Experimental models of hemorrhagic shock: A review

European Surgical Research

Volumn 50, Issue 2, 2013, Pages 57-70

  Fulop A ^a   Turoczi Z ^a   Garbaisz, D ^a   Harsanyi L ^a   Szijarto A ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Animal model; Experimental model; Hemorrhage; Hemorrhagic shock; Shock

Indexed keywords

OXYGEN;

ABDOMINAL AORTA ANEURYSM; ANIMAL MODEL; BLEEDING; BLOOD VOLUME; CONFOUNDING VARIABLE; DISEASE MODEL; EXPERIMENTAL DOG; EXPERIMENTAL MODEL; EXPERIMENTAL MOUSE; EXPERIMENTAL PIG; EXPERIMENTAL RAT; HEMODYNAMICS; HEMORRHAGIC SHOCK; HUMAN; HYPOVOLEMIC SHOCK; LEG INJURY; MEAN ARTERIAL PRESSURE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SCIENTIST; SPECIES; DOG; IMMUNE SYSTEM; LEG ISCHEMIA; PATHOPHYSIOLOGY; PIG;

ANIMALS; ANOXIA; AORTIC ANEURYSM, ABDOMINAL; AORTIC RUPTURE; BLOOD PRESSURE; BLOOD VOLUME; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; REPERFUSION INJURY; SHOCK, HEMORRHAGIC; WOUNDS AND INJURIES;

EID: 84876455771     PISSN: 0014312X     EISSN: 14219921     Source Type: Journal    
DOI: 10.1159/000348808     Document Type: Review

References (128)

1. Nunez TC, Cotton BA: Transfusion therapy in hemorrhagic shock. Curr Opin Crit Care 2009; 15: 536-541
2. Hamar J, Kovach AG, Reivich M, Nyary I, Durity F: Effect of phenoxybenzamine on cerebral blood flow and metabolism in the baboon during hemorrhagic shock. Stroke 1979; 10: 401-407
3. Kovach AG, Mitsanyi A, Monos E, Nyary I, Sulyok A: Control of organ blood flow following hemorrhage. Adv Exp Med Biol 1972; 33: 1-17
4. Gutierrez G, Reines HD, Wulf-Gutierrez ME: Clinical review: Hemorrhagic shock. Crit Care 2004; 8: 373-381
5. Swanson KS, Mazur MJ, Vashisht K, Rund LA, Beever JE, Counter CM, Schook LB: Genomics and clinical medicine: Rationale for creating and effectively evaluating animal models. Exp Biol Med 2004; 229: 866-875
6. Majde JA: Animal models for hemorrhage and resuscitation research. J Trauma 2003; 54:S100-S105
7. Frink M, Andruszkow H, Zeckey C, Krettek C, Hildebrand F: Experimental trauma models: An update. J Biomed Biotechnol 2011; 2011: 797383
8. Hauser C: Preclinical models of traumatic, hemorrhagic shock. Shock 2005; 24(suppl 1):24-32
9. Kemming G, Messick JB, Mueller W, Enders G, Meisner F, Muenzing S, Kisch-Wedel H, Schropp A, Wojtczyk C, Packert K, Messmer K, Thein E: Can we continue research in splenectomized dogs? Mycoplasma haemocanis: Old problem -new insight. Eur Surg Res 2004; 36: 198-205
10. Cheung AT, Duong PL, Driessen B, Chen PC, Jahr JS, Gunther RA: Systemic function, oxygenation and microvascular correlation during treatment of hemorrhagic shock with blood substitutes. Clin Hemorheol Microcirc 2006; 34: 325-334
11. Carroll RG, Iams SG, Pryor WH Jr, Allison EJ Jr: Single hemorrhage: A clinically relevant canine model of hemorrhagic shock. Resuscitation 1988; 16: 119-126
12. Hannon J: Hemorrhage and hemorrhagic-shock in swine -A review; in Swindle M (ed): Swine as Models in Biomedical Research. Ames, Iowa State University Press, 1992, pp 197-245
13. Lomas-Niera J, Perl M, Chung C, Ayala A: Shock and hemorrhage: An overview of animal models. Shock 2005; 24 (suppl 1):33-39
