Interaction of hemorrhagic shock and subsequent polymicrobial sepsis on gastrointestinal motility

Shock

Volumn 31, Issue 4, 2009, Pages 382-389

  Overhaus, Marcus ^a,b   Toegel, Sandra ^a   Bauer, Anthony J ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Cecal ligation and puncture; Gastrointestinal motility; Hemorrhagic shock; IL 10; Sepsis

Indexed keywords

BETHANECHOL; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; MESSENGER RNA; MYELOPEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CECUM; CONTROL GROUP; CONTROLLED STUDY; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRACT; GASTROINTESTINAL TRANSIT; HEMORRHAGIC SHOCK; IN VITRO STUDY; LIGATION; MALE; MORTALITY; MUSCLE CONTRACTILITY; NEUTROPHIL; NONHUMAN; PUNCTURE; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEPSIS; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD PRESSURE; COLON; DISEASE MODELS, ANIMAL; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRANSIT; LEUKOCYTES; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESUSCITATION; SEPSIS; SHOCK, HEMORRHAGIC;

EID: 64849102179     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3181862ea4     Document Type: Article

References (55)

1. Marshall JC, Christou NV, Meakins JL: The gastrointestinal tract. The "undrained abscess" of multiple organ failure. Ann Surg 218:111-119, 1993.
2. Deitch EA, Rutan R, Waymack JP: Trauma, shock, and gut translocation. New Horiz 4:289-299, 1996.
3. Fink MP: Intestinal epithelial hyperpermeability: update on the pathogenesis of gut mucosal barrier dysfunction in critical illness [Review]. Curr Opin Crit Care 9:143-151, 2003.
4. Kallakuri S, Ascher E, Pagala M, Gade P, Hingorani A, Scheinman M, Mehraein K, Jacob T: Protective effect of glycine in mesenteric ischemia and reperfusion injury in a rat model. J Vasc Surg 38:1113-1120, 2003.
5. Hierholzer C, Kalff JC, Billiar TR, Bauer AJ, Tweardy DJ, Harbrecht BG: Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol 286:G225-G233, 2004.
6. Hierholzer C, Kalff JC, Chakraborty A, Watkins SC, Billiar TR, Bauer AJ, Tweardy DJ: Impaired gut contractility following hemorrhagic shock is accompanied by IL-6 and G-CSF production and neutrophil infiltration. Dig Dis Sci 46:230-241, 2001.
7. Kalff JC, Hierholzer C, Tsukada K, Billiar TR, Bauer AJ: Hemorrhagic shock results in intestinal muscularis intercellular adhesion molecule (ICAM-1) expression, neutrophil infiltration, and smooth muscle dysfunction. Arch Orthop Trauma Surg 119:89-93, 1999.
8. Moore-Olufemi SD, Kozar RA, Moore FA, Sato N, Hassoun HT, Cox CS Jr, Kone BC: Ischemic preconditioning protects against gut dysfunction and mucosal injury after ischemia/reperfusion injury. Shock 23:258-263, 2005.
9. Zou L, Attuwaybi B, Kone BC: Effects of NF-kappa B inhibition on mesenteric ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 284: G713-G721, 2003.
10. Hierholzer C, Billiar TR: Molecular mechanisms in the early phase of hemorrhagic shock. Langenbecks Arch Surg 386:302-308, 2001.
11. Jarrar D, Chaudry IH, Wang P: Organ dysfunction following hemorrhage and sepsis: mechanisms and therapeutic approaches. Int J Mol Med 4:575-583, 1999.
12. Grotz MR, Deitch EA, Ding J, Xu D, Huang Q, Regel G: Intestinal cytokine response after gut ischemia: role of gut barrier failure. Ann Surg 229:478-486, 1999.
13. Cullen JJ, Mercer D, Hinkhouse M, Ephgrave KS, Conklin JL: Effects of endotoxin on regulation of intestinal smooth muscle nitric oxide synthase and intestinal transit. Surgery 125:339-344, 1999.
14. Eskandari MK, Kalff JC, Billiar TR, Lee KK, Bauer AJ: Lipopolysaccharide activates the muscularis macrophage network and suppresses circular smooth muscle activity. Am J Physiol 273:G727-G734, 1997.
