Disseminated intravascular coagulation in a novel porcine model of severe Staphylococcus aureus sepsis fulfills human clinical criteria

Journal of Comparative Pathology

Volumn 149, Issue 4, 2013, Pages 463-474

  Soerensen, K E ^a,c   Olsen, H G ^a   Skovgaard, K ^b   Wiinberg, B ^a   Nielsen, O L ^a   Leifsson, P S ^a   Jensen, H E ^a   Kristensen, A T ^a   Iburg, T M ^a,c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c NATIONAL VETERINARY INSTITUTE   (Sweden)

Author keywords

DIC; Porcine model; Sepsis; Staphylococcus aureus

Indexed keywords

ACUTE PHASE PROTEIN; ANTITHROMBIN; C REACTIVE PROTEIN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FIBRINOGEN; MESSENGER RNA; PROCOAGULANT; VON WILLEBRAND FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING TIME; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DISSEMINATED INTRAVASCULAR CLOTTING; DOWN REGULATION; EXPERIMENTAL PIG; FEMALE; FIBRINOGEN BLOOD LEVEL; FIBRINOLYSIS; HISTOPATHOLOGY; HYPERCOAGULABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCAL BACTEREMIA; STAPHYLOCOCCUS AUREUS; THROMBOELASTOGRAPHY; UPREGULATION;

ANIMALIA; STAPHYLOCOCCUS AUREUS; SUIDAE; SUS;

DIC; PORCINE MODEL; SEPSIS; STAPHYLOCOCCUS AUREUS;

ANIMALS; DISEASE MODELS, ANIMAL; DISSEMINATED INTRAVASCULAR COAGULATION; FEMALE; HUMANS; REAL-TIME POLYMERASE CHAIN REACTION; SEPSIS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; SWINE;

EID: 84884821717     PISSN: 00219975     EISSN: 15323129     Source Type: Journal    
DOI: 10.1016/j.jcpa.2013.04.003     Document Type: Article

References (56)