14. Mikkelsen T, Hillier L, Eichler E, Zody M, Jaffe D, Yang S, Enard W, Hellmann I, Lindblad-Toh K, Altheide T, Archidiacono N, Bork P, Butler J, Chang J, Cheng Z, Chinwalla A, deJong P, Delehaunty K, Fronick C, Fulton L, Gilad Y, Glusman G, Gnerre S, Graves T, Hayakawa T, Hayden K, Huang X, Ji H, Kent W, King M, Kulbokas E, Lee M, Liu G, Lopez-Otin C, Makova K, Man O, Mardis E, Mauceli E, Miner T, Nash W, Nelson J, Paabo S, Patterson N, Pohl C, Pollard K, Prufer K, Puente X, Reich D, Rocchi M, Rosenbloom K, Ruvolo M, Richter D, Schaffner S, Smit A, Smith S, Suyama M, Taylor J, Torrents D, Tuzun E, Varki A, Velasco G, Ventura M, Wallis J, Wendl M, Wilson R, Lander E, Waterston R; Chimpanzee Sequencing and Analysis Consortium: Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 2005; 437: 69-87
15. Redl H, Bahrami S: Large animal models: Baboons for trauma, shock, and sepsis studies. Shock 2005; 24(suppl 1):88-93
16. Schlag G, Redl H, Till G, Davies J, Martin U, Dumont L: Anti-L-selectin antibody treatment of hemorrhagic-Traumatic shock in baboons. Crit Care Med 1999; 27: 1900-1907
17. Deitch E: Animal models of sepsis and shock: A review and lessons learned. Reply. Shock 1998; 10: 442-445
18. Gainer J, Lipa M, Ficenec M: Hemorrhagic-shock in rats. Lab Anim Sci 1995; 45: 169-172
19. Frankel DA, Acosta JA, Anjaria DJ, Porcides RD, Wolf PL, Coimbra R, Hoyt DB: Physiologic response to hemorrhagic shock depends on rate and means of hemorrhage. J Surg Res 2007; 143: 276-280
20. Diehl KH, Hull R, Morton D, Pfister R, Rabemampianina Y, Smith D, Vidal JM, van de Vorstenbosch C: A good practice guide to the administration of substances and removal of blood, including routes and volumes. J Appl Toxicol 2001; 21: 15-23
21. Pellicane JV, Gore DC, DeMaria EJ: Decreased lactate in endotoxin-resistant mice undergoing hemorrhage is independent of tumor necrosis factor availability. J Surg Res 1994; 56: 361-366
22. Rajnik M, Salkowski CA, Thomas KE, Li YY, Rollwagen FM, Vogel SN: Induction of early inflammatory gene expression in a murine model of nonresuscitated, fixed-volume hemorrhage. Shock 2002; 17: 322-328
23. Oberbeck R, Nickel E, von Griensven M, Tschernig T, Wittwer T, Schmitz D, Pape HC: The effect of dehydroepiandrosterone on hemorrhage-induced suppression of cellular immune function. Intensive Care Med 2002; 28: 963-968
24. Hewitt PM, Armstrong N, Bowrey P, Cherian M, Morris DL: Cimetidine prevents suppression of delayed hypersensitivity in an animal model of haemorrhagic shock. Injury 2002; 33: 673-678
25. Mackrell PJ, Daly JM, Mestre JR, Stapleton PP, Howe LR, Subbaramaiah K, Dannenberg AJ: Elevated expression of cyclooxygenase-2 contributes to immune dysfunction in a murine model of trauma. Surgery 2001; 130: 826-833
26. Dennis AM, Haselkorn ML, Vagni VA, Garman RH, Janesko-Feldman K, Bayir H, Clark RS, Jenkins LW, Dixon CE, Kochanek PM: Hemorrhagic shock after experimental traumatic brain injury in mice: Effect on neuronal death. J Neurotrauma 2009; 26: 889-899
27. Zakaria el Rasheid, Garrison RN, Kawabe T, Harris PD: Direct peritoneal resuscitation from hemorrhagic shock: Effect of time delay in therapy initiation. J Trauma 2005; 58: 499-506, discussion 506-508
28. Fukudome EY, Kochanek AR, Li Y, Smith EJ, Liu B, Kheirbek T, Lu J, Kim K, Hamwi K, Velmahos GC, Alam HB: Pharmacologic resuscitation promotes survival and attenuates hemorrhage-induced activation of extracellular signal-regulated kinase 1/2. J Surg Res 2010; 163: 118-126
