Inflammatory mediators in intra-abdominal sepsis or injury - a scoping review

Zhengwen Xiao, Crystal Wilson, Helen Lee Robertson, Derek J Roberts, Chad G Ball, Craig N Jenne, Andrew W Kirkpatrick, Zhengwen Xiao, Crystal Wilson, Helen Lee Robertson, Derek J Roberts, Chad G Ball, Craig N Jenne, Andrew W Kirkpatrick

Abstract

Introduction: Inflammatory and protein mediators (cytokine, chemokine, acute phase proteins) play an important, but still not completely understood, role in the morbidity and mortality of intra-abdominal sepsis/injury. We therefore systematically reviewed preclinical and clinical studies of mediators in intra-abdominal sepsis/injury in order to evaluate their ability to: (1) function as diagnostic/prognostic biomarkers; (2) serve as therapeutic targets; and (3) illuminate the pathogenesis mechanisms of sepsis or injury-related organ dysfunction.

Methods: We searched MEDLINE, PubMed, EMBASE and the Cochrane Library. Two investigators independently reviewed all identified abstracts and selected articles for full-text review. We included original studies assessing mediators in intra-abdominal sepsis/injury.

Results: Among 2437 citations, we selected 182 studies in the scoping review, including 79 preclinical and 103 clinical studies. Serum procalcitonin and C-reactive protein appear to be useful to rule out infection or monitor therapy; however, the diagnostic and prognostic value of mediators for complications/outcomes of sepsis or injury remains to be established. Peritoneal mediator levels are substantially higher than systemic levels after intra-abdominal infection/trauma. Common limitations of current studies included small sample sizes and lack of uniformity in study design and outcome measures. To date, targeted therapies against mediators remain experimental.

Conclusions: Whereas preclinical data suggests mediators play a critical role in intra-abdominal sepsis or injury, there is no consensus on the clinical use of mediators in diagnosing or managing intra-abdominal sepsis or injury. Measurement of peritoneal mediators should be further investigated as a more sensitive determinant of intra-abdominal inflammatory response. High-quality clinical trials are needed to better understand the role of inflammatory mediators.

Figures

Fig. 1
Fig. 1
Flow chart of steps for study selection

References

    1. Oberholzer A, Oberholzer C, Moldawer LL. Sepsis syndromes: understanding the role of innate and acquired immunity. Shock (Augusta, Ga) 2001;16:83–96. doi: 10.1097/00024382-200116020-00001.
    1. Tsukamoto T, Chanthaphavong RS, Pape HC. Current theories on the pathophysiology of multiple organ failure after trauma. Injury. 2010;41:21–6. doi: 10.1016/j.injury.2009.07.010.
    1. Cohen MJ, Brohi K, Calfee CS, Rahn P, Chesebro BB, Christiaans SC, et al. Early release of high mobility group box nuclear protein 1 after severe trauma in humans: role of injury severity and tissue hypoperfusion. Crit Care. 2009;13:R174. doi: 10.1186/cc8152.
    1. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 2010;464:104–7. doi: 10.1038/nature08780.
    1. Matzinger P. The danger model: a renewed sense of self. Science. 2002;296:301–5. doi: 10.1126/science.1071059.
    1. West AP, Shadel GS, Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol. 2011;11:389–402. doi: 10.1038/nri2975.
    1. Hotchkiss RS, Opal S. Immunotherapy for sepsis--a new approach against an ancient foe. N Engl J Med. 2010;363:87–9. doi: 10.1056/NEJMcibr1004371.
    1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med. 2001;29:1303–10. doi: 10.1097/00003246-200107000-00002.
    1. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348:1546–54. doi: 10.1056/NEJMoa022139.
    1. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, et al. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med. 2003;31:1250–6. doi: 10.1097/01.CCM.0000050454.01978.3B.
    1. Wanner GA, Keel M, Steckholzer U, Beier W, Stocker R, Ertel W. Relationship between procalcitonin plasma levels and severity of injury, sepsis, organ failure, and mortality in injured patients. Crit Care Med. 2000;28:950–7. doi: 10.1097/00003246-200004000-00007.
    1. Anderson R, Schmidt R. Clinical biomarkers in sepsis. Front Biosci (Elite Ed) 2010;2:504–20. doi: 10.2741/e109.
    1. Levac D, Colquhoun H, O’Brien KK. Scoping studies: advancing the methodology. Implement Sci. 2010;5:69. doi: 10.1186/1748-5908-5-69.
    1. Berlin JA. Does blinding of readers affect the results of meta-analyses? University of Pennsylvania Meta-analysis Blinding Study Group. Lancet. 1997;350:185–6. doi: 10.1016/S0140-6736(05)62352-5.
    1. Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13:818–29. doi: 10.1097/00003246-198510000-00009.
    1. Vincent JL, Moreno R, Takala J, Willatts S, De Mendonca A, Bruining H, et al. The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the Working Group on Sepsis-Related Problems of the European Society of Intensive Care Medicine. Intensive Care Med. 1996;22:707–10. doi: 10.1007/BF01709751.
    1. 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;14:187–96. doi: 10.1097/00005373-197403000-00001.
    1. Ciriello V, Gudipati S, Stavrou PZ, Kanakaris NK, Bellamy MC, Giannoudis PV. Biomarkers predicting sepsis in polytrauma patients: current evidence. Injury. 2013;44:1680–92. doi: 10.1016/j.injury.2013.09.024.
    1. Furlan AD, Pennick V, Bombardier C, van Tulder M. 2009 updated method guidelines for systematic reviews in the Cochrane Back Review Group. Spine. 2009;34:1929–41. doi: 10.1097/BRS.0b013e3181b1c99f.
    1. Hayden JA, van der Windt DA, Cartwright JL, Cote P, Bombardier C. Assessing bias in studies of prognostic factors. Ann Intern Med. 2013;158:280–6. doi: 10.7326/0003-4819-158-4-201302190-00009.
    1. Schentag JJ, O’Keeffe D, Marmion M, Wels PB. C-reactive protein as an indicator of infection relapse in patients with abdominal sepsis. Arch Surg. 1984;119:300–4. doi: 10.1001/archsurg.1984.01390150040010.
    1. Duswald KH, Jochum M, Schramm W, Fritz H. Released granulocytic elastase: an indicator of pathobiochemical alterations in septicemia after abdominal surgery. Surgery. 1985;98:892–9.
    1. Deby-Dupont G, Braun M, Lamy M, Deby C, Pincemail J, Faymonville ME, et al. Thromboxane and prostacyclin release in adult respiratory distress syndrome. Intensive Care Med. 1987;13:167–74. doi: 10.1007/BF00254700.
    1. Mustard RA, Jr, Bohnen JM, Haseeb S, Kasina R. C-reactive protein levels predict postoperative septic complications. Arch Surg. 1987;122:69–73. doi: 10.1001/archsurg.1987.01400130075011.
    1. Ingram RR, Mohammed R, Tillman J. C-reactive protein and acute appendicitis. J R Coll Surg Edinb. 1988;33:115–6.
    1. Dueholm S, Bagi P, Bud M. Laboratory aid in the diagnosis of acute appendicitis. A blinded, prospective trial concerning diagnostic value of leukocyte count, neutrophil differential count, and C-reactive protein. Dis Colon Rectum. 1989;32:855–9. doi: 10.1007/BF02554555.
    1. Damas P, Ledoux D, Nys M, Vrindts Y, De Groote D, Franchimont P, et al. Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg. 1992;215:356–62. doi: 10.1097/00000658-199204000-00009.
