Intravenous injection of trauma-hemorrhagic shock mesenteric lymph causes lung injury that is dependent upon activation of the inducible nitric oxide synthase pathway

Annals of Surgery

Volumn 246, Issue 5, 2007, Pages 822-830

  Senthil, Maheswari ^a   Watkins, Anthony ^a   Barlos, Dimitrios ^a   Xu, Da Zhong ^a   Lu, Qi ^a   Abungu, Billy ^a   Caputo, Frank ^a   Feinman, Rena ^a   Deitch, Edwin A ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGUANIDINE; NITRATE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; NITRITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HEMORRHAGIC SHOCK; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INTESTINE; KNOCKOUT MOUSE; LIVER; LUNG INJURY; MACROPHAGE; MALE; MESENTERY LYMPH NODE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PARENCHYMA; PERMEABILITY; PRIORITY JOURNAL; RAT; WILD TYPE;

ANIMALS; DISEASE MODELS, ANIMAL; INJECTIONS, INTRAVENOUS; LYMPH; MALE; MESENTERY; MICE; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY DISTRESS SYNDROME, ADULT; SHOCK, HEMORRHAGIC;

EID: 35648971049     PISSN: 00034932     EISSN: None     Source Type: Journal    
DOI: 10.1097/SLA.0b013e3180caa3af     Document Type: Article

References (36)