29. Guarini S, Bazzani C, Ricigliano GM, Bini A, Tomasi A, Bertolini A: Influence of ACTH-(1-24) on free radical levels in the blood of haemorrhage-shocked rats: Direct ex vivo detection by electron spin resonance spectrometry. Br J Pharmacol 1996; 119: 29-34
30. Johnson RA, Durante W, Craig T, Peyton KJ, Myers JG, Stewart RM, Johnson FK: Vascular arginase contributes to arteriolar endothelial dysfunction in a rat model of hemorrhagic shock. J Trauma 2010; 69: 384-391
31. Kretschmar K, Rosenthal V: Cytoskeletal alterations in endothelial cells of mesenteric microcirculatory bed in experimental traumatic haemorrhagic shock. Acta Histochem Suppl 1991; 41: 265-270
32. Troy BP, Heslop DJ, Bandler R, Keay KA: Haemodynamic response to haemorrhage: Distinct contributions of midbrain and forebrain structures. Auton Neurosci 2003; 108: 1-11
33. Santibanez-Gallerani AS, Barber AE, Williams SJ, Zhao Y, Shires GT: Hepatic integrity dependent on matrix metalloproteinase inhibition, not tumor necrosis factor alpha or different bleeding rates. J Surg Res 2000; 90: 156-160
34. Crippen D, Safar P, Snyder C, Porter L: Dying pattern in volume-controlled hemorrhagic shock in awake rats. Resuscitation 1991; 21: 259-270
35. Hall C, Malkevich N, Handrigan M, Vandermolen C, Aranaud F, Hong J, Dong F, Rice J, Philbin N, Ahlers S, McCarron R, Freilich D, McGwin G, Flournoy WS, Pearce LB: Innate immune responses in swine resuscitated from severe traumatic hemorrhagic shock with hemoglobin-based oxygen carrier-201. Artif Cells Blood Substit Immobil Biotechnol 2007; 35: 259-274
36. Herff H, Paal P, von Goedecke A, Lindner KH, Severing AC, Wenzel V: Influence of ventilation strategies on survival in severe controlled hemorrhagic shock. Crit Care Med 2008; 36: 2613-2620
37. Xanthos TT, Balkamou XA, Stroumpoulis KI, Pantazopoulos IN, Rokas GI, Agrogiannis GD, Troupis GT, Demestiha TD, Skandalakis PN: A model of hemorrhagic shock and acute lung injury in landrace-large white swine. Comp Med 2011; 61: 158-162
38. Noritomi DT, Pereira AJ, Bugano DD, Rehder PS, Silva E: Impact of Plasma-Lyte pH 7.4 on acid-base status and hemodynamics in a model of controlled hemorrhagic shock. Clinics (Sao Paulo) 2011; 66: 1969-1974
39. van Iterson M, Bezemer R, Heger M, Siegemund M, Ince C: Microcirculation follows macrocirculation in heart and gut in the acute phase of hemorrhagic shock and isovolemic autologous whole blood resuscitation in pigs. Transfusion 2012; 52: 1552-1559
40. Arnaud F, Scultetus AH, Haque A, Saha B, Kim B, Auker C, Moon-Massat P, McCarron R, Freilich D: Sodium nitroprusside ameliorates systemic but not pulmonary HBOC-201-induced vasoconstriction: An exploratory study in a swine controlled haemorrhage model. Resuscitation 2012; 83: 1038-1045
41. Crookes B, Cohn S, Bonet H, Burton E, Nelson J, Majetschak M, Varon A, Linden J, Proctor K: Building a better fluid for emergency resuscitation of traumatic brain injury. J Trauma 2004; 57: 547-554
42. Gibson J, Maxwell R, Schweitzer J, Fabian T, Proctor K: Resuscitation from severe hemorrhagic shock after traumatic brain injury using saline, shed blood, or a blood substitute. Shock 2002; 17: 234-244
43. Jacobsen J, Sofelt S, Sheikh S, Warberg J, Secher NH: Cardiovascular and endocrine responses to haemorrhage in the pig. Acta Physiol Scand 1990; 138: 167-173
44. Frey L, Kesel K, Pruckner S, Pacheco A, Welte M, Messmer K: Is sodium acetate dextran superior to sodium chloride dextran for small volume resuscitation from traumatic hemorrhagic shock? Anesth Analg 1994; 79: 517-524
