Biomarkers of endothelial activation are associated with poor outcome in critical illness

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Mikacenic, Carmen ^a   Hahn, William O ^a   Price, Brenda L ^a   Harju Baker, Susanna ^a   Katz, Ronit ^a   Kain, Kevin C ^b   Himmelfarb, Jonathan ^a   Liles, W Conrad ^a   Wurfel, Mark M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR RECEPTOR 1; VASCULAR CELL ADHESION MOLECULE 1; BIOLOGICAL MARKER;

ADULT; APACHE; ARTICLE; COMORBIDITY; CRITICALLY ILL PATIENT; FEMALE; HUMAN; INFLAMMATION; INTENSIVE CARE; MAJOR CLINICAL STUDY; MALE; MORTALITY; PROGNOSIS; SENSITIVITY ANALYSIS; SEPSIS; SEQUENTIAL ORGAN FAILURE ASSESSMENT SCORE; SHOCK; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; COHORT ANALYSIS; CRITICAL ILLNESS; METABOLISM; MIDDLE AGED; MULTIPLE ORGAN FAILURE; ORGAN DYSFUNCTION SCORE; PATHOLOGY; SURVIVAL RATE; VASCULAR ENDOTHELIUM;

BIOMARKERS; COHORT STUDIES; CRITICAL ILLNESS; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MALE; MIDDLE AGED; MULTIPLE ORGAN FAILURE; ORGAN DYSFUNCTION SCORES; PROGNOSIS; SURVIVAL RATE; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 84949907848     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141251     Document Type: Article

References (57)

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: 1250-1256. PMID: 12682500
2. 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: 1303-1310. PMID: 11445675
3. Bone RC. Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS). Ann Intern Med. 1996; 125: 680-687. PMID: 8849154
4. Thijs LG, Hack CE. Time course of cytokine levels in sepsis. Intensive Care Med 1995; 21 Suppl 2: S258-263. PMID: 8636533
5. Damas P, Canivet JL, de Groote D, Vrindts Y, Albert A, Franchimont P, et al. Sepsis and serum cytokine concentrations. Crit Care Med. 1997; 25: 405-412. PMID: 9118654
6. Bozza FA, Salluh JI, Japiassu AM, Soares M, Assis EF, Gomes RN, et al. Cytokine profiles as markers of disease severity in sepsis: a multiplex analysis. Crit Care. 2007; 11: R49. doi:10.1186/cc5783 PMID: 17448250
7. Marti L, Cervera C, Filella X, Marin JL, Almela M, Moreno A. Cytokine-release patterns in elderly patients with systemic inflammatory response syndrome. Gerontology. 2007; 53: 239-244. doi:10.1159/000101436 PMID: 17396033
8. Suárez-Santamaría M, Santolaria F, Pérez-Ramírez A, Alemán-Valls M-R, Martínez-Riera A, González-Reimers E, et al. Prognostic value of inflammatory markers (notably cytokines and procalcitonin), nutritional assessment, and organ function in patients with sepsis. Eur Cytokine Netw. 2010; 21: 19-26. doi:10.1684/ecn.2009.0185 PMID: 20146986
9. Kornblit B, Hellemann D, Munthe-Fog L, Bonde J, Strøm JJ, Madsen HO, et al. Plasma YKL-40 and CHI3L1 in systemic inflammation and sepsis-experience from two prospective cohorts. Immunobiology. 2013; 218: 1227-1234. PMID: 23706599
10. Ulla M, Pizzolato E, Lucchiari M, Loiacono M, Soardo F, Forno D, et al. Diagnostic and prognostic value of presepsin in the management of sepsis in the emergency department: a multicenter prospective study. Crit Care. 2013; 17: R168. doi:10.1186/cc12847 PMID: 23899120
11. Park DW, Kwak DS, Park YY, Chang Y, Huh JW, Lim C-M, et al. Impact of serial measurements of lysophosphatidylcholine on 28-day mortality prediction in patients admitted to the intensive care unit with severe sepsis or septic shock. J Crit Care. 2014; 29: 882.e5-11. doi:10.1016/j.jcrc.2014.05.003