15. Lodato RF, Khan AR, Zembowicz MJ, Weisbrodt NW, Pressley TA, Li YF, Lodato JA, Zembowicz A, Moody FG: Roles of IL-1 and TNF in the decreased ileal muscle contractility induced by lipopolysaccharide. Am J Physiol 276: G1356-G1362, 1999.
16. Eskandari MK, Kalff JC, Billiar TR, Lee KK, Bauer AJ: LPS-induced muscularis macrophage nitric oxide suppresses rat jejunal circular muscle activity. Am J Physiol 277:G478-G486, 1999.
17. Schwarz NT, Engel B, Eskandari MK, Kalff JC, Grandis JR, Bauer AJ: Lipopolysaccharide preconditioning and cross-tolerance: the induction of protective mechanisms for rat intestinal ileus. Gastroenterology 123:586-598, 2002.
18. Wirthlin DJ, Cullen JJ, Spates ST, Conklin JL, Murray J, Caropreso DK, Ephgrave KS: Gastrointestinal transit during endotoxemia: the role of nitric oxide. J Surg Res 60:307-311, 1996.
19. Türler A, Schwarz NT, Turler E, Kalff JC, Bauer AJ: MCP-1 causes leukocyte recruitment and subsequently endotoxemic ileus in rat. Am J Physiol Gastrointest Liver Physiol 282:G145-G155, 2001.
20. Overhaus M, Togel S, Pezzone MA, Bauer AJ: Mechanisms of polymicrobial sepsis-induced ileus. Am J Physiol Gastrointest Liver Physiol 287:G685-G694, 2004.
21. Moore FA, Moore EE: Evolving concepts in the pathogenesis of postinjury multiple organ failure. Surg Clin North Am 75:257-277, 1995.
22. Moore EE, Moore FA, Harken AH, Johnson JL, Ciesla D, Banerjee A: The twoevent construct of postinjury multiple organ failure. Shock 24(suppl 4):71-74, 2005.
23. Rizoli SB, Kapus A, Fan J, Li YH, Marshall JC, Rotstein OD: Immunomodulatory effects of hypertonic resuscitation on the development of lung inflammation following hemorrhagic shock. J Immunol 161:6288, 1998.
24. Schwacha MG: Macrophages and post-burn immune dysfunction. Burns 29: 1-14, 2003.
25. Lomas JL, Chung CS, Grutkoski PS, LeBlanc BW, Lavigne L, Reichner J, Gregory SH, Doughty LA, Cioffi WG, Ayala A: Differential effects of macrophage inflammatory chemokine-2 and keratinocyte-derived chemokine on hemorrhage-induced neutrophil priming for lung inflammation: assessment by adoptive cells transfer in mice. Shock 19:358-365, 2003.
26. Ayala A, Chung CS, Lomas JL, Song GY, Doughty LA, Gregory SH, Cioffi WG, LeBlanc BW, Reichner J, Simms HH, et al.: Shock-induced neutrophil mediated priming for acute lung injury in mice: divergent effects of TLR-4 and TLR-4/FasL deficiency. Am J Pathol 161:2283-2294, 2002.
27. Lomas-Neira J, Chung CS, Grutkoski PS, Dunican A, Simms HH, Cioffi WG, Ayala A: Divergent roles of murine neutrophil chemokines in hemorrhage induced priming for acute lung injury. Cytokine 31:169-179, 2005.
28. Osuchowski MF, Welch K, Siddiqui J, Remick DG: Circulating cytokine/ inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J Immunol 177:1967-1974, 2006.
29. Moore FA, Sauaia A, Moore EE, Haenel JB, Burch JM, Lezotte DC: Postinjury multiple organ failure: a bimodal phenomenon. J Trauma 40:501-510, 1996.
30. Mallick IH, Yang W, Winslet MC, Seifalian AM: Ischaemic preconditioning improves microvascular perfusion and oxygenation following reperfusion injury of the intestine. Br J Surg 92:1169-1176, 2005.
31. Wu B, Ootani A, Iwakiri R, Fujise T, Tsunada S, Toda S, Fujimoto K: Ischemic preconditioning attenuates ischemia-reperfusion-induced mucosal apoptosis by inhibiting the mitochondria-dependent pathway in rat small intestine. Am J Physiol Gastrointest Liver Physiol 286:G580-G587, 2004.
32. Hierholzer C, Kelly E, Tsukada K, Loeffert E, Watkins S, Billiar TR, Tweardy DJ: Hemorrhagic shock induces G-CSF expression in bronchial epithelium. Am J Physiol 273:L1058-L1064, 1997.
33. Overhaus M, Moore BA, Barbato JE, Behrendt FF, Doering JG, Bauer AJ: Biliverdin protects against polymicrobial sepsis by modulating inflammatory mediators. Am J Physiol Gastrointest Liver Physiol 290:G695-G703, 2006.