    1. Hamilton G, Hofbauer S, Hamilton B. Endotoxin, TNF-alpha, interleukin-6 and parameters of the cellular immune system in patients with intraabdominal sepsis. Scand J Infect Dis. 1992;24:361–8. doi: 10.3109/00365549209061344.
    1. Ohzato H, Yoshizaki K, Nishimoto N, Ogata A, Tagoh H, Monden M, et al. Interleukin-6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and C-reactive protein after surgery. Surgery. 1992;111:201–9.
    1. Fugger R, Zadrobilek E, Gotzinger P, Klimann S, Rogy M, Winkler S, et al. Perioperative TNF alpha and IL-6 concentrations correlate with septic state, organ function, and APACHE II scores in intra-abdominal infection. Eur J Surg. 1993;159:525–9.
    1. Cabie A, Farkas JC, Fitting C, Laurian C, Cormier JM, Carlet J, et al. High levels of portal TNF-alpha during abdominal aortic surgery in man. Cytokine. 1993;5:448–53. doi: 10.1016/1043-4666(93)90034-3.
    1. Gurleyik E, Gurleyik G, Unalmiser S. Accuracy of serum C-reactive protein measurements in diagnosis of acute appendicitis compared with surgeon’s clinical impression. Dis Colon Rectum. 1995;38:1270–4. doi: 10.1007/BF02049151.
    1. Holzheimer RG, Schein M, Wittmann DH. Inflammatory response in peritoneal exudate and plasma of patients undergoing planned relaparotomy for severe secondary peritonitis. Arch Surg. 1995;130:1314–9. doi: 10.1001/archsurg.1995.01430120068010.
    1. Kaufmann P, Tilz GP, Smolle KH, Demel U, Krejs GJ. Increased plasma concentrations of circulating intercellular adhesion molecule-1 (clCAM-1) in patients with necrotizing pancreatitis. Immunobiology. 1996;195:209–19. doi: 10.1016/S0171-2985(96)80040-4.
    1. Riche F, Panis Y, Laisne MJ, Briard C, Cholley B, Bernard-Poenaru O, et al. High tumor necrosis factor serum level is associated with increased survival in patients with abdominal septic shock: a prospective study in 59 patients. Surgery. 1996;120:801–7. doi: 10.1016/S0039-6060(96)80087-0.
    1. Tang GJ, Kuo CD, Yen TC, Kuo HS, Chan KH, Yien HW, et al. Perioperative plasma concentrations of tumor necrosis factor-alpha and interleukin-6 in infected patients. Crit Care Med. 1996;24:423–8. doi: 10.1097/00003246-199603000-00010.
    1. Hammond JM, Potgieter PD. The influence of surgery on cytokines in patients with intra-abdominal sepsis. Anaesth Intensive Care. 1996;24:430–4.
    1. Frohlich D, Eiber RM, Jochum M, Billing A. Perioperative pattern of peritoneal interleukin 8, tumour necrosis factor-alpha, and granulocyte elastase release in human secondary peritonitis. Cytokine. 1997;9:288–92. doi: 10.1006/cyto.1996.0166.
    1. Berger D, Bolke E, Seidelmann M, Beger HG. Time-scale of interleukin-6, myeloid related proteins (MRP), C reactive protein (CRP), and endotoxin plasma levels during the postoperative acute phase reaction. Shock. 1997;7:422–6. doi: 10.1097/00024382-199706000-00006.
    1. Gilliland HE, Armstrong MA, Carabine U, McMurray TJ. The choice of anesthetic maintenance technique influences the antiinflammatory cytokine response to abdominal surgery. Anesth Analg. 1997;85:1394–8.
    1. Groeneveld AB, Raijmakers PG, Rauwerda JA, Hack CE. The inflammatory response to vascular surgery-associated ischaemia and reperfusion in man: effect on postoperative pulmonary function. Eur J Vasc Endovasc Surg. 1997;14:351–9. doi: 10.1016/S1078-5884(97)80284-5.
    1. Donati A, Battisti D, Recchioni A, Paoletti P, Conti G, Caporelli S, et al. Predictive value of interleukin 6 (IL-6), interleukin 8 (IL-8) and gastric intramucosal pH (pH-i) in major abdominal surgery. Intensive Care Med. 1998;24:329–35. doi: 10.1007/s001340050575.
    1. Kato M, Honda I, Suzuki H, Murakami M, Matsukawa S, Hashimoto Y. Interleukin-10 production during and after upper abdominal surgery. J Clin Anesth. 1998;10:184–8. doi: 10.1016/S0952-8180(97)00264-X.
    1. Simovic MO, Bonham MJD, Abu-Zidan FM, Windsor JA. Anti-inflammatory cytokine response and clinical outcome in acute pancreatitis. Crit Care Med. 1999;27:2662–5. doi: 10.1097/00003246-199912000-00009.
    1. Holmberg A, Bergqvist D, Westman B, Siegbahn A. Cytokine and fibrinogen response in patients undergoing open abdominal aortic aneurysm surgery. Eur J Vasc Endovasc Surg. 1999;17:294–300. doi: 10.1053/ejvs.1998.0767.
    1. Pape HC, Remmers D, Grotz M, Schedel I, von Glinski S, Oberbeck R, et al. Levels of antibodies to endotoxin and cytokine release in patients with severe trauma: does posttraumatic dysergy contribute to organ failure? J Trauma. 1999;46:907–13. doi: 10.1097/00005373-199905000-00022.
    1. Erkasap S, Ates E, Ustuner Z, Sahin A, Yilmaz S, Yasar B, et al. Diagnostic value of interleukin-6 and C-reactive protein in acute appendicitis. Swiss Surg. 2000;6:169–72. doi: 10.1024/1023-9332.6.4.169.
    1. Holzheimer RG, Capel P, Cavaillon JM, Cainzos M, Frileux P, Haupt W, et al. Immunological surrogate parameters in a prognostic model for multi-organ failure and death. Eur J Med Res. 2000;5:283–94.
    1. Reith HB, Mittelkotter U, Wagner R, Thiede A. Procalcitonin (PCT) in patients with abdominal sepsis. Intensive Care Med. 2000;26:S165–169. doi: 10.1007/s001340051137.
    1. Riche FC, Cholley BP, Panis YH, Laisne MJ, Briard CG, Graulet AM, et al. Inflammatory cytokine response in patients with septic shock secondary to generalized peritonitis. Crit Care Med. 2000;28:433–7. doi: 10.1097/00003246-200002000-00024.
    1. Scheingraber S, Bauerfeind F, Bohme J, Dralle H. Limits of peritoneal cytokine measurements during abdominal lavage treatment for intraabdominal sepsis. Am J Surg. 2001;181:301–8. doi: 10.1016/S0002-9610(01)00587-6.
    1. Bolke E, Jehle PM, Graf M, Baier A, Wiedeck H, Steinbach G, et al. Inflammatory response during abdominal and thyroid surgery: a prospective clinical trial on mediator release. Shock. 2001;16:334–9. doi: 10.1097/00024382-200116050-00002.
    1. Buttenschoen K, Buttenschoen DC, Berger D, Vasilescu C, Schafheutle S, Goeltenboth B, et al. Endotoxemia and acute-phase proteins in major abdominal surgery. Am J Surg. 2001;181:36–43. doi: 10.1016/S0002-9610(00)00534-1.
    1. Wiik H, Karttunen R, Haukipuro K, Syrjala H. Maximal local and minimal systemic cytokine response to colorectal surgery: the influence of perioperative filgrastim. Cytokine. 2001;14:188–92. doi: 10.1006/cyto.2001.0870.
    1. Gurleyik G, Gurleyik E, Cetinkaya F, Unalmiser S. Serum interleukin-6 measurement in the diagnosis of acute appendicitis. ANZ J Surg. 2002;72:665–7. doi: 10.1046/j.1445-2197.2002.02516.x.