45. Li KC, Pelc LR, Puvvala S, Wright GA: Mesenteric ischemia due to hemorrhagic shock: MR imaging diagnosis and monitoring in a canine model. Radiology 1998; 206: 219-225
46. Nascimento P Jr, de Paiva Filho O, de Carvalho LR, Braz JR: Early hemodynamic and renal effects of hemorrhagic shock resuscitation with lactated Ringer's solution, hydroxyethyl starch, and hypertonic saline with or without 6% dextran-70. J Surg Res 2006; 136: 98-105
47. Braz JR, do Nascimento P Jr, Paiva Filho O, Braz LG, Vane LA, Vianna PT, Rodrigues GR Jr: The early systemic and gastrointestinal oxygenation effects of hemorrhagic shock resuscitation with hypertonic saline and hypertonic saline 6% dextran-70: A comparative study in dogs. Anesth Analg 2004; 99: 536-546, table of contents
48. Yamamoto M, Horinouchi H, Kobayashi K, Seishi Y, Sato N, Itoh M, Sakai H: Fluid resuscitation of hemorrhagic shock with hemoglobin vesicles in beagle dogs: Pilot study. Artif Cells Blood Substit Immobil Biotechnol 2012; 40: 179-195
49. Glick YA, Wilson LD, Aiello J: Hematocrit and metabolic changes caused by varied resuscitation strategies in a canine model of hemorrhagic shock. Am J Emerg Med 2002; 20: 303-309
50. Penfield W: The treatment of severe and progressive hemorrhage by intravenous injections. Am J Physiol 1919; 48: 121-132
51. Wiggers CJ: The present status of the shock problem. Physiol Rev 1942; 22: 74-123
52. Ayala A, Wang P, Chaudry I: Shock models: Hemorrhage; in Souba W, Wilmore D (eds): Surgical Research. San Diego, Academic Press, 2001, pp 357-366
53. Kawasaki T, Fujimi S, Lederer JA, Hubbard WJ, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: Traumahemorrhage induces depressed splenic dendritic cell functions in mice. J Immunol 2006; 177: 4514-4520
54. Murao Y, Isayama K, Saito F, Hirakawa A, Nakatani T: Effect of hypertonic saline resuscitation on CD4+CD25+ regulatory T cells and gammadelta T cells after hemorrhagic shock and resuscitation in relation to apoptosis and iNOS. J Trauma 2009; 67: 975-982
55. Hsieh CH, Nickel EA, Hsu JT, Schwacha MG, Bland KI, Chaudry IH: Trauma-hemorrhage and hypoxia differentially influence kupffer cell phagocytic capacity: Role of hypoxia-inducible-factor-1alpha and phosphoinositide 3-kinase/akt activation. Ann Surg 2009; 250: 995-1001
56. Samy T, Ayala A, Catania R, Chaudry I: Trauma-hemorrhage activates signal transduction pathways in mouse splenic T cells. Shock 1998; 9: 443-450
57. Schneider C, Nickel E, Samy T, Schwacha M, Cioffi W, Bland K, Chaudry I: The aromatase inhibitor, 4-hydroxyandrostenedione, restores immune responses following trauma-hemorrhage in males and decreases mortality from subsequent sepsis. Shock 2000; 14: 347-353
58. Cai C, Gill R, Eum HA, Cao Z, Loughran PA, Darwiche S, Edmonds RD, Menzel CL, Billiar TR: Complement factor 3 deficiency attenuates hemorrhagic shock-related hepatic injury and systemic inflammatory response syndrome. Am J Physiol Regul Integr Comp Physiol 2010; 299:R1175-R1182
59. Cai B, Dong W, Sharpe S, Deitch EA, Ulloa L: Survival and inflammatory responses in experimental models of hemorrhage. J Surg Res 2011; 169: 257-266