1. Aird W.C.M. Vascular bed-specific hemostasis: role of endothelium in sepsis pathogenesis. Critical Care Medicine 2001, 29:S28-S34.
2. Andersen C.L., Jensen J.L., Orntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research 2004, 64:5245-5250.
3. Bancroft J., Gamble M. Theory and Practice of Histological Techniques 2007, Churchill Livingstone, New York. 6th Edit.
4. Bauer P.R. Microvascular responses to sepsis: clinical significance. Pathophysiology 2002, 8:141-148.
5. Berthelsen L.O., Kristensen A.T., Wiinberg B., Tranholm M. Implementation of the ISTH classification of non-overt DIC in a thromboplastin-induced rabbit model. Thrombosis Research 2009, 124:490-497.
6. Bick R.L. Disseminated intravascular coagulation. Disorders of Thrombosis and Haemostasis. Clinical and Laboratory Practice 2002, 139-164. Lippincott, Willams and Wilkins, Philadelphia. 3rd Edit. R.L. Bick (Ed.).
7. Bick R.L., Arun B., Frenkel E.P. Disseminated intravascular coagulation - clinical and pathophysiological mechanisms and manifestations. Haemostasis 1999, 29:111-134.
8. Bick R.L., Murano G. Physiology of hemostasis. Disorders of Thrombosis and Haemostasis. Clinical and Laboratory Practice 2002, 1-29. Lippincott, Willams and Wilkins, Philadelphia. 3rd Edit. R.L. Bick (Ed.).
9. Bone R.C. Gram-positive organisms and sepsis. Archives of Internal Medicine 1994, 154:26-34.
10. Franco R.F., de Jonge E., Dekkers P.E.P., Timmerman J.J., Spek C.A., et al. The in-vivo kinetics of tissue factor messenger RNA expression during human endotoxemia: relationship with activation of coagulation. Blood 2000, 96:554-559.
11. Gebrane-Younes J., Drouet L., Caen J.P., Orcel L. Heterogeneous distribution of Weibel-Palade bodies and von Willebrand factor along the porcine vascular tree. American Journal of Pathology 1991, 139:1471-1484.
12. Goldfarb R.D., Dellinger R.P., Parrillo J.E. Porcine models of severe sepsis: emphasis on porcine peritonitis. Shock 2005, 24:S75-S81.
13. Hack C.E., de Groot E.R., Felt-Bersma R.J., Nuijens J.H., Strack Van Schijndel R.J., et al. Increased plasma levels of interleukin-6 in sepsis. Blood 1989, 74:1704-1710.
14. Hack C.E., Zeerleder S. The endothelium in sepsis: source of and a target for inflammation. Critical Care Medicine 2001, 29:S21-S27.
15. Hoffman M., Monroe D.M., Roberts H.R. Cellular interactions in hemostasis. Haemostasis 1996, 26:S12-S16.
16. Kayal S., Jais J.P., Aguini N., Chaudiere J., Labrousse J. Elevated circulating E-selectin, intercellular adhesion molecule 1, and von Willebrand factor in patients with severe infection. American Journal of Respiratory Critical Care Medicine 1998, 157:776-784.
17. Kvist P.H., Bielecki M., Gerstenberg M., Rossmeisl C., Jensen H.E., et al. Evaluation of subcutaneously-implanted glucose sensors for continuous glucose measurements in hyperglycemic pigs. InVivo 2006, 20:195-203.
18. Leifsson P.S., Iburg T., Jensen H.E., Agerholm J.S., Kjelgaard-Hansen M., et al. Intravenous inoculation of Staphylococcus aureus in pigs induces severe sepsis asindicated by increased hypercoagulability and hepatic dysfunction. FEMS Microbiology Letters 2010, 309:208-216.
19. Levi M. Disseminated intravascular coagulation. Critical Care Medicine 2007, 35:2191-2195.
20. Levi M. The coagulant response in sepsis and inflammation. Hämostaseologie 2010, 30:10-16.
21. Levi M., de Jonge E., van der Poll T., ten Cate H. Disseminated intravascular coagulation. Journal of Thrombosis and Haemostasis 1999, 82:695-705.
22. Lupu C., Westmuckett A.D., Peer G., Ivanciu L., Zhu H., et al. Tissue factor-dependent coagulation is preferentially up-regulated within arterial branching areas in a baboon model of Escherichia coli sepsis. American Journal of Pathology 2005, 167:1161-1172.
23. Madoiwa S., Nunomiya S., Ono T., Shintani Y., Ohmori T., et al. Plasminogen activator inhibitor 1 promotes a poor prognosis in sepsis-induced disseminated intravascular coagulation. International Journal of Hematology 2006, 84:398-405.
24. Martin G.S., Mannino D.M., Eaton S., Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. New England Journal of Medicine 2003, 348:1546-1554.
25. McKay D.G. Progress in disseminated intravascular coagulation. California Medicine 1969, 111:186-198.
26. Moesgaard S.G., Olsen L.H., Aasted B., Viuff B.M., Pedersen L.G., et al. Direct measurements of nitric oxide release in relation to expression of endothelial nitric oxide synthase in isolated porcine mitral valves. Journal of Veterinary Medicine A; Physiology Pathology and Clinical Medicine 2007, 54:156-160.
27. Moncada S., Higgs A. The l-arginine-nitric oxide pathway. New England Journal of Medicine 1993, 329:2002-2012.
28. Nielsen O.L., Iburg T., Aalbaek B., Leifsson P.S., Agerholm J.S., et al. A pig model of acute Staphylococcus aureus induced pyemia. Acta Veterinaria Scandinavica 2009, 51. [online edition].
29. Nikolic N.L., Wiinberg B., Kjelgaard H.M., Jensen A.L., Kristensen A.T. Prolonged activated prothromboplastin time and breed specific variation in haemostatic analytes in healthy adult Bernese Mountain dogs. Veterinary Journal 2011, 190:150-153.
30. Osterud B. Tissue factor expression in blood cells. Thrombosis Research 2010, 125:S31-S34.
31. Palsgaard-Van Lue A., Strøm H., Lee M.H., Jensen A.L., Birck M.M., et al. Cellular, hemostatic and inflammatory parameters of the surgical stress response in pigs undergoing partial pericardectomy via open thoracotomy or thoracoscopy. Surgical Endoscopy and Other Interventional Techniques 2007, 21:785-792.