    1. Herwig R, Glodny B, Kuhle C, Schluter B, Brinkmann OA, Strasser H, et al. Early identification of peritonitis by peritoneal cytokine measurement. Dis Colon Rectum. 2002;45:514–21. doi: 10.1007/s10350-004-6231-z.
    1. Lindberg M, Hole A, Johnsen H, Asberg A, Rydning A, Myrvold HE, et al. Reference intervals for procalcitonin and C-reactive protein after major abdominal surgery. Scand J Clin Lab Invest. 2002;62:189–94. doi: 10.1080/003655102317475443.
    1. Ikuta S, Ono S, Kinoshita M, Tsujimoto H, Yamauchi A, Mochizuki H. Interleukin-18 concentration in the peritoneal fluid correlates with the severity of peritonitis. Am J Surg. 2003;185:550–5. doi: 10.1016/S0002-9610(03)00080-1.
    1. Yang MD, Jeng LB, Kao A, Lin CC, Lee CC. C-reactive protein and gallium scintigraphy in patients after abdominal surgery. Hepatogastroenterology. 2003;50:354–6.
    1. Latifi SQ, O’Riordan MA, Levine AD, Stallion A. Persistent elevation of serum interleukin-6 in intraabdominal sepsis identifies those with prolonged length of stay. J Pediatr Surg. 2004;39:1548–52. doi: 10.1016/j.jpedsurg.2004.06.015.
    1. Jansson K, Redler B, Truedsson L, Magnuson A, Matthiessen P, Andersson M, et al. Intraperitoneal cytokine response after major surgery: higher postoperative intraperitoneal versus systemic cytokine levels suggest the gastrointestinal tract as the major source of the postoperative inflammatory reaction. Am J Surg. 2004;187:372–7. doi: 10.1016/j.amjsurg.2003.12.019.
    1. Chachkhiani I, Gurlich R, Maruna P, Frasko R, Lindner J. The postoperative stress response and its reflection in cytokine network and leptin plasma levels. Physiol Res. 2005;54:279–85.
    1. Karamarkovic A, Radenkovic D, Milic N, Bumbasirevic V, Stefanovic B. Protein C as an early marker of severe septic complications in diffuse secondary peritonitis. World J Surg. 2005;29:759–65. doi: 10.1007/s00268-005-7771-7.
    1. Mokart D, Merlin M, Sannini A, Brun JP, Delpero JR, Houvenaeghel G, et al. Procalcitonin, interleukin 6 and systemic inflammatory response syndrome (SIRS): early markers of postoperative sepsis after major surgery. Br J Anaesth. 2005;94:767–73. doi: 10.1093/bja/aei143.
    1. Yamamoto T, Umegae S, Kitagawa T, Matsumoto K. Intraperitoneal cytokine productions and their relationship to peritoneal sepsis and systemic inflammatory markers in patients with inflammatory bowel disease. Dis Colon Rectum. 2005;48:1005–15. doi: 10.1007/s10350-004-0866-7.
    1. Sarbinowski R, Arvidsson S, Tylman M, Oresland T, Bengtsson A. Plasma concentration of procalcitonin and systemic inflammatory response syndrome after colorectal surgery. Acta Anaesthesiol Scand. 2005;49:191–6. doi: 10.1111/j.1399-6576.2004.00565.x.
    1. Kermarrec N, Selloum S, Plantefeve G, Chosidow D, Paoletti X, Lopez A, et al. Regulation of peritoneal and systemic neutrophil-derived tumor necrosis factor-alpha release in patients with severe peritonitis: role of tumor necrosis factor-alpha converting enzyme cleavage. Crit Care Med. 2005;33:1359–64. doi: 10.1097/01.CCM.0000166359.47577.57.
    1. Birchley D. Patients with clinical acute appendicitis should have pre-operative full blood count and C-reactive protein assays. Ann R Coll Surg Engl. 2006;88:27–32. doi: 10.1308/003588406X83041.
    1. Haecker FM, Fasler-Kan E, Manasse C, Fowler B, Hertel R, von Schweinitz D. Peritonitis in childhood: clinical relevance of cytokines in the peritoneal exudate. Eur J Pediatr Surg. 2006;16:94–9. doi: 10.1055/s-2006-924049.
    1. Sack U, Biereder B, Elouahidi T, Bauer K, Keller T, Trobs RB. Diagnostic value of blood inflammatory markers for detection of acute appendicitis in children. BMC Surg. 2006;6:15. doi: 10.1186/1471-2482-6-15.
    1. Kowal-Vern A, Ortegel J, Bourdon P, Chakrin A, Latenser BA, Kimball D, et al. Elevated cytokine levels in peritoneal fluid from burned patients with intra-abdominal hypertension and abdominal compartment syndrome. Burns. 2006;32:563–9. doi: 10.1016/j.burns.2005.12.010.
    1. Dimopoulou I, Armaganidis A, Douka E, Mavrou I, Augustatou C, Kopterides P, et al. Tumour necrosis factor-alpha (TNFalpha) and interleukin-10 are crucial mediators in post-operative systemic inflammatory response and determine the occurrence of complications after major abdominal surgery. Cytokine. 2007;37:55–61. doi: 10.1016/j.cyto.2007.02.023.
    1. Novotny AR, Emmanuel K, Maier S, Westerholt A, Weighardt H, Stadler J, et al. Cytochrome P450 activity mirrors nitric oxide levels in postoperative sepsis: predictive indicators of lethal outcome. Surgery. 2007;141:376–84. doi: 10.1016/j.surg.2006.08.011.
    1. Svoboda P, Kantorova I, Scheer P, Radvanova J, Radvan M. Can procalcitonin help us in timing of re-intervention in septic patients after multiple trauma or major surgery? Hepatogastroenterology. 2007;54:359–63.
    1. Ilias I, Tzanela M, Mavrou I, Douka E, Kopterides P, Armaganidis A, et al. Thyroid function changes and cytokine alterations following major surgery. Neuroimmunomodulation. 2007;14:243–7. doi: 10.1159/000112049.
    1. Determann RM, van Till JWO, van Ruler O, van Veen SQ, Schultz MJ, Boermeester MA. sTREM-1 is a potential useful biomarker for exclusion of ongoing infection in patients with secondary peritonitis. Cytokine. 2009;46:36–42. doi: 10.1016/j.cyto.2008.12.006.
    1. Novotny AR, Emmanuel K, Hueser N, Knebel C, Kriner M, Ulm K, et al. Procalcitonin ratio indicates successful surgical treatment of abdominal sepsis. Surgery. 2009;145:20–6. doi: 10.1016/j.surg.2008.08.009.
    1. Schroeder S, Hochreiter M, Koehler T, Schweiger AM, Bein B, Keck FS, et al. Procalcitonin (PCT)-guided algorithm reduces length of antibiotic treatment in surgical intensive care patients with severe sepsis: results of a prospective randomized study. Langenbecks Arch Surg. 2009;394:221–6. doi: 10.1007/s00423-008-0432-1.
    1. Buttenschoen K, Schneider ME, Utz K, Kornmann M, Beger HG, Carli BD. Effect of major abdominal surgery on endotoxin release and expression of Toll-like receptors 2/4. Langenbecks Arch Surg. 2009;394:293–302. doi: 10.1007/s00423-008-0357-8.
    1. Hofer S, Brenner T, Bopp C, Steppan J, Lichtenstern C, Weitz J, et al. Cell death serum biomarkers are early predictors for survival in severe septic patients with hepatic dysfunction. Crit Care. 2009;13:R93. doi: 10.1186/cc7923.