12. Claeys R, Vinken S, Spapen H, ver Elst K, Decochez K, Huyghens L, et al. Plasma procalcitonin and C-reactive protein in acute septic shock: clinical and biological correlates. Crit Care Med. 2002; 30: 757-762. PMID: 11940741
13. Hack CE, De Groot ER, Felt-Bersma RJ, Nuijens JH, Strack Van Schijndel RJ, Eerenberg-Belmer AJ, et al. Increased plasma levels of interleukin-6 in sepsis. Blood. 1989; 74: 1704-1710. PMID: 2790194
14. Marty C, Misset B, Tamion F, Fitting C, Carlet J, Cavaillon JM. Circulating interleukin-8 concentrations in patients with multiple organ failure of septic and nonseptic origin. Crit Care Med. 1994; 22: 673-679. PMID: 8143477
15. Presneill JJ, Waring PM, Layton JE, Maher DW, Cebon J, Harley NS, et al. Plasma granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor levels in critical illness including sepsis and septic shock: relation to disease severity, multiple organ dysfunction, and mortality. Crit Care Med. 2000; 28: 2344-2354. PMID: 10921563
16. de Pablo R, Monserrat J, Reyes E, Diaz-Martin D, Rodriguez Zapata M, Carballo F, et al. Mortality in patients with septic shock correlates with anti-inflammatory but not proinflammatory immunomodulatory molecules. J Intensive Care Med. 2011; 26: 125-132. doi:10.1177/0885066610384465 PMID: 21464065
17. Zeni F, Freeman B, Natanson C. Anti-inflammatory therapies to treat sepsis and septic shock: a reassessment. Crit Care Med. 1997; 25: 1095-1100. PMID: 9233726
18. Aird WC. The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood. 2003; 101: 3765-3777. doi:10.1182/blood-2002-06-1887 PMID: 12543869
19. Hickey MJ, Kubes P. Intravascular immunity: the host-pathogen encounter in blood vessels. Nat Rev Immunol. 2009; 9: 364-375. doi:10.1038/nri2532 PMID: 19390567
20. Mehta D, Ravindran K, Kuebler WM. Novel regulators of endothelial barrier function. Am J Physiol Lung Cell Mol Physiol. 2014; 307: L924-935. doi:10.1152/ajplung.00318.2014 PMID: 25381026
21. Opal SM, van der Poll T. Endothelial barrier dysfunction in septic shock. J Intern Med. 2015; 277: 277-293. doi:10.1111/joim.12331 PMID: 25418337
22. Fiedler U, Augustin HG. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 2006; 27: 552-558. doi:10.1016/j.it.2006.10.004 PMID: 17045842
23. Parikh SM. Dysregulation of the angiopoietin-Tie-2 axis in sepsis and ARDS. Virulence. 2013; 4: 517-524. doi:10.4161/viru.24906 PMID: 23652985
24. Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med. 2000; 6: 460-463. doi:10.1038/74725 PMID: 10742156
25. Ricciuto DR, dos Santos CC, Hawkes M, Toltl LJ, Conroy AL, Rajwans N, et al. Angiopoietin-1 and angiopoietin-2 as clinically informative prognostic biomarkers of morbidity and mortality in severe sepsis. Crit Care Med. 2011; 39: 702-710. PMID: 21242795
26. Parikh SM, Mammoto T, Schultz A, Yuan H-T, Christiani D, Karumanchi SA, et al. Excess circulating angiopoietin-2 may contribute to pulmonary vascular leak in sepsis in humans. PLoS Med. 2006; 3: e46. doi:10.1371/journal.pmed.0030046 PMID: 16417407
27. Calfee CS, Gallagher D, Abbott J, Thompson BT, Matthay MA, NHLBI ARDS Network. Plasma angiopoietin-2 in clinical acute lung injury: prognostic and pathogenetic significance. Crit Care Med. 2012; 40: 1731-1737. PMID: 22610178