60. Gonzalez RJ, Moore EE, Ciesla DJ, Nieto JR, Johnson JL, Silliman CC: Post-hemorrhagic shock mesenteric lymph activates human pulmonary microvascular endothelium for in vitro neutrophil-mediated injury: The role of intercellular adhesion molecule-1. J Trauma 2003; 54: 219-223
61. Hoppen RA, Corso CO, Grezzana TJ, Severino A, Dal-Pizzol F, Ritter C: Hypertonic saline and hemorrhagic shock: Hepatocellular function and integrity after six hours of treatment. Acta Cir Bras 2005; 20: 414-417
62. Rupani B, Caputo FJ, Watkins AC, Vega D, Magnotti LJ, Lu Q, Xu da Z, Deitch EA: Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock. Surgery 2007; 141: 481-489
63. Yang R, Harada T, Mollen KP, Prince JM, Levy RM, Englert JA, Gallowitsch-Puerta M, Yang L, Yang H, Tracey KJ, Harbrecht BG, Billiar TR, Fink MP: Anti-HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. Mol Med 2006; 12: 105-114
64. Zingarelli B, Ischiropoulos H, Salzman AL, Szabo C: Amelioration by mercaptoethylguanidine of the vascular and energetic failure in haemorrhagic shock in the anesthetised rat. Eur J Pharmacol 1997; 338: 55-65
65. Chiara O, Pelosi P, Brazzi L, Bottino N, Taccone P, Cimbanassi S, Segala M, Gattinoni L, Scalea T: Resuscitation from hemorrhagic shock: Experimental model comparing normal saline, dextran, and hypertonic saline solutions. Crit Care Med 2003; 31: 1915-1922
66. George ME, Mulier KE, Beilman GJ: Hypothermia is associated with improved outcomes in a porcine model of hemorrhagic shock. J Trauma 2010; 68: 662-668
67. Soller BR, Khan T, Favreau J, Hsi C, Puyana JC, Heard SO: Investigation of muscle pH as an indicator of liver pH and injury from hemorrhagic shock. J Surg Res 2003; 114: 195-201
68. Szebeni J, Baranyi L, Savay S, Gotze O, Alving CR, Bunger R, Mongan PD: Complement activation during hemorrhagic shock and resuscitation in swine. Shock 2003; 20: 347-355
69. 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 ischemiareperfusion. J Trauma 2002; 52: 625-631, discussion 632
70. York GB, Eggers JS, Smith DL, Jenkins DH, McNeil JD, Mueller D, Josephs JD, Kerby JD: Low-volume resuscitation with a polymerized bovine hemoglobin-based oxygen-carrying solution (HBOC-201) provides adequate tissue oxygenation for survival in a porcine model of controlled hemorrhage. J Trauma 2003; 55: 873-885
71. Cooper ES, Bateman SW, Muir WW: Evaluation of hyperviscous fluid resuscitation in a canine model of hemorrhagic shock: A randomized, controlled study. J Trauma 2009; 66: 1365-1373
72. Redl H, Krosl P, Schlag G, Hammerschmidt D: Permeability studies in a hypovolemic traumatic shock mod -el -comparison of Ringer's lactate and albumin as volume replacement fluids. Resuscitation 1989; 17: 77-90
73. Garcia-Martinez D, Portilla-de Buen E, Leal C, Santillan P, Muniz J: The immediate response to severe shock in a canine model with a combination of hypertonic-hyperoncotic solution with naloxone. Shock 2006; 26: 379-385
74. Huang Y, Zeng Q, Luo A: The change of arteriovenous carbon dioxide and pH gradients during severe hemorrhagic shock and resuscitation. Chin Med Sci J 1998; 13: 53-55
75. Poole GV Jr, Prough DS, Johnson JC, Stullken EH, Stump DA, Howard G: Effects of resuscitation from hemorrhagic shock on cerebral hemodynamics in the presence of an intracranial mass. J Trauma 1987; 27: 18-23
76. Bedirli A, Sozuer EM, Muhtaroglu S, Alper M: The role of oxygen free radicals and nitric oxide in organ injury following hemorrhagic shock and reinfusion. Int J Surg Investig 2000; 2: 275-284