    1. Bingold TM, Ziesche E, Scheller B, Sadik CD, Franck K, Just L, et al. Interleukin-22 detected in patients with abdominal sepsis. Shock. 2010;34:337–40. doi: 10.1097/SHK.0b013e3181dc07b1.
    1. Brenner T, Hofer S, Rosenhagen C, Steppan J, Lichtenstern C, Weitz J, et al. Macrophage migration inhibitory factor (MIF) and manganese superoxide dismutase (MnSOD) as early predictors for survival in patients with severe sepsis or septic shock. J Surg Res. 2010;164:e163–171. doi: 10.1016/j.jss.2010.05.004.
    1. Hranjec T, Swenson BR, Dossett LA, Metzger R, Flohr TR, Popovsky KA, et al. Diagnosis-dependent relationships between cytokine levels and survival in patients admitted for surgical critical care. J Am Coll Surg. 2010;210:833–44. doi: 10.1016/j.jamcollsurg.2009.12.042.
    1. Manganelli V, Signore M, Pacini I, Misasi R, Tellan G, Garofalo T, et al. Increased HMGB1 expression and release by mononuclear cells following surgical/anesthesia trauma. Crit Care. 2010;14:R197. doi: 10.1186/cc9316.
    1. Albayrak Y, Albayrak A, Celik M, Gelincik I, Demiryilmaz I, Yildirim R, et al. High mobility group box protein-1 (HMGB-1) as a new diagnostic marker in patients with acute appendicitis. Scand J Trauma Resusc Emerg Med. 2011;19:27. doi: 10.1186/1757-7241-19-27.
    1. Kumar RV, Kumar RM, Pradeep Kumar NS, Ananthakrishnan N. Diagnostic value of C-reactive protein in suspected acute appendicitis--a prospective case control study. Indian J Med Sci. 2011;65:399–405. doi: 10.4103/0019-5359.108956.
    1. Ravishankaran P, Shah AM, Bhat R. Correlation of interleukin-6, serum lactate, and C-reactive protein to inflammation, complication, and outcome during the surgical course of patients with acute abdomen. J Interferon Cytokine Res. 2011;31:685–90. doi: 10.1089/jir.2011.0021.
    1. Tschaikowsky K, Hedwig-Geissing M, Braun GG, Radespiel-Troeger M. Predictive value of procalcitonin, interleukin-6, and C-reactive protein for survival in postoperative patients with severe sepsis. J Crit Care. 2011;26:54–64. doi: 10.1016/j.jcrc.2010.04.011.
    1. Yamamoto T, Umegae S, Matsumoto K, Saniabadi AR. Peritoneal cytokines as early markers of peritonitis following surgery for colorectal carcinoma: a prospective study. Cytokine. 2011;53:239–42. doi: 10.1016/j.cyto.2010.10.006.
    1. Nguyen-Vermillion A, Juul SE, McPherson RJ, Ledbetter DJ. Time course of C-reactive protein and inflammatory mediators after neonatal surgery. J Pediatr. 2011;159:121–6. doi: 10.1016/j.jpeds.2010.12.048.
    1. Steppan J, Hofer S, Funke B, Brenner T, Henrich M, Martin E, et al. Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix. J Surg Res. 2011;165:136–41. doi: 10.1016/j.jss.2009.04.034.
    1. Almeida AB, Faria G, Moreira H, Pinto-de-Sousa J, Correia-da-Silva P, Maia JC. Elevated serum C-reactive protein as a predictive factor for anastomotic leakage in colorectal surgery. Int J Surg. 2012;10:87–91. doi: 10.1016/j.ijsu.2011.12.006.
    1. Azevedo JR, Torres OJ, Czeczko NG, Tuon FF, Nassif PA, Souza GD. Procalcitonin as a prognostic biomarker of severe sepsis and septic shock. Rev Col Bras Cir. 2012;39:456–61. doi: 10.1590/S0100-69912012000600003.
    1. Benkoe T, Reck C, Gleiss A, Kettner S, Repa A, Horcher E, et al. Interleukin 8 correlates with intestinal involvement in surgically treated infants with necrotizing enterocolitis. J Pediatr Surg. 2012;47:1548–54. doi: 10.1016/j.jpedsurg.2011.11.049.
    1. Bezmarevic M, Mirkovic D, Soldatovic I, Stamenkovic D, Mitrovic N, Perisic N, et al. Correlation between procalcitonin and intra-abdominal pressure and their role in prediction of the severity of acute pancreatitis. Pancreatology. 2012;12:337–43. doi: 10.1016/j.pan.2012.05.007.
    1. Celik IH, Yilmaz Y, Erdeve O, Demirel G, Oguz SS, Uras N, et al. The acute-phase response in differentiating sepsis from inflammation in neonates who require abdominal surgery. Acta Chir Belg. 2012;112:292–6.
    1. Kimura A, Ono S, Hiraki S, Takahata R, Tsujimoto H, Miyazaki H, et al. The postoperative serum interleukin-15 concentration correlates with organ dysfunction and the prognosis of septic patients following emergency gastrointestinal surgery. J Surg Res. 2012;175:e83–88. doi: 10.1016/j.jss.2011.12.003.
    1. Witczak A, Juralowicz P, Modzelewski B, Gawlik M. C-reactive protein as a marker of postoperative septic complications. Pol Przegl Chir. 2012;84:93–8.
    1. Wu C, Sun H, Wang H, Chi J, Liu Q, Guo H, et al. Evaluation of high mobility group box 1 protein as a presurgical diagnostic marker reflecting the severity of acute appendicitis. Scand J Trauma Resusc Emerg Med. 2012;20:61. doi: 10.1186/1757-7241-20-61.
    1. Barbic J, Ivic D, Alkhamis T, Drenjancevic D, Ivic J, Harsanji-Drenjancevic I, et al. Kinetics of changes in serum concentrations of procalcitonin, interleukin-6, and C- reactive protein after elective abdominal surgery. Can it be used to detect postoperative complications? Coll Antropol. 2013;37:195–201.
    1. Jung B, Molinari N, Nasri M, Hajjej Z, Chanques G, Jean-Pierre H, et al. Procalcitonin biomarker kinetics fails to predict treatment response in perioperative abdominal infection with septic shock. Crit Care. 2013;17:R255. doi: 10.1186/cc13082.
    1. Riche F, Gayat E, Collet C, Mateo J, Laisne MJ, Launay JM, et al. Local and systemic innate immune response to secondary human peritonitis. Crit Care. 2013;17:R201. doi: 10.1186/cc12895.
    1. Scepanovic MS, Kovacevic B, Cijan V, Antic A, Petrovic Z, Asceric R, et al. C-reactive protein as an early predictor for anastomotic leakage in elective abdominal surgery. Tech Coloproctol. 2013;17:541–7. doi: 10.1007/s10151-013-1013-z.
    1. Stamataki E, Stathopoulos A, Garini E, Kokkoris S, Glynos C, Psachoulia C, et al. Serum S100B protein is increased and correlates with interleukin 6, hypoperfusion indices, and outcome in patients admitted for surgical control of hemorrhage. Shock. 2013;40:274–80. doi: 10.1097/SHK.0b013e3182a35de5.
    1. Yamanouchi S, Kudo D, Yamada M, Miyagawa N, Furukawa H, Kushimoto S. Plasma mitochondrial DNA levels in patients with trauma and severe sepsis: time course and the association with clinical status. J Crit Care. 2013;28:1027–31. doi: 10.1016/j.jcrc.2013.05.006.
