Balance between Hyperinflammation and Immunosuppression in Sepsis

Seminars in Respiratory and Critical Care Medicine

Volumn 37, Issue 1, 2016, Pages 42-50

  Yadav, Hemang ^a   Cartin Ceba, Rodrigo ^a  

^a MAYO CLINIC   (United States)

Author keywords

glucocorticoid; immunology; immunosuppression; sepsis

Indexed keywords

IMMUNOMODULATING AGENT; GLUCOCORTICOID;

ARTICLE; CAUSE OF DEATH; HOSPITAL PATIENT; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSTIMULATION; INFLAMMATION; INTENSIVE CARE UNIT; MORBIDITY; MORTALITY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SEPSIS; ADVERSE EFFECTS; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; INTENSIVE CARE; PROCEDURES; RANDOMIZED CONTROLLED TRIAL (TOPIC);

CRITICAL CARE; GLUCOCORTICOIDS; HUMANS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SEPSIS;

EID: 84956474298     PISSN: 10693424     EISSN: 10989048     Source Type: Journal    
DOI: 10.1055/s-0035-1570356     Document Type: Article

References (82)

1. Gaieski D. F., Edwards J. M., Kallan M. J., Carr B. G. Benchmarking the incidence and mortality of severe sepsis in the United States. Crit Care Med: 2013; 41 5 1167 1174
2. Martin G. S., Mannino D. M., Eaton S., Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med: 2003; 348 16 1546 1554
3. Kaukonen K. M., Bailey M., Suzuki S., Pilcher D., Bellomo R. Mortality related to severe sepsis and septic shock among critically ill patients in Australia and New Zealand, 2000-2012. JAMA: 2014; 311 13 1308 1316
4. Miller R. R. III, Dong L., Nelson N. C., et al. Intermountain Healthcare Intensive Medicine Clinical Program Multicenter implementation of a severe sepsis and septic shock treatment bundle. Am J Respir Crit Care Med: 2013; 188 1 77 82
5. Lagu T., Rothberg M. B., Shieh M. S., Pekow P. S., Steingrub J. S., Lindenauer P. K. Hospitalizations, costs, and outcomes of severe sepsis in the United States 2003 to 2007. Crit Care Med: 2012; 40 3 754 761
6. Hotchkiss R. S., Monneret G., Payen D. Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat Rev Immunol: 2013; 13 12 862 874
7. Maslove D. M., Tang B. M., McLean A. S. Identification of sepsis subtypes in critically ill adults using gene expression profiling. Crit Care: 2012; 16 5 R183
8. Takasu O., Gaut J. P., Watanabe E., et al. Mechanisms of cardiac and renal dysfunction in patients dying of sepsis. Am J Respir Crit Care Med: 2013; 187 5 509 517
9. Crouser E. D., Julian M. W., Blaho D. V., Pfeiffer D. R. Endotoxin-induced mitochondrial damage correlates with impaired respiratory activity. Crit Care Med: 2002; 30 2 276 284
10. Rosser D. M., Stidwill R. P., Jacobson D., Singer M. Cardiorespiratory and tissue oxygen dose response to rat endotoxemia. Am J Physiol: 1996; 271 3, Pt 2 H891 H895
11. Kirschenbaum L. A., Aziz M., Astiz M. E., Saha D. C., Rackow E. C. Influence of rheologic changes and platelet-neutrophil interactions on cell filtration in sepsis. Am J Respir Crit Care Med: 2000; 161 5 1602 1607
12. Piagnerelli M., Boudjeltia K. Z., Brohee D., Vincent J. L., Vanhaeverbeek M. Modifications of red blood cell shape and glycoproteins membrane content in septic patients. Adv Exp Med Biol: 2003; 510 109 114
13. Coopersmith C. M., Stromberg P. E., Dunne W. M., et al. Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis. JAMA: 2002; 287 13 1716 1721
14. Vincent J. L., Zhang H., Szabo C., Preiser J. C. Effects of nitric oxide in septic shock. Am J Respir Crit Care Med: 2000; 161 6 1781 1785
15. Sharshar T., Gray F., Lorin de la Grandmaison G., et al. Apoptosis of neurons in cardiovascular autonomic centres triggered by inducible nitric oxide synthase after death from septic shock. Lancet: 2003; 362 9398 1799 1805
16. Tsuneyoshi I., Yamada H., Kakihana Y., Nakamura M., Nakano Y., Boyle W. A. III. Hemodynamic and metabolic effects of low-dose vasopressin infusions in vasodilatory septic shock. Crit Care Med: 2001; 29 3 487 493
17. Landry D. W., Levin H. R., Gallant E. M., et al. Vasopressin deficiency contributes to the vasodilation of septic shock. Circulation: 1997; 95 5 1122 1125
18. Hoffmann J. N., Werdan K., Hartl W. H., Jochum M., Faist E., Inthorn D. Hemofiltrate from patients with severe sepsis and depressed left ventricular contractility contains cardiotoxic compounds. Shock: 1999; 12 3 174 180