77. Cannon W, Frasen J, Cowel E: The preventive treatment of wound shock. JAMA 1918; 70: 618-621
78. Burris D, Rhee P, Kaufmann C, Pikoulis E, Austin B, Eror A, DeBraux S, Guzzi L, Leppaniemi A: Controlled resuscitation for uncontrolled hemorrhagic shock. J Trauma 1999; 46: 216-223
79. Bickell WH, Bruttig SP, Millnamow GA, O'Benar J, Wade CE: The detrimental effects of intravenous crystalloid after aortotomy in swine. Surgery 1991; 110: 529-536
80. Alam HB, Punzalan CM, Koustova E, Bowyer MW, Rhee P: Hypertonic saline: Intraosseous infusion causes myonecrosis in a dehydrated swine model of uncontrolled hemorrhagic shock. J Trauma 2002; 52: 18-25
81. Bruscagin V, de Figueiredo LF, Rasslan S, Varicoda EY, Rocha e Silva M: Fluid resuscitation improves hemodynamics without increased bleeding in a model of uncontrolled hemorrhage induced by an iliac artery tear in dogs. J Trauma 2002; 52: 1147-1152
82. Heinius G, Hahn RG, Sonden A: Hypothermia increases rebleeding during uncontrolled hemorrhage in the rat. Shock 2011; 36: 60-66
83. Hirst H, Brinkman J, Beasley A, Crocker R, O'Sullivan J: The effects of blood pressure on rebleeding when using ExcelArrest TM in a porcine model of lethal femoral injury. J Emerg Trauma Shock 2011; 4: 207-211
84. Krausz MM, Hirsh M: Bolus versus continuous fluid resuscitation and splenectomy for treatment of uncontrolled hemorrhagic shock after massive splenic injury. J Trauma 2003; 55: 62-68
85. Krausz M, Bashenko Y, Hirsh M: Crystalloid or colloid resuscitation of uncontrolled hemorrhagic shock after moderate splenic injury. Shock 2000; 13: 230-235
86. Sondeen JL, Prince MD, Kheirabadi BS, Wade CE, Polykratis IA, de Guzman R, Dubick MA: Initial resuscitation with plasma and other blood components reduced bleeding compared to hetastarch in anesthetized swine with uncontrolled splenic hemorrhage. Transfusion 2011; 51: 779-792
87. Varicoda EY, Poli de Figueiredo LF, Cruz RJ Jr, Silva LE, Rocha e Silva M: Blood loss after fluid resuscitation with isotonic or hypertonic saline for the initial treatment of uncontrolled hemorrhage induced by spleen rupture. J Trauma 2003; 55: 112-117
88. Matsuoka T, Hildreth J, Wisner DH: Liver injury as a model of uncontrolled hemorrhagic shock: Resuscitation with different hypertonic regimens. J Trauma 1995; 39: 674-680
89. Todd SR, Malinoski D, Muller PJ, Schreiber MA: Lactated Ringer's is superior to normal saline in the resuscitation of uncontrolled hemorrhagic shock. J Trauma 2007; 62: 636-639
90. Kiraly L, Differding J, Enomoto T, Sawai R, Muller P, Diggs B, Tieu B, Englehart M, Underwood S, Wiesberg T, Schreiber M: Resuscitation with normal saline (NS) vs. lactated ringers (LR) modulates hypercoagulability and leads to increased blood loss in an uncontrolled hemorrhagic shock swine model. J Trauma 2006; 61: 57-64
91. Kentner R, Safar P, Behringer W, Wu X, Henchir J, Ma L, Hsia CJ, Tisherman SA: Small volume resuscitation with tempol is detrimental during uncontrolled hemorrhagic shock in rats. Resuscitation 2007; 72: 295-305
92. Capone AC, Safar P, Stezoski W, Tisherman S, Peitzman AB: Improved outcome with fluid restriction in treatment of uncontrolled hemorrhagic shock. J Am Coll Surg 1995; 180: 49-56
93. Krausz MM, Horn Y, Gross D: The combined effect of small volume hypertonic saline and normal saline solutions in uncontrolled hemorrhagic shock. Surg Gynecol Obstet 1992; 174: 363-368