    1. Zhu P, Liang Z, Fu J, Chen W, Wang Z, Jiang H, et al. Procalcitonin in abdominal exudate to predict prolonged postoperative ileus following colorectal carcinoma surgery. Int J Biol Markers. 2013;28:187–91. doi: 10.5301/jbm.5000028.
    1. Moore FA, Moore EE, Poggetti R, McAnena OJ, Peterson VM, Abernathy CM, et al. Gut bacterial translocation via the portal vein: a clinical perspective with major torso trauma. J Trauma. 1991;31:629–36. doi: 10.1097/00005373-199105000-00006.
    1. Holzer K, Konietzny P, Wilhelm K, Encke A, Henrich D. Phagocytosis by emigrated, intra-abdominal neutrophils is depressed during human secondary peritonitis. Eur Surg Res. 2002;34:275–84. doi: 10.1159/000063071.
    1. Poeze M, Ramsay G, Buurman WA, Greve JWM, Dentener M, Takala J. Increased hepatosplanchnic inflammation precedes the development of organ dysfunction after elective high-risk surgery. Shock. 2002;17:451–8. doi: 10.1097/00024382-200206000-00002.
    1. Riese J, Schoolmann S, Denzel C, Herrmann O, Hohenberger W, Haupt W. Effect of abdominal infections on peritoneal and systemic production of interleukin 6 and monocyte chemoattractant protein-1. Shock. 2002;17:361–4. doi: 10.1097/00024382-200205000-00003.
    1. Adembri C, Kastamoniti E, Bertolozzi I, Vanni S, Dorigo W, Coppo M, et al. Pulmonary injury follows systemic inflammatory reaction in infrarenal aortic surgery. Crit Care Med. 2004;32:1170–7. doi: 10.1097/01.CCM.0000124875.98492.11.
    1. Boldt J, Ducke M, Kumle B, Papsdorf M, Zurmeyer EL. Influence of different volume replacement strategies on inflammation and endothelial activation in the elderly undergoing major abdominal surgery. [Retraction in Intensive Care Med. 2011;37:1231; PMID: 21604012] Intensive Care Med. 2004;30:416–22. doi: 10.1007/s00134-003-2110-7.
    1. Sperry JL, Friese RS, Frankel HL, West MA, Cuschieri J, Moore EE, et al. Male gender is associated with excessive IL-6 expression following severe injury. J Trauma. 2008;64:572–8. doi: 10.1097/TA.0b013e3181650fdf.
    1. van Till JWO, van Veen SQ, den Broeder V, Bresser P, Lutter R, Out TA, et al. Compartmental apoptosis and neutrophil accumulation in severe peritonitis. J Surg Res. 2010;164:321–8. doi: 10.1016/j.jss.2009.09.020.
    1. Chen ZY, Qi QH. Study for effect of kangyanling on cytokine and C-reactive protein in patients of systemic inflammatory reaction syndrome and multi-organ dysfunction syndrome after abdominal surgery. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2001;21:102–4.
    1. Matsuno N, Ikeda T, Ikeda K, Hama K, Iwamoto H, Uchiyama M, et al. Changes of cytokines in direct endotoxin adsorption treatment on postoperative multiple organ failure. Ther Apher. 2001;5:36–9. doi: 10.1046/j.1526-0968.2001.005001036.x.
    1. Schmidt SC, Hamann S, Langrehr JM, Hoflich C, Mittler J, Jacob D, et al. Preoperative high-dose steroid administration attenuates the surgical stress response following liver resection: results of a prospective randomized study. J Hepatobiliary Pancreat Surg. 2007;14:484–92. doi: 10.1007/s00534-006-1200-7.
    1. Schwarz A, Bolke E, Peiper M, Schulte am Esch J, Steinbach G, van Griensven M, et al. Inflammatory peritoneal reaction after perforated appendicitis: continuous peritoneal lavage versus non lavage. Eur J Med Res. 2007;12:200–5.
    1. Bakker OJ, van Santvoort HC, van Brunschot S, Geskus RB, Besselink MG, Bollen TL, et al. Endoscopic transgastric vs surgical necrosectomy for infected necrotizing pancreatitis: a randomized trial. JAMA. 2012;307:1053–61. doi: 10.1001/jama.2012.276.
    1. Schietroma M, Piccione F, Carlei F, Clementi M, Bianchi Z, de Vita F, et al. Peritonitis from perforated appendicitis: stress response after laparoscopic or open treatment. Am Surg. 2012;78:582–90.
    1. Schietroma M, Piccione F, Carlei F, Sista F, Cecilia EM, Amicucci G. Peritonitis from perforated peptic ulcer and immune response. J Invest Surg. 2013;26:294–304. doi: 10.3109/08941939.2012.762073.
    1. Sista F, Schietroma M, Santis GD, Mattei A, Cecilia EM, Piccione F, et al. Systemic inflammation and immune response after laparotomy vs laparoscopy in patients with acute cholecystitis, complicated by peritonitis. World J Gastrointest Surg. 2013;5:73–82. doi: 10.4240/wjgs.v5.i4.73.
    1. Kirkpatrick AW, Roberts DJ, Faris PD, Ball CG, Kubes P, Tiruta C, et al. Active negative pressure peritoneal therapy after abbreviated laparotomy: the intraperitoneal vacuum randomized controlled trial. Ann Surg. 2015;262:38–46. doi: 10.1097/SLA.0000000000001095.
    1. Guo W, Soltesz V, Ding JW, Willen R, Liu X, Andersson R, et al. Abdominal rubber drain piece aggravates intra-abdominal sepsis in the rat. Eur J Clin Invest. 1994;24:540–7. doi: 10.1111/j.1365-2362.1994.tb01104.x.
    1. Walley KR, Lukacs NW, Standiford TJ, Strieter RM, Kunkel SL. Balance of inflammatory cytokines related to severity and mortality of murine sepsis. Infect Immun. 1996;64:4733–8.
    1. Lane JS, Todd KE, Lewis MP, Gloor B, Ashley SW, Reber HA, et al. Interleukin-10 reduces the systemic inflammatory response in a murine model of intestinal ischemia/reperfusion. Surgery. 1997;122:288–94. doi: 10.1016/S0039-6060(97)90020-9.
    1. Rongione AJ, Kusske AM, Ashley SW, Reber HA, McFadden DW. Interleukin-10 prevents early cytokine release in severe intraabdominal infection and sepsis. J Surg Res. 1997;70:107–12. doi: 10.1006/jsre.1997.5071.
    1. Wickel DJ, Cheadle WG, Mercer-Jones MA, Garrison RN. Poor outcome from peritonitis is caused by disease acuity and organ failure, not recurrent peritoneal infection. Ann Surg. 1997;225:744–53. doi: 10.1097/00000658-199706000-00012.
    1. Bathe OF, Chow AW, Phang PT. Splanchnic origin of cytokines in a porcine model of mesenteric ischemia-reperfusion. Surgery. 1998;123:79–88. doi: 10.1016/S0039-6060(98)70232-6.
    1. Lawlor DK, Brock RW, Harris KA, Potter RF. Cytokines contribute to early hepatic parenchymal injury and microvascular dysfunction after bilateral hindlimb ischemia. J Vasc Surg. 1999;30:533–41. doi: 10.1016/S0741-5214(99)70081-9.
    1. Martineau L, Shek PN. Peritoneal cytokine concentrations and survival outcome in an experimental bacterial infusion model of peritonitis. Crit Care Med. 2000;28:788–94. doi: 10.1097/00003246-200003000-00030.
    1. Knoferl MW, Diodato MD, Schwacha MG, Cioffi WG, Bland KI, Chaudry IH. Cyclooxygenase-2-mediated regulation of Kupffer cell interleukin-6 production following trauma-hemorrhage and subsequent sepsis. Shock. 2001;16:479–83. doi: 10.1097/00024382-200116060-00013.