1. Deitch EA. Multiple organ failure pathophysiology and potential future therapy. Ann Surg. 1992;216:117-134.
2. Navarrete-Navarro P, Rodriguez A, Reynolds N, et al. Acute respiratory distress syndrome among trauma patients: trends in ICU mortality, risk factors, complications and resource utilization. Intensive Care Med. 2001;27:1133-1140.
3. Rush BF, Sori AJ, Murphy TF, et al. Endotoxemia and bacteremia during hemorrhagic shock. The link between trauma and sepsis? Ann Surg. 1988;207:549-554.
4. Doig CJ, Sutherland LR, Sandham JD, et al. Increased intestinal permeability is associated with the development of multiple organ dysfunction syndrome in critically ill ICU patients. Am J Respir Crit Care Med. 1998;158:444-451.
5. Magnotti LJ, Upperman JS, Xu DZ, et al. Gut derived mesenteric lymph but not portal blood increases endothelial cell permeability and promotes lung injury after hemorrhagic shock. Ann Surg. 1998;228:518-527.
6. Deitch EA, Forsythe R, Anjaria D, 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;22:221-228.
7. Deitch EA, Adams CA, Lu Q, et al. A time course study of the protective effects of mesenteric lymph duct ligation on hemorrhagic shock induced pulmonary injury and the toxic effects of lymph from shocked rats on endothelial cell monolayer permeability. Surgery. 2001;129:39-47.
8. Sambol JT, Xu DZ, Adams CA, et al. Mesenteric lymph duct ligation provides long term protection against hemorrhagic shock induced lung injury. Shock. 2000;14:416-420.
9. Deitch EA, Adams CA, Lu Q, et al. Mesenteric lymph from rats subjected to trauma - hemorrhagic shock are injurious to rat pulmonary microvascular endothelial cells as well as human umbilical vein endothelial cells. Shock. 2001;16:290-293.
10. Caruso JM, Feketeova E, Dayal SD, et al. Factors in intestinal lymph after shock increase neutrophil adhesion molecule expression and pulmonary leukosequestration. J Trauma. 2003;55:727-733.
11. Upperman JS, Deitch EA, Guo W, et al. Post-Hemorrhagic shock mesenteric lymph is cytotoxic to endothelial cells and activates neutrophils. Shock. 1998;10:407-414.
12. Thiemermann C, Szabo C, Mitchell JA, et al. Vascular hyporeactivity to vasoconstrictor agents and hemodynamic decompensation in hemorrhagic shock is mediated by nitric oxide. Proc Nat Acad Sci. 1993;90:267-271.
13. Heirholzer C, Harbrecht B, Menezes JM, et al. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med. 1998;187:917-928.
14. Heirholzer C, Kalff JC, Billiar TR, et al. Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol. 2004;286:G225-G233.
15. Suzuki Y, Deitch EA, Mishima S, et al. Inducible nitric oxide synthase gene knockout mice have increased resistance to gut injury and bacterial translocation after an intestinal ischemia-reperfusion injury. Crit Care med. 2000;28:3692-3696.
16. Caruso JM, Deitch EA, Xu DZ, et al. Gut injury and gut induced lung injury after trauma hemorrhagic shock is gender and estrus cycle specific in the rat. J Trauma. 2003;55:531-539.
17. Griffith MJ, Messent M, Macalister RJ, et al. Aminoguanidine selectively inhibits inducible nitric oxide synthase. Br J Pharm. 1993;110:963-968.
18. Shirhan MD, Shabbir MM, Kerwin LS. The role of inducible nitric oxide synthase inhibitor on the arteriolar hyporesponsiveness in hemorrhagic shocked rats. Life Sci. 2003;73:1825-1834.
19. Collins JL, Vodovotz Y, Heirholzer C, et al. Characterization of the expression of inducible nitric oxide synthase in rat and human liver during hemorrhagic shock. Shock. 2003;19:117-122.
20. Smail N, Catania RA, Wang P, et al. Gut and liver: the organs responsible for increased nitric oxide production after trauma-hemorrhage and resuscitation. Arch Surg. 1998;133:399-405.
21. Claridge JA, Enelow RI, Young JS. Hemorrhage and resuscitation induce delayed inflammation and pulmonary dysfunction in mice. J Surg Res. 2000;92:206-213.
22. Mishima S, Xu DZ, Lu Q, et al. Bacterial translocation is inhibited in inducible nitric oxide synthase knockout mice after endotoxin challenge but not in a model of bacterial overgrowth. Arch Surg. 1997;132:1190-1195.
23. Adams CA, Xu DZ, Lu Q, et al. Factors larger than 100 kd in post-hemorrhagic shock mesenteric lymph are toxic to endothelial cells. Surgery. 2001;129:351-362.
24. Baker JW, Deitch EA, Li M, et al. Hemorrhagic shock induces bacterial translocation from the gut. J Trauma. 1988;28:896-906.
25. Moore FA, Moore EE, Poggetti R, et al. Gut bacterial translocation via the portal vein: a clinical perspective with major torso trauma. J Trauma. 1991;31:629-638.
26. Magnotti LJ, Xu DZ, Lu Q, et al. Gut derived mesenteric lymph: a link between burn and lung injury. Arch Surg. 1999;143:1333-1341.
27. Deitch EA. Bacterial translocation or lymphatic drainage of toxic products from the gut: what is important in human beings? Surgery. 2002;131:241-244.
28. Harkin DW, Rubin BB, Romaschin A, et al. Selective inducible nitric oxide inhibition attenuates remote acute lung injury in a model of ruptured abdominal aortic aneurysm. J Surg Res. 2004;120:230-241.
29. Hierholzer C, Menezes JM, Ungeheuer A, et al. A nitric oxide scavenger protects against pulmonary inflammation following hemorrhagic shock. Shock. 2002;17:98-103.
30. Davidson MT, Deitch EA, Lu Q, et al. A study of the biologic activiy of trauma-hemorrhagic shock mesenteric lymph and the relative role of cytokines. Surgery. 2004;136:32-41.
31. Gonzalez RJ, Moore EE, Biffl WL, et al. The lipid fraction of posthemorrhagic shock mesenteric lymph (PHSML) inhibits neutrophil apoptosis and enhances cytotoxic potential. Shock. 2000;14:404-408.
32. Kaiser VL, Sifri ZC, Dikdan GS, et al. Trauma-hemorrhagic shock mesenteric lymph from rat contains a modified form of albumin that is implicated in endothelial cell toxicity. Shock. 2005;23:417-425.
33. Zallen G, Moore EE, Johnson JL, et al. Hypertonic saline resuscitation abrogates neutrophil priming by mesenteric lymph. J Trauma. 2000;48:45-48.
34. Shi HP, Deitch EA, Xu DZ, et al. Hypertonic saline improves intestinal mucosa barrier function and lung injury after trauma-hemorrhagic shock. Shock. 2002;17:496-501.
35. Deitch EA, Shi HP, Lu Q, et al. Serine proteases are involved in the pathogenesis of trauma-hemorrhagic shock-induced gut and lung injury. Shock. 2003;19:452-456.
36. Osband AJ, Deitch EA, Hauser CJ, et al. Albumin protects against gut induced lung injury in vitro and in vivo. Ann Surg. 2004;240:331-339.