32. Parker S.J., Watkins P.E. Experimental models ofgram-negative sepsis. British Journal of Surgery 2001, 88:22-30.
33. Pawlinski R., Mackman N. Cellular sources of tissue factor in endotoxemia and sepsis. Thrombosis Research 2010, 125:S70-S73.
34. Pors S.E., Chadfield M.S., Sorensen D.B., Offenberg H., Heegaard P.M.H., et al. Pathology, tissue metalloproteinase transcription and haptoglobin responses in mice after experimental challenge with different isolates of Pasteurella multocida obtained from cases of porcine pneumonia. Journal of Comparative Pathology 2011, 145:251-260.
35. Rees D.D., Palmer R.M., Moncada S. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proceedings of the National Academy of Sciences of the USA 1989, 86:3375-3378.
36. Reinhart K., Bayer O., Brunkhorst F., Meisner M. Markers of endothelial damage in organ dysfunction and sepsis. Critical Care Medicine 2002, 30:S302-S312.
37. Ribes J.A., Francis C.W., Wagner D.D. Fibrin induces release of von Willebrand factor from endothelial cells. Journal of Clinical Investigation 1987, 79:117-123.
38. Robboy S.J., Major M.C., Colman R.W., Minna J.D. Pathology of disseminated intravascular coagulation (DIC). Analysis of 26 cases. Human Pathology 1972, 3:327-343.
39. Schiefer B., Searcy G. Disseminated intravascular coagulation and consumption coagulopathy. Canadian Veterinary Journal 1975, 16:151-159.
40. Schleef R.R., Bevilacqua M.P., Sawdey M., Gimbrone M.A., Loskutoff D.J. Cytokine activation of vascular endothelium. Effects on tissue-type plasminogen activator and type 1 plasminogen activator inhibitor. Journal of Biological Chemistry 1988, 263:5797-5803.
41. Schorer A.E., Moldow C.F., Rick M.E. Interleukin 1 or endotoxin increases the release of von Willebrand factor from human endothelial cells. British Journal of Haematology 1987, 67:193-197.
42. Skjorten F., Kierulf P.B., Degre M. Formation of hyaline microthrombi in the mouse. Evidence for dependence on the fibrinolytic system. Acta Pathologica et Microbiologica Scandinavica; Section A - Pathology 1970, 78:351-361.
43. Skovgaard K., Mortensen S., Boye M., Poulsen K.T., Campbell F.M., et al. Rapid and widely disseminated acute phase protein response after experimental bacterial infection of pigs. Veterinary Research 2009, 40:23.
44. Skovgaard K., Mortensen S., Poulsen K.T., Angen O., Heegaard P.M. Validation of putative reference genes for qRT-PCR normalization in tissues and blood from pigs infected with Actinobacillus pleuropneumoniae. Veterinary Immunology and Immunopathology 2007, 118:140-146.
45. Soerensen K.E., Nielsen O.L., Birck M.M., Leifsson P.S., Jensen H.E., et al. The use of sequential organ failure assessment parameters in an awake porcine model of severe Staphylococcus aureus sepsis. APMIS 2012, 120:909-921.
46. Soerensen K.E., Skovgaard K., Heegaard P., Jensen H.E., Nielsen O.L., et al. The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs. Veterinary Pathology 2012, 49:950-962.
47. Taylor F.B., Toh C.H., Hoots W.K., Wada H., Levi M. Towards definition, clinical and laboratory criteria, and a scoring system for disseminated intravascular coagulation - on behalf of the Scientific Subcommittee on Disseminated Intravascular Coagulation (DIC) of the International Society on Thrombosis and Haemostasis (ISTH). Thrombosis and Haemostasis 2001, 86:1327-1330.
48. Vandesompele J., de Preter K., Pattyn F., Poppe B., Van Roy N., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 2002, 3. [online edition].
49. Vincent J.L., Sakr Y., Sprung C.L., Ranieri V.M., Reinhart K., et al. Sepsis in European intensive care units: results of the SOAP study. Critical Care Medicine 2006, 34:344-353.
50. Wang L., Wei W., Hu Y., Song S., Yan Z. An oligonucleotide decoy for nuclear factor-κ B inhibits tumor necrosis factor-α-induced human umbilical cord vein endothelial cell tissue factor expression invitro. Blood Coagulation and Fibrinolysis 2004, 15:483-490.
51. Wiinberg B., Jensen A.L., Johansson P.I., Rozanski E., Tranholm M., et al. Thromboelastographic evaluation of hemostatic function in dogs with disseminated intravascular coagulation. Journal of Veterinary Internal Medicine 2008, 22:357-365.
52. Wiinberg B., Jensen A.L., Kjelgaard-Hansen M., Rojkjaer R., Johansson P.I., et al. Study on biological variation of haemostatic parameters in clinically healthy dogs. Veterinary Journal 2007, 174:62-68.
53. Wiinberg B., Jensen A.L., Rojkjaer R., Johansson P., Kjelgaard-Hansen M., et al. Validation of human recombinant tissue factor-activated thromboelastography on citrated whole blood from clinically healthy dogs. Veterinary Clinical Pathology 2005, 34:389-393.
54. Wiinberg B., Jensen A.L., Rozanski E., Johansson P.I., Kjelgaard-Hansen M., et al. Tissue factor activated thromboelastography correlates to clinical signs of bleeding in dogs. Veterinary Journal 2009, 179:121-129.
55. Wiinberg B., Kristensen A.T. Thromboelastography in veterinary medicine. Seminars in Thrombosis and Hemostasis 2010, 36:747-756.
56. Yao L., Bengualid V., Lowy F.D., Gibbons J.J., Hatcher V.B., et al. Internalization of Staphylococcus aureus by endothelial cells induces cytokine gene expression. Infection and Immunity 1995, 63:1835-1839.