    1. Yao V, Cooper D, McCauley R, Platell C, Hall J. Bacterial translocation in a non-lethal rat model of peritonitis. Colorectal Dis. 2001;3:338–44. doi: 10.1046/j.1463-1318.2001.00260.x.
    1. Oda J, Ivatury RR, Blocher CR, Malhotra AJ, Sugerman HJ. Amplified cytokine response and lung injury by sequential hemorrhagic shock and abdominal compartment syndrome in a laboratory model of ischemia-reperfusion. J Trauma. 2002;52:625–31. doi: 10.1097/00005373-200204000-00003.
    1. Rezende-Neto JB, Moore EE, Melo de Andrade MV, Teixeira MM, Lisboa FA, Arantes RM, et al. Systemic inflammatory response secondary to abdominal compartment syndrome: stage for multiple organ failure. J Trauma. 2002;53:1121–8. doi: 10.1097/00005373-200212000-00015.
    1. van Griensven M, Kuzu M, Breddin M, Bottcher F, Krettek C, Pape HC, et al. Polymicrobial sepsis induces organ changes due to granulocyte adhesion in a murine two hit model of trauma. Exp Toxicol Pathol. 2002;54:203–9. doi: 10.1078/0940-2993-00247.
    1. Ding LA, Li JS. Effects of glutamine on intestinal permeability and bacterial translocation in TPN-rats with endotoxemia. World J Gastroenterol. 2003;9:1327–32. doi: 10.3748/wjg.v9.i6.1327.
    1. Ono S, Ueno C, Seki S, Matsumoto A, Mochizuki H. Interleukin-12 and -18 induce severe liver injury in mice recovered from peritonitis after sublethal endotoxin challenge. Surgery. 2003;134:92–100. doi: 10.1067/msy.2003.189.
    1. Rezende-Neto JB, Moore EE, Masuno T, Moore PK, Johnson JL, Sheppard FR, et al. The abdominal compartment syndrome as a second insult during systemic neutrophil priming provokes multiple organ injury. Shock. 2003;20:303–8. doi: 10.1097/01.shk.0000082487.34705.d3.
    1. Welborn MB, 3rd, Moldawer LL, Seeger JM, Minter RM, Huber TS. Role of endogenous interleukin-10 in local and distant organ injury after visceral ischemia-reperfusion. Shock. 2003;20:35–40. doi: 10.1097/01.SHK.0000071062.67193.b6.
    1. Deitch EA, Forsythe R, Anjaria D, Livingston DH, Lu Q, Xu DZ, et al. The role of lymph factors in lung injury, bone marrow suppression, and endothelial cell dysfunction in a primate model of trauma-hemorrhagic shock. Shock. 2004;22:221–8. doi: 10.1097/01.shk.0000133592.55400.83.
    1. Jarrar D, Song GY, Kuebler JF, Rue LW, Bland KI, Chaudry IH. The effect of inhibition of a major cell signaling pathway following trauma hemorrhage on hepatic injury and interleukin 6 levels. Arch Surg. 2004;139:896–901. doi: 10.1001/archsurg.139.8.896.
    1. Hildebrand F, Pape HC, Harwood P, Muller K, Hoevel P, Putz C, et al. Role of adhesion molecule ICAM in the pathogenesis of polymicrobial sepsis. Exp Toxicol Pathol. 2005;56:281–90. doi: 10.1016/j.etp.2004.09.004.
    1. Frink M, Hsieh YC, Hu S, Hsieh CH, Pape HC, Choudhry MA, et al. Mechanism of salutary effects of finasteride on post-traumatic immune/inflammatory response: upregulation of estradiol synthesis. Ann Surg. 2007;246:836–43. doi: 10.1097/SLA.0b013e318158fca0.
    1. Kiank C, Entleutner M, Furll B, Westerholt A, Heidecke CD, Schutt C. Stress-induced immune conditioning affects the course of experimental peritonitis. Shock. 2007;27:305–11. doi: 10.1097/01.shk.0000239754.82711.c0.
    1. Pimenta MBP, Aguilar-Nascimento JE, Martins DC, Silva DR, Bacelo KL, Bocchese IC, et al. The intestinal tract as the major source of interleukin 6 production during abdominal aortic clamping and hind limb ischaemia-reperfusion injury. Acta Cir Bras. 2007;22:34–9. doi: 10.1590/S0102-86502007000700008.
    1. Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Suzuki T, Bland KI, et al. Flutamide attenuates pro-inflammatory cytokine production and hepatic injury following trauma-hemorrhage via estrogen receptor-related pathway. Ann Surg. 2007;245:297–304. doi: 10.1097/01.sla.0000232523.88621.17.
    1. Hsieh CH, Frink M, Hsieh YC, Kan WH, Hsu JT, Schwacha MG, et al. The role of MIP-1 alpha in the development of systemic inflammatory response and organ injury following trauma hemorrhage. J Immunol. 2008;181:2806–12. doi: 10.4049/jimmunol.181.4.2806.
    1. Kan W-H, Hsu J-T, Schwacha MG, Choudhry MA, Raju R, Bland KI, et al. Selective inhibition of iNOS attenuates trauma-hemorrhage/resuscitation-induced hepatic injury. J Appl Physiol. 2008;105:1076–82. doi: 10.1152/japplphysiol.90495.2008.
    1. Kan WH, Hsieh CH, Schwacha MG, Choudhry MA, Raju R, Bland KI, et al. Flutamide protects against trauma-hemorrhage-induced liver injury via attenuation of the inflammatory response, oxidative stress, and apopotosis. J Appl Physiol. 2008;105:595–602. doi: 10.1152/japplphysiol.00012.2008.
    1. Teke Z, Sacar S, Yenisey C, Atalay AO, Kavak T, Erdem E. Role of activated protein C on wound healing process in left colonic anastomoses in the presence of intra-abdominal sepsis induced by cecal ligation and puncture: an experimental study in the rat. World J Surg. 2008;32:2434–43. doi: 10.1007/s00268-008-9696-4.
    1. Kiris I, Narin C, Gulmen S, Yilmaz N, Sutcu R, Kapucuoglu N. Endothelin receptor antagonism by tezosentan attenuates lung injury induced by aortic ischemia-reperfusion. Ann Vasc Surg. 2009;23:382–91. doi: 10.1016/j.avsg.2008.10.003.
    1. Liu C, Wu Q, Li Q, Liu D, Su H, Shen N, et al. Mesenteric lymphatic ducts ligation decreases the degree of gut-induced lung injury in a portal vein occlusion and reperfusion canine model. J Surg Res. 2009;154:45–50. doi: 10.1016/j.jss.2008.06.006.
    1. Hendriks T, Bleichrodt RP, Lomme RMLM, De Man BM, van Goor H, Buyne OR. Peritoneal cytokines predict mortality after surgical treatment of secondary peritonitis in the rat. J Am Coll Surg. 2010;211:263–70. doi: 10.1016/j.jamcollsurg.2010.03.038.
    1. Shah SK, Jimenez F, Walker PA, Aroom KR, Xue H, Feeley TD, et al. A novel mechanism for neutrophil priming in trauma: potential role of peritoneal fluid. Surgery. 2010;148:263–70. doi: 10.1016/j.surg.2010.03.019.
    1. Wang P, Gong G, Li Y, Li J. Hydroxyethyl starch 130/0.4 augments healing of colonic anastomosis in a rat model of peritonitis. Am J Surg. 2010;199:232–9. doi: 10.1016/j.amjsurg.2009.01.023.
