et al. 1998 Expression of inducible nitric oxide synthase and inflammatory cytokines in alveolar macrophages of ARDS following sepsis Chest 113 1632 1639 9631804
128. Y. Tsukahara T. Morisaki Y. Horita M. Torisu M. Tanaka 1998 Expression of inducible nitric oxide synthase in circulating neutrophils of the systemic inflammatory response syndrome and septic patients World J Surg 22 771 777 9673545
129. J.B. Weinberg M.A. Misukonis P.J. Shami S.N. Mason D.L. Sauls W.A. Dittman, et al. 1995 Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages Blood 86 1184 1195 7542498
130. T. Tashiro H. Yamamori K. Takagi N. Hayashi K. Furukawa H. Nitta, et al. 1999 Changes in immune function following surgery for esophageal carcinoma Nutrition 15 760 766 10501289
131. E. Faist T.S. Kupper C.C. Baker I.H. Chaudry J. Dwyer A.E. Baue 1986 Depression of cellular immunity after major injury. Its association with posttraumatic complications and its reversal with immunomodulation Arch Surg 121 1000 1005 3741094
132. J.B. O'Mahony S.B. Palder J.J. Wood A. McIrvine M.L. Rodrick R.H. Demling, et al. 1984 Depression of cellular immunity after multiple trauma in the absence of sepsis J Trauma 24 869 875 6238173
133. A.J. McIrvine J.B. O'Mahony I. Saporoschetz J.A. Mannick 1982 Depressed immune response in burn patients: use of monoclonal antibodies and functional assays to define the role of suppressor cells Ann Surg 196 297 304 6214221
134. T.R. Mosmann H. Cherwinski M.W. Bond M.A. Giedlin R.L. Coffman 1986 Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins J Immunol 136 2348 2357 2419430
135. D. Decker M. Schondorf F. Bidlingmaier A. Hirner A.A. von Ruecker 1996 Surgical stress induces a shift in the type-1/type-2 T-helper cell balance, suggesting down-regulation of cell-mediated and up-regulation of antibody-mediated immunity commensurate to the trauma Surgery 119 316 325 8619187
136. C.D. Heidecke T. Hensler H. Weighardt N. Zantl H. Wagner J.R. Siewert, et al. 1999 Selective defects of T lymphocyte function in patients with lethal intra-abdominal infection Am J Surg 178 288 292 10587185
137. S. Zedler R.C. Bone A.E. Baue G.H. von Donnersmarck E. Faist 1999 T-cell reactivity and its predictive role in immunosuppression after burns Crit Care Med 27 66 72 9934895
138. P. Kidd 2003 Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease Altern Med Rev 8 223 246 12946237
139. E.S. Hwang S.J. Szabo P.L. Schwartzberg L.H. Glimcher 2005 T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3 Science 307 430 433 15662016
140. A.C. Miller R.M. Rashid E.M. Elamin 2007 The "Tr" in trauma: the helper T-cell response and the role of immunomodulation in trauma and burn patients J Trauma 63 1407 1417 18212667
141. A. O'Garra N. Arai 2000 The molecular basis of T helper 1 and T helper 2 cell differentiation Trends Cell Biol 10 542 550 11121747
142. C. O'suilleabhain S.T. O'sullivan J.L. Kelly J. Lederer J.A. Mannick M.L. Rodrick 1996 Interleukin-12 treatment restores normal resistance to bacterial challenge after burn injury Surgery 120 290 296 8751595
143. T. Hensler C.D. Heidecke H. Hecker K. Heeg H. Bartels N. Zantl, et al. 1998 Increased susceptibility to postoperative sepsis in patients with impaired monocyte IL-12 production J Immunol 161 2655 2659 9725269
144. B. Afzali G. Lombardi R.I. Lechler G.M. Lord 2007 The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease Clin Exp Immunol 148 32 46 17328715
145. K.H. Mills 2008 Induction, function and regulation of IL-17-producing T cells Eur J Immunol 38 2636 2649 18958872
146. Z. Chen J.J. O'shea 2008 Th17 cells: a new fate for differentiating helper T cells Immunol Res 41 87 102 18172584
147. M. Saruta Q.T. Yu P.R. Fleshner P.Y. Mantel C.B. Schmidt-Weber A.H. Banham, et al. 2007 Characterization of FOXP3+CD4+ regulatory T cells in Crohn's disease Clin Immunol 125 281 290 17897887
148. D. Xu J. Fu L. Jin H. Zhang C. Zhou Z. Zou, et al. 2006 Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B J Immunol 177 739 747 16785573
149. M.P. MacConmara A.A. Maung S. Fujimi A.M. McKenna A. Delisle P.H. Lapchak, et al. 2006 Increased CD4+ CD25+ T regulatory cell activity in trauma patients depresses protective Th1 immunity Ann Surg 244 514 523 16998360
150. M.M. Tiemessen A.L. Jagger H.G. Evans M.J. van Herwijnen S. John L.S. Taams 2007 CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages Proc Natl Acad Sci USA 104 19446 19451 18042719
151. T. Korn A.C. Anderson E. Bettelli M. Oukka 2007 The dynamics of effector T cells and Foxp3+ regulatory T cells in the promotion and regulation of autoimmune encephalomyelitis J Neuroimmunol 191 51 60 17916388
152. Y. Zheng D.M. Danilenko P. Valdez I. Kasman J. Eastham-Anderson J. Wu, et al. 2007 Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis Nature 445 7128 648 651 17187052
153. C.C. Loong H.G. Hsieh W.Y. Lui A. Chen C.Y. Lin 2002 Evidence for the early involvement of interleukin 17 in human and experimental renal allograft rejection J Pathol 197 322 332 12115878
154. S. Fujino A. Andoh S. Bamba A. Ogawa K. Hata Y. Araki, et al. 2003 Increased expression of interleukin 17 in inflammatory bowel disease Gut 52 65 70 12477762 (Pubitemid 36020767)
155. T.M. Frangen D. Bogdanski C. Schinkel B. Roetman T. Kälicke G. Muhr, et al. 2008 Systemic IL-17 after severe injuries Shock 29 4 462 467 17909455
156. R.S. Hotchkiss K.W. Tinsley P.E. Swanson R.E. Schmieg Jr J.J. Hui K.C. Chang, et al. 2001 Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans J Immunol 166 6952 6963 11359857
157. K.A. Felmet M.W. Hall R.S. Clark R. Jaffe J.A. Carcillo 2005 Prolonged lymphopenia, lymphoid depletion, and hypoprolactinemia in children with nosocomial sepsis and multiple organ failure J Immunol 174 3765 3772 15749917
158. R.S. Hotchkiss S.B. Osmon K.C. Chang T.H. Wagner C.M. Coopersmith I.E. Karl 2005 Accelerated lymphocyte death in sepsis occurs by both the death receptor and mitochondrial pathways J Immunol 174 5110 5118 15814742
159. D.E. Wesche J.L. Lomas-Neira M. Perl C.S. Chung A. Ayala 2005 Leukocyte apoptosis and its significance in sepsis and shock J Leukoc Biol 78 325 337 15817707
160. R.S. Hotchkiss D.W. Nicholson 2006 Apoptosis and caspases regulate death