28. Agrawal A, Matthay MA, Kangelaris KN, Stein J, Chu JC, Imp BM, et al. Plasma angiopoietin-2 predicts the onset of acute lung injury in critically ill patients. Am J Respir Crit Care Med. 2013; 187: 736-742. doi:10.1164/rccm.201208-1460OC PMID: 23328529
29. Kumpers P, Gueler F, David S, Slyke PV, Dumont DJ, Park J-K, et al. The synthetic tie2 agonist peptide vasculotide protects against vascular leakage and reduces mortality in murine abdominal sepsis. Crit Care. 2011; 15: R261. doi:10.1186/cc10523 PMID: 22040774
30. Siner JM, Bhandari V, Engle KM, Elias JA, Siegel MD. Elevated serum angiopoietin 2 levels are associated with increased mortality in sepsis. Shock. 2009; 31: 348-353. PMID: 18791490
31. Schuetz P, Jones AE, Aird WC, Shapiro NI. Endothelial cell activation in emergency department patients with sepsis-related and non-sepsis-related hypotension. Shock. 2011; 36: 104-108. PMID: 21522043
32. de Pablo R, Monserrat J, Reyes E, Díaz D, Rodríguez-Zapata M, de la Hera A, et al. Circulating sICAM-1 and sE-Selectin as biomarker of infection and prognosis in patients with systemic inflammatory response syndrome. Eur J Intern Med. 2013; 24: 132-138. doi:10.1016/j.ejim.2012.10.009 PMID: 23352000
33. American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med. 1992; 20: 864-874. PMID: 1597042
34. Ko DC, Shukla KP, Fong C, Wasnick M, Brittnacher MJ, Wurfel MM, et al. A genome-wide in vitro bacterial-infection screen reveals human variation in the host response associated with inflammatory disease. Am J Hum Genet. 2009; 85: 214-227. doi:10.1016/j.ajhg.2009.07.012 PMID: 19664744
35. Knaus WA, Wagner DP, Draper EA, Zimmerman JE, Bergner M, Bastos PG, et al. The APACHE III prognostic system. Risk prediction of hospital mortality for critically ill hospitalized adults. Chest. 1991; 100: 1619-1636. PMID: 1959406
36. Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça 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: 707-710. PMID: 8844239
37. The R Project for Statistical Computing [Internet]. Available: http://www.r-project.org/.Accessed 2015 Jan 14.
38. Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA. 2012; 307: 2526-2533. doi:10.1001/jama.2012.5669 PMID: 22797452
39. Mehta RL, Kellum JA, Shah SV, Molitoris BA, Ronco C, Warnock DG, et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care. 2007; 11: R31. doi:10.1186/cc5713 PMID: 17331245
40. Lovegrove FE, Tangpukdee N, Opoka RO, Lafferty EI, Rajwans N, Hawkes M, et al. Serum angiopoietin-1 and -2 levels discriminate cerebral malaria from uncomplicated malaria and predict clinical outcome in African children. PLoS ONE. 2009; 4: e4912. doi:10.1371/journal.pone.0004912 PMID: 19300530
41. Brun-Buisson C. The epidemiology of the systemic inflammatory response. Intensive Care Med. 2000; 26 Suppl 1: S64-74. PMID: 10786961
42. David S, Mukherjee A, Ghosh CC, Yano M, Khankin EV, Wenger JB, et al. Angiopoietin-2 may contribute to multiple organ dysfunction and death in sepsis∗. Crit Care Med. 2012; 40: 3034-3041. PMID: 22890252
43. Kümpers P, Hafer C, David S, Hecker H, Lukasz A, Fliser D, et al. Angiopoietin-2 in patients requiring renal replacement therapy in the ICU: relation to acute kidney injury, multiple organ dysfunction syndrome and outcome. Intensive Care Med. 2010; 36: 462-470. doi:10.1007/s00134-009-1726-7 PMID: 19956923