    1. Zou L, Feng Y, Chen YJ, Si R, Shen S, Zhou Q, et al. Toll-like receptor 2 plays a critical role in cardiac dysfunction during polymicrobial sepsis. Crit Care Med. 2010;38:1335–42.
    1. Kubiak BD, Albert SP, Gatto LA, Vieau CJ, Roy SK, Snyder KP, et al. A clinically applicable porcine model of septic and ischemia/reperfusion-induced shock and multiple organ injury. J Surg Res. 2011;166:e59–69. doi: 10.1016/j.jss.2010.10.014.
    1. Fernandes ES, Liang L, Smillie SJ, Kaiser F, Purcell R, Rivett DW, et al. TRPV1 deletion enhances local inflammation and accelerates the onset of systemic inflammatory response syndrome. J Immunol. 2012;188:5741–51. doi: 10.4049/jimmunol.1102147.
    1. He GZ, Zhou KG, Zhang R, Wang YK, Chen XF. Impact of intestinal ischemia/reperfusion and lymph drainage on distant organs in rats. World J Gastroenterol. 2012;18:7271–8. doi: 10.3748/wjg.v18.i48.7271.
    1. Jiang H, Huang Y, Xu H, Hu R, Li QF. Inhibition of hypoxia inducible factor-1alpha ameliorates lung injury induced by trauma and hemorrhagic shock in rats. Acta Pharmacol Sin. 2012;33:635–43. doi: 10.1038/aps.2012.5.
    1. Jung E, Perrone EE, Liang Z, Breed ER, Dominguez JA, Clark AT, et al. Cecal ligation and puncture followed by methicillin-resistant Staphylococcus aureus pneumonia increases mortality in mice and blunts production of local and systemic cytokines. Shock. 2012;37:85–94. doi: 10.1097/SHK.0b013e3182360faf.
    1. Shah SK, Jimenez F, Walker PA, Xue H, Feeley TD, Uray KS, et al. Peritoneal fluid: a potential mechanism of systemic neutrophil priming in experimental intra-abdominal sepsis. Am J Surg. 2012;203:211–6. doi: 10.1016/j.amjsurg.2010.12.012.
    1. Gui H, Sun Y, Luo ZM, Su DF, Dai SM, Liu X. Cannabinoid receptor 2 protects against acute experimental sepsis in mice. Mediators Inflamm. 2013;2013:741303. doi: 10.1155/2013/741303.
    1. Hirano Y, Takeuchi H, Suda K, Hagiwara T, Miyasho T, Kawamura Y, et al. (Pro)renin receptor blocker improves survival of rats with sepsis. J Surg Res. 2014;186:269–77. doi: 10.1016/j.jss.2013.08.004.
    1. Hsu JT, Yeh HC, Chen TH, Kuo CJ, Lin CJ, Chiang KC, et al. Role of Akt/HO-1 pathway in estrogen-mediated attenuation of trauma-hemorrhage-induced lung injury. J Surg Res. 2013;182:319–25. doi: 10.1016/j.jss.2012.10.926.
    1. Khailova L, Frank DN, Dominguez JA, Wischmeyer PE. Probiotic administration reduces mortality and improves intestinal epithelial homeostasis in experimental sepsis. Anesthesiology. 2013;119:166–77. doi: 10.1097/ALN.0b013e318291c2fc.
    1. Zheng Y, Yang Y, Li Y, Xu L, Wang Y, Guo Z, et al. Ephedrine hydrochloride inhibits PGN-induced inflammatory responses by promoting IL-10 production and decreasing proinflammatory cytokine secretion via the PI3K/Akt/GSK3beta pathway. Cell Mol Immunol. 2013;10:330–7. doi: 10.1038/cmi.2013.3.
    1. Zou L, Feng Y, Li Y, Zhang M, Chen C, Cai J, et al. Complement factor B is the downstream effector of TLRs and plays an important role in a mouse model of severe sepsis. J Immunol. 2013;191:5625–35. doi: 10.4049/jimmunol.1301903.
    1. Khailova L, Petrie B, Baird CH, Dominguez J, Wischmeyer P. Lactobacillus longum rhamnosus GG and Bifidobacterium attenuate lung injury and inflammatory response in experimental sepsis. PLoS One. 2014;9 doi: 10.1371/journal.pone.0097861.
    1. Eskandari MK, Bolgos G, Miller C, Nguyen DT, DeForge LE, Remick DG. Anti-tumor necrosis factor antibody therapy fails to prevent lethality after cecal ligation and puncture or endotoxemia. J Immunol. 1992;148:2724–30.
    1. Remick D, Manohar P, Bolgos G, Rodriguez J, Moldawer L, Wollenberg G. Blockade of tumor necrosis factor reduces lipopolysaccharide lethality, but not the lethality of cecal ligation and puncture. Shock. 1995;4:89–95. doi: 10.1097/00024382-199508000-00002.
    1. Angele MK, Wichmann MW, Ayala A, Cioffi WG, Chaudry IH. Testosterone receptor blockade after hemorrhage in males. Restoration of the depressed immune functions and improved survival following subsequent sepsis. Arch Surg. 1997;132:1207–14. doi: 10.1001/archsurg.1997.01430350057010.
    1. Angele MK, Catania RA, Ayala A, Cioffi WG, Bland KI, Chaudry IH. Dehydroepiandrosterone: an inexpensive steroid hormone that decreases the mortality due to sepsis following trauma-induced hemorrhage. Arch Surg. 1998;133:1281–8. doi: 10.1001/archsurg.133.12.1281.
    1. Hogaboam CM, Steinhauser ML, Schock H, Lukacs N, Strieter RM, Standiford T, et al. Therapeutic effects of nitric oxide inhibition during experimental fecal peritonitis: role of interleukin-10 and monocyte chemoattractant protein 1. Infect Immun. 1998;66:650–5.
    1. Villa P, Shaklee CL, Meazza C, Agnello D, Ghezzi P, Senaldi G. Granulocyte colony-stimulating factor and antibiotics in the prophylaxis of a murine model of polymicrobial peritonitis and sepsis. J Infect Dis. 1998;178:471–7. doi: 10.1086/515643.
    1. Balague C, Targarona EM, Pujol M, Filella X, Espert JJ, Trias M. Peritoneal response to a septic challenge. Comparison between open laparotomy, pneumoperitoneum laparoscopy, and wall lift laparoscopy. Surg Endosc. 1999;13:792–6. doi: 10.1007/s004649901101.
    1. Jarrar D, Wang P, Song GY, Cioffi WG, Bland KI, Chaudry IH. Inhibition of tyrosine kinase signaling after trauma-hemorrhage: a novel approach for improving organ function and decreasing susceptibility to subsequent sepsis. Ann Surg. 2000;231:399–407. doi: 10.1097/00000658-200003000-00013.
    1. Oberbeck R, Dahlweid M, Koch R, van Griensven M, Emmendorfer A, Tscherne H, et al. Dehydroepiandrosterone decreases mortality rate and improves cellular immune function during polymicrobial sepsis. Crit Care Med. 2001;29:380–4. doi: 10.1097/00003246-200102000-00029.
    1. Bauhofer A, Stinner B, Kohlert F, Reckzeh B, Lorenz W, Celik I. Granulocyte colony-stimulating factor but not peritoneal lavage increases survival rate after experimental abdominal contamination and infection. Br J Surg. 2002;89:1457–64. doi: 10.1046/j.1365-2168.2002.02227.x.
    1. Pross M, Mantke R, Kunz D, Reinheckel T, Halangk W, Lippert H, et al. Reduced neutrophil sequestration in lung tissue after laparoscopic lavage in a rat peritonitis model. World J Surg. 2002;26:49–53. doi: 10.1007/s00268-001-0180-7.