94. Sondeen J, Dubick M, Holcomb J, Wade C: Uncontrolled hemorrhage differs from volume-or pressure-matched controlled hemorrhage in swine. Shock 2007; 28: 426-433
95. Rady MY, Kirkman E, Cranley J, Little RA: Nociceptive somatic nerve stimulation and skeletal muscle injury modify systemic hemodynamics and oxygen transport and utilization after resuscitation from hemorrhage. Crit Care Med 1996; 24: 623-630
96. Blalock A: Principles of surgical care, shock and other problems. JAMA 1941; 116: 548-548
97. American College of Surgeons: Shock; in: Advanced Trauma Life Support Manual. Chicago, American College of Surgeons, 1997, pp 87-108
98. Rixen D, Neugebauer EAM: Changing paradigms in animal models of traumatic/hemorrhagic shock. Eur J Trauma 2004; 30: 279-288
99. Crowell JW, Smith EE: Oxygen deficit and irreversible hemorrhagic shock. Am J Physiol 1964; 206: 313-316
100. Rixen D, Siegel JH: Bench-To-bedside review: Oxygen debt and its metabolic correlates as quantifiers of the severity of hemorrhagic and post-Traumatic shock. Crit Care 2005; 9: 441-453
101. Dunham CM, Siegel JH, Weireter L, Fabian M, Goodarzi S, Guadalupi P, Gettings L, Linberg SE, Vary TC: Oxygen debt and metabolic acidemia as quantitative predictors of mortality and the severity of the ischemic insult in hemorrhagic shock. Crit Care Med 1991; 19: 231-243
102. Diodato MD, Knoferl MW, Schwacha MG, Bland KI, Chaudry IH: Gender differences in the inflammatory response and survival following haemorrhage and subsequent sepsis. Cytokine 2001; 14: 162-169
103. Angele M, Schwacha M, Ayala A, Chaudry I: Effect of gender and sex hormones on immune responses following shock. Shock 2000; 14: 81-90
104. Nickel E, Schwacha M, Schneider C, Bland K, Chaudry I: Trauma-haemorrhage-induced alterations in thymic prolactin receptor expression: Implications in immune dysfunction. Cytokine 2002; 18: 127-132
105. Matsutani T, Kang S, Miyashita M, Sasajima K, Choudhry M, Bland K, Chaudry I: Liver cytokine production and ICAM-1 expression following bone fracture, tissue trauma, and hemorrhage in middle-Aged mice. Am J Physiol Gastrointest Liver Physiol 2007; 292: 268-274
106. Brunner E, Cheng S, Berman M: Effects of anesthesia on intermediary metabolism. Annu Rev Med 1975; 26: 391-401
107. Hauser G, Dayao E, Zukowskagrojec Z: Effect of pentobarbital anesthesia on the pressor reponse to agonists in vivo in normal and endotoxemic rats. Res Commun Mol Pathol Pharmacol 1995; 90: 289-300
108. Stenseth R, Berg E, Bjella L, Christensen O, Levang O, Gisvold S: The influence of thoracic epidural analgesia alone and in combination with general anesthesia on cardiovascular function and myocordial metabolism in patients receiving beta-Adrenergic blockers. Anesth Analg 1993; 77: 463-468
109. Kelbel I, Weiss M: Anaesthetics and immune function. Curr Opin Anaesthesiol 2001; 14: 685-691
110. Hilburger M, Adler M, Truant A, Meissler J, Satishchandran V, Rogers T, Eisenstein T: Morphine induces sepsis in mice. J Infect Dis 1997; 176: 183-188
111. Le Page GA: The effects of hemorrhage on tissue metabolites. Am J Physiol 1946; 147: 446-453
112. Collins JA, Stechenberg L: The effects of the concentration and function of hemoglobin on the survival of rats after hemorrhage. Surgery 1979; 85: 412-418