44. Simmons EM, Himmelfarb J, Sezer MT, Chertow GM, Mehta RL, Paganini EP, et al. Plasma cytokine levels predict mortality in patients with acute renal failure. Kidney Int. 2004; 65: 1357-1365. doi:10.1111/j.1523-1755.2004.00512.x PMID: 15086475
45. Ziegler T, Horstkotte J, Schwab C, Pfetsch V, Weinmann K, Dietzel S, et al. Angiopoietin 2 mediates microvascular and hemodynamic alterations in sepsis. J Clin Invest. 2013; doi:10.1172/JCI66549
46. Alfieri A, Watson JJ, Kammerer RA, Tasab M, Progias P, Reeves K, et al. Angiopoietin-1 variant reduces LPS-induced microvascular dysfunction in a murine model of sepsis. Crit Care. 2012; 16: R182. doi:10.1186/cc11666 PMID: 23036162
47. Stiehl T, Thamm K, Kaufmann J, Schaeper U, Kirsch T, Haller H, et al. Lung-targeted RNA interference against angiopoietin-2 ameliorates multiple organ dysfunction and death in sepsis. Crit Care Med. 2014; 42: e654-662. PMID: 25083983
48. David S, Park J-K, van Meurs M, Zijlstra JG, Koenecke C, Schrimpf C, et al. Acute administration of recombinant Angiopoietin-1 ameliorates multiple-organ dysfunction syndrome and improves survival in murine sepsis. Cytokine. 2011; 55: 251-259. doi:10.1016/j.cyto.2011.04.005 PMID: 21531574
49. Luz Fiusa MM, Costa-Lima C, de Souza GR, Vigorito AC, Penteado Aranha FJ, Lorand-Metze I, et al. A high angiopoietin-2/angiopoietin-1 ratio is associated with a high risk of septic shock in patients with febrile neutropenia. Crit Care. 2013; 17: R169. doi:10.1186/cc12848 PMID: 23915833
50. Vassiliou AG, Mastora Z, Orfanos SE, Jahaj E, Maniatis NA, Koutsoukou A, et al. Elevated biomarkers of endothelial dysfunction/activation at ICU admission are associated with sepsis development. Cytokine. 2014; 69: 240-247. doi:10.1016/j.cyto.2014.06.010 PMID: 25016133
51. Darwish I, Liles WC. Emerging therapeutic strategies to prevent infection-related microvascular endothelial activation and dysfunction. Virulence. 2013; 4: 572-582. doi:10.4161/viru.25740 PMID: 23863603
52. Whalen MJ, Doughty LA, Carlos TM, Wisniewski SR, Kochanek PM, Carcillo JA. Intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 are increased in the plasma of children with sepsis-induced multiple organ failure. Crit Care Med. 2000; 28: 2600-2607. PMID: 10921602
53. Shapiro NI, Schuetz P, Yano K, Sorasaki M, Parikh SM, Jones AE, et al. The association of endothelial cell signaling, severity of illness, and organ dysfunction in sepsis. Crit Care. 2010; 14: R182. doi:10.1186/cc9290 PMID: 20942957
54. 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: 950-957. PMID: 10809265
55. Herrmann W, Ecker D, Quast S, Klieden M, Rose S, Marzi I. Comparison of procalcitonin, sCD14 and interleukin-6 values in septic patients. Clin Chem Lab Med. 2000; 38: 41-46. doi:10.1515/CCLM.2000.007 PMID: 10774960
56. Pettilä V, Hynninen M, Takkunen O, Kuusela P, Valtonen M. Predictive value of procalcitonin and interleukin 6 in critically ill patients with suspected sepsis. Intensive Care Med. 2002; 28: 1220-1225. doi:10.1007/s00134-002-1416-1 PMID: 12209268
57. Shehabi Y, Sterba M, Garrett PM, Rachakonda KS, Stephens D, Harrigan P, et al. Procalcitonin algorithm in critically ill adults with undifferentiated infection or suspected sepsis. A randomized controlled trial. Am J Respir Crit Care Med. 2014; 190: 1102-1110. doi:10.1164/rccm.201408-1483OC PMID: 25295709