    1. Kuhn R, Schubert D, Tautenhahn J, Nestler G, Schulz HU, Bartelmann M, et al. Effect of intraperitoneal application of an endotoxin inhibitor on survival time in a laparoscopic model of peritonitis in rats. World J Surg. 2005;29:766–70. doi: 10.1007/s00268-005-7409-9.
    1. Steinberg J, Halter J, Schiller H, Gatto L, Carney D, Lee HM, et al. Chemically modified tetracycline prevents the development of septic shock and acute respiratory distress syndrome in a clinically applicable porcine model. Shock. 2005;24:348–56. doi: 10.1097/01.shk.0000180619.06317.2c.
    1. Bruhn A, Verdant C, Vercruysse V, Su F, Vray B, Vincent JL. Effects of dexamethasone on macrophage migration inhibitory factor production in sepsis. Shock. 2006;26:169–73. doi: 10.1097/01.shk.0000225416.27742.cb.
    1. Suzuki T, Shimizu T, Szalay L, Choudhry MA, Rue LW, 3rd, Bland KI, et al. Androstenediol ameliorates alterations in immune cells cytokine production capacity in a two-hit model of trauma-hemorrhage and sepsis. Cytokine. 2006;34:76–84. doi: 10.1016/j.cyto.2006.04.007.
    1. Yang R, Harada T, Mollen KP, Prince JM, Levy RM, Englert JA, et al. Anti-HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. Mol Med. 2006;12:105–14. doi: 10.2119/2006-00010.Yang.
    1. Ozen IO, Ekingen G, Taslipinar MY, Bukan N, Demirogullari B, Karabulut R, et al. Effect of melatonin on healing of colonic anastomosis in a rat model of peritonitis. Eur Surg Res. 2007;39:122–7. doi: 10.1159/000102592.
    1. Karakoc D, Sayek I. Effect of peritoneal lavage on TNF-alpha, IL-1beta, and IL-6 levels and mortality in intraabdominal infections. Int Surg. 2008;93:346–53.
    1. Chatzimavroudis G, Pavlidis TE, Koutelidakis I, Giamarrelos-Bourboulis EJ, Atmatzidis S, Kontopoulou K, et al. CO(2) pneumoperitoneum prolongs survival in an animal model of peritonitis compared to laparotomy. J Surg Res. 2009;152:69–75. doi: 10.1016/j.jss.2008.02.030.
    1. Kubiak BD, Albert SP, Gatto LA, Snyder KP, Maier KG, Vieau CJ, et al. Peritoneal negative pressure therapy prevents multiple organ injury in a chronic porcine sepsis and ischemia/reperfusion model. Shock. 2010;34:525–34. doi: 10.1097/SHK.0b013e3181e14cd2.
    1. Yuan Y, Ren J, Wu X, Cao S, Li J. Exogenous C3 postpones complement exhaustion and confers organ protection in murine sepsis. J Surg Res. 2011;168:e87–94. doi: 10.1016/j.jss.2011.01.062.
    1. Calisto KL, Camacho AC, Mittestainer FC, Carvalho BM, Guadagnini D, Carvalheira JB, et al. Diacerhein attenuates the inflammatory response and improves survival in a model of severe sepsis. Crit Care. 2012;16:R158. doi: 10.1186/cc11478.
    1. Herzig DS, Guo Y, Fang G, Toliver-Kinsky TE, Sherwood ER. Therapeutic efficacy of CXCR3 blockade in an experimental model of severe sepsis. Crit Care. 2012;16:R168. doi: 10.1186/cc11642.
    1. Peng ZY, Wang HZ, Srisawat N, Wen X, Rimmele T, Bishop J, et al. Bactericidal antibiotics temporarily increase inflammation and worsen acute kidney injury in experimental sepsis. Crit Care Med. 2012;40:538–43. doi: 10.1097/CCM.0b013e31822f0d2e.
    1. Bangash MN, Patel NSA, Benetti E, Collino M, Hinds CJ, Thiemermann C, et al. Dopexamine can attenuate the inflammatory response and protect against organ injury in the absence of significant effects on hemodynamics or regional microvascular flow. Crit Care. 2013;17:R57. doi: 10.1186/cc12585.
    1. Chen F, Fan XH, Wu YP, Zhu JL, Wang F, Bo LL, et al. Resolvin D1 improves survival in experimental sepsis through reducing bacterial load and preventing excessive activation of inflammatory response. Eur J Clin Microbiol Infect Dis. 2014;33:457–64. doi: 10.1007/s10096-013-1978-6.
    1. da Silva JBNF, de Oliveira SKM, Campos IA, de Carvalho-Junior CHR, Coutinho TDC, Silva TG. Propionibacterium acnes-killed attenuates the inflammatory response and protects mice from sepsis by modulating inflammatory factors. Braz J Infect Dis. 2013;17:20–6. doi: 10.1016/j.bjid.2012.08.023.
    1. Du MH, Luo HM, Hu S, Lv Y, Lin ZL, Ma L. Electroacupuncture improves gut barrier dysfunction in prolonged hemorrhagic shock rats through vagus anti-inflammatory mechanism. World J Gastroenterol. 2013;19:5988–99. doi: 10.3748/wjg.v19.i36.5988.
    1. Fujimura N, Obara H, Suda K, Takeuchi H, Miyasho T, Kawasako K, et al. Neutrophil elastase inhibitor improves survival rate after ischemia reperfusion injury caused by supravisceral aortic clamping in rats. J Surg Res. 2013;180:e31–6. doi: 10.1016/j.jss.2012.04.037.
    1. Teixeira-da-Cunha MG, Gomes RN, Roehrs N, Bozza FA, Prescott SM, Stafforini D, et al. Bacterial clearance is improved in septic mice by platelet-activating factor-acetylhydrolase (PAF-AH) administration. PLoS One. 2013;8 doi: 10.1371/journal.pone.0074567.
    1. Theobaldo MC, Llimona F, Petroni RC, Rios EC, Velasco IT, Soriano FG. Hypertonic saline solution drives neutrophil from bystander organ to infectious site in polymicrobial sepsis: a cecal ligation and puncture model. PLoS One. 2013;8 doi: 10.1371/journal.pone.0074369.
    1. Matsuda A, Yang W, Jacob A, Aziz M, Matsuo S, Matsutani T, et al. FK866, a visfatin inhibitor, protects against acute lung injury after intestinal ischemia-reperfusion in mice via NF-k B pathway. Ann Surg. 2014;259:1007–17. doi: 10.1097/SLA.0000000000000329.
    1. Simmons JD, Lee YL, Mulekar S, Kuck JL, Brevard SB, Gonzalez RP, et al. Elevated levels of plasma mitochondrial DNA DAMPs are linked to clinical outcome in severely injured human subjects. Ann Surg. 2013;258:591–6.
    1. Mi Q, Constantine G, Ziraldo C, Solovyev A, Torres A, Namas R, et al. A dynamic view of trauma/hemorrhage-induced inflammation in mice: principal drivers and networks. PLoS One. 2011;6 doi: 10.1371/journal.pone.0019424.
    1. Nieman G, Brown D, Sarkar J, Kubiak B, Ziraldo C, Dutta-Moscato J, et al. A two-compartment mathematical model of endotoxin-induced inflammatory and physiologic alterations in swine. Crit Care Med. 2012;40:1052–63. doi: 10.1097/CCM.0b013e31823e986a.
    1. Sartelli M, Viale P, Catena F, Ansaloni L, Moore E, Malangoni M, et al. 2013 WSES guidelines for management of intra-abdominal infections. World J Emerg Surg. 2013;8:3. doi: 10.1186/1749-7922-8-3.

Source: PubMed

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