113. Sayeed MM, Baue AE: Mitochondrial metabolism of succinate, beta-hydroxybutyrate, and alpha-ketoglutarate in hemorrhagic shock. Am J Physiol 1971; 220: 1275-1281
114. Rana M, Singh G, Wang P, Ayala A, Zhou M, Chaudry I: Protective effects of preheparinization on the microvasculature during and after hemmorhagic shock. J Trauma 1992; 32: 420-426
115. Mackway-Jones K, Foex BA, Kirkman E, Little RA: Modification of the cardiovascular response to hemorrhage by somatic afferent nerve stimulation with special reference to gut and skeletal muscle blood flow. J Trauma 1999; 47: 481-485
116. Chaudry I, Wang P, Singh G, Hauptman J, Ayala A: Rat and mouse models of hypovolemic-Traumatic shock.; in Schlag G, Redl H (eds): Pathophysiology of Shock, Sepsis, and Organ Failure. Berlin, Springer, 1993, pp 371-383
117. Lu Q, Xu D, Sharpe S, Doucet D, Pisarenko V, Lee M, Deitch E: The anatomic sites of disruption of the mucus layer directly correlate with areas of trauma/hemorrhagic shock-induced gut injury. J Trauma 2011; 70: 630-635
118. Gill R, Ruan X, Menzel C, Namkoong S, Loughran P, Hackam D, Billiar T: Systemic inflammation and liver injury following hemorrhagic shock and peripheral tissue trauma involve functional TLR9 signaling on bone marrowderived cells and parenchymal cells. Shock 2011; 35: 164-170
119. Krausz M, Bashenko Y, Hirsh M: Improved survival in uncontrolled hemorrhagic shock induced by massive splenic injury in the proestrus phase of the reproductive cycle in the female rat. Shock 2003; 20: 444-448
120. Brundage S, Schreiber M, Holcomb J, Zautke N, Mastrangelo M, Xq X, Macaitis J, Tweardy D: Amplification of the proinflammatory transcription factor cascade increases with severity of uncontrolled hemorrhage in swine. J Surg Res 2003; 113: 74-80
121. Howes D, Stratford A, Stirling M, Ferri C, Bardell T: Administration of recombinant factor VIIa decreases blood loss after blunt trauma in noncoagulopathic pigs. J Trauma 2007; 62: 311-314
122. Alam HB, Shuja F, Butt MU, Duggan M, Li Y, Zacharias N, Fukudome EY, Liu B, Demoya M, Velmahos GC: Surviving blood loss without blood transfusion in a swine poly-Trauma model. Surgery 2009; 146: 325-333
123. Kauvar D, Baer D, Dubick M, Walters T: Effect of fluid resuscitation on acute skeletal muscle ischemia-reperfusion injury after hemorrhagic shock in rats. J Am Coll Surg 2006; 202: 888-896
124. Labruto F, Song X, Valen G, Vaage J: Lazaroid U-83836E improves tolerance to hemorrhagic shock and limb ischemia and reperfusion in rats and increases cardiac heat shock protein 72. Acad Emerg Med 2006; 13: 7-12
125. Verhoeven E, Prins T, van den Dungen J, Tielliu I, Hulsebos R, van Schilfgaarde R: Endovascular repair of acute AAAs under local anesthesia with bifurcated endografts: A feasibility study. J Endovasc Ther 2002; 9: 729-735
126. Owens TM, Watson WC, Prough DS, Uchida T, Kramer GC: Limiting initial resuscitation of uncontrolled hemorrhage reduces internal bleeding and subsequent volume requirements. J Trauma 1995; 39: 200-207, discussion 208-209
127. Kowalenko T, Stern S, Dronen S, Xu W: Improved outcome with hypotensive resuscitation of uncontrolled hemorrhagic shock in a swine model. J Trauma 1992; 33: 349-353
128. Harkin DW, Romaschin A, Taylor SM, Rubin BB, Lindsay TF: Complement C5a receptor antagonist attenuates multiple organ injury in a model of ruptured abdominal aortic aneurysm. J Vasc Surg 2004; 39: 196-206