34. Kalff JC, Buchholz BM, Eskandari MK, Hierholzer C, Schraut WH, Simmons RL, Bauer AJ: Biphasic response to gut manipulation and temporal correlation of cellular infiltrates and muscle dysfunction in rat. Surgery 126:498-509, 1999.
35. Williams CL, Bihm CC, Rosenfeld GC, Burks TF: Morphine tolerance and dependence in the rat intestine in vivo. J Pharmacol Exp Ther 280:656-663, 1997.
36. Kalff JC, Schraut WH, Simmons RL, Bauer AJ: Surgical manipulation of the gut elicits an intestinal muscularis inflammatory response resulting in postsurgical ileus. Ann Surg 228:652-663, 1998.
37. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW: Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285: 194-204, 2000.
38. Schulman AM, Claridge JA, Ghezel-Ayagh A, Johnson O III, Young JS: Differential local and systemic tumor necrosis factor-alpha responses to a second hit of lipopolysaccharide after hemorrhagic shock. J Trauma 55:298-307, 2003.
39. Patton JH Jr, Lyden SP, Ragsdale DN, Croce MA, Fabian TC, Proctor KG: Granulocyte colony-stimulating factor improves host defense to resuscitated shock and polymicrobial sepsis without provoking generalized neutrophilmediated damage. J Trauma 44:750-758, 1998.
40. Fan J, Shek PN, Suntres ZE, Li YH, Oreopoulos GD, Rotstein OD: Liposomal antioxidants provide prolonged protection against acute respiratory distress syndrome. Surgery 128:332-338, 2000.
41. Bone RC: Sir Isaac Newton, sepsis, SIRS, and CARS. Crit Care Med 24: 1125-1128, 1996.
42. Murry CE, Jennings RB, Reimer KA: Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136, 1986.
43. Raeburn CD, Cleveland JC Jr, Zimmerman MA, Harken AH: Organ preconditioning. Arch Surg 136:1263-1266, 2001.
44. Hierholzer C, Kalff JC, Audolfsson G, Billiar TR, Tweardy DJ, Bauer AJ: Molecular and functional contractile sequelae of rat intestinal ischemia/ reperfusion injury. Transplantation 68:1244-1254, 1999.
45. Damas P, Ledoux D, Nys M, Vrindts Y, De Groote D, Franchimont P, Lamy M: Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 215:356-362, 1992.
46. Kamei K, Nimura Y, Nagino M, Aono K, Nakashima I: Surgical stress reduces mortality from endotoxin shock. Langenbecks Arch Surg 386:512-517, 2002.
47. Stark ME, Bauer AJ, Sarr MG, Szurszewski JH: Nitric oxide mediates inhibitory nerve input in human and canine jejunum. Gastroenterology 104:398-409, 1993.
48. Kalff JC, Schraut WH, Billiar TR, Simmons RL, Bauer AJ: Role of inducible nitric oxide synthase in postoperative intestinal smooth muscle dysfunction in rodents. Gastroenterology 118:316-327, 2000.
49. Oberholzer A, Oberholzer C, Moldawer LL: Interleukin-10: a complex role in the pathogenesis of sepsis syndromes and its potential as an anti-inflammatory drug. Crit Care Med 30:58-63, 2002.
50. Randow F, Syrbe U, Meisel C, Krausch D, Zuckermann H, Platzer C, Volk HD: Mechanism of endotoxin desensitization: involvement of interleukin 10 and transforming growth factor beta. J Exp Med 181:1887-1892, 1995.
51. Steinhauser ML, Hogaboam CM, Kunkel SL, Lukacs NW, Strieter RM, Standiford TJ: IL-10 is a major mediator of sepsis-induced impairment in lung antibacterial host defense. J Immunol 162:392-399, 1999.
52. Lee PJ, Alam J, Wiegand GW, Choi AM: Overexpression of heme oxygenase- 1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci U S A 93:10393-10398, 1996.
53. Otterbein LE, Soares MP, Yamashita K, Bach FH: Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449-455, 2003.
54. Tamion F, Richard V, Lacoume Y, Thuillez C: Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am J Physiol Gastrointest Liver Physiol 283:G408-G414, 2002.
55. Moncure M, Chen L, Childs EW, Smalley D, Udobi KF, Cheung LY: Hemeoxygenase-1 mRNA expression affects hemorrhagic shock-induced leukocyte adherence. J Trauma 55:118-125, 2003.