19. Boomer J. S., Green J. M., Hotchkiss R. S. The changing immune system in sepsis: is individualized immuno-modulatory therapy the answer? Virulence: 2014; 5 1 45 56
20. Casey L. C. Immunologic response to infection and its role in septic shock. Crit Care Clin: 2000; 16 2 193 213
21. Suffredini A. F., Fromm R. E., Parker M. M., et al. The cardiovascular response of normal humans to the administration of endotoxin. N Engl J Med: 1989; 321 5 280 287
22. Guidet B., Barakett V., Vassal T., Petit J. C., Offenstadt G. Endotoxemia and bacteremia in patients with sepsis syndrome in the intensive care unit. Chest: 1994; 106 4 1194 1201
23. Frantz S., Ertl G., Bauersachs J. Mechanisms of disease: Toll-like receptors in cardiovascular disease. Nat Clin Pract Cardiovasc Med: 2007; 4 8 444 454
24. Hutchins N. A., Unsinger J., Hotchkiss R. S., Ayala A. The new normal: immunomodulatory agents against sepsis immune suppression. Trends Mol Med: 2014; 20 4 224 233
25. Ritter C., Andrades M., Frota Júnior M. L., et al. Oxidative parameters and mortality in sepsis induced by cecal ligation and perforation. Intensive Care Med: 2003; 29 10 1782 1789
26. Gao X. P., Standiford T. J., Rahman A., et al. Role of NADPH oxidase in the mechanism of lung neutrophil sequestration and microvessel injury induced by Gram-negative sepsis: studies in p47phox-/- and gp91phox-/- mice. J Immunol: 2002; 168 8 3974 3982
27. Goode H. F., Cowley H. C., Walker B. E., Howdle P. D., Webster N. R. Decreased antioxidant status and increased lipid peroxidation in patients with septic shock and secondary organ dysfunction. Crit Care Med: 1995; 23 4 646 651
28. Long C. L., Maull K. I., Krishnan R. S., et al. Ascorbic acid dynamics in the seriously ill and injured. J Surg Res: 2003; 109 2 144 148
29. Cowley H. C., Bacon P. J., Goode H. F., Webster N. R., Jones J. G., Menon D. K. Plasma antioxidant potential in severe sepsis: a comparison of survivors and nonsurvivors. Crit Care Med: 1996; 24 7 1179 1183
30. Galley H. F., Webster N. R. Elevated serum bleomycin-detectable iron concentrations in patients with sepsis syndrome. Intensive Care Med: 1996; 22 3 226 229
31. Yin H., Jin X. B., Gong Q., et al. Fructose-1,6-diphosphate attenuates acute lung injury induced by lipopolysaccharide in mice. Int Immunopharmacol: 2008; 8 13-14 1842 1847
32. Nunes F. B., Simões Pires M. G., Alves Filho J. C., Wächter P. H., Rodrigues De Oliveira J. Physiopathological studies in septic rats and the use of fructose 1,6-bisphosphate as cellular protection. Crit Care Med: 2002; 30 9 2069 2074
33. Xie K., Yu Y., Pei Y., et al. Protective effects of hydrogen gas on murine polymicrobial sepsis via reducing oxidative stress and HMGB1 release. Shock: 2010; 34 1 90 97
34. Angstwurm M. W., Engelmann L., Zimmermann T., et al. Selenium in Intensive Care (SIC): results of a prospective randomized, placebo-controlled, multiple-center study in patients with severe systemic inflammatory response syndrome, sepsis, and septic shock. Crit Care Med: 2007; 35 1 118 126
35. Nathens A. B., Neff M. J., Jurkovich G. J., et al. Randomized, prospective trial of antioxidant supplementation in critically ill surgical patients. Ann Surg: 2002; 236 6 814 822
36. Seok J., Warren H. S., Cuenca A. G., et al. Inflammation and Host Response to Injury, Large Scale Collaborative Research Program Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A: 2013; 110 9 3507 3512
37. Meagher L. C., Cousin J. M., Seckl J. R., Haslett C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J Immunol: 1996; 156 11 4422 4428
38. Rinehart J. J., Sagone A. L., Balcerzak S. P., Ackerman G. A., LoBuglio A. F. Effects of corticosteroid therapy on human monocyte function. N Engl J Med: 1975; 292 5 236 241
39. Borson D. B., Gruenert D. C. Glucocorticoids induce neutral endopeptidase in transformed human tracheal epithelial cells. Am J Physiol: 1991; 260 2, Pt 1 L83 L89
40. Slade J. D., Hepburn B. Prednisone-induced alterations of circulating human lymphocyte subsets. J Lab Clin Med: 1983; 101 3 479 487
41. Visser J., van Boxel-Dezaire A., Methorst D., Brunt T., de Kloet E. R., Nagelkerken L. Differential regulation of interleukin-10 (IL-10) and IL-12 by glucocorticoids in vitro. Blood: 1998; 91 11 4255 4264
42. Settipane G. A., Pudupakkam R. K., McGowan J. H. Corticosteroid effect on immunoglobulins. J Allergy Clin Immunol: 1978; 62 3 162 166
43. Winston D. J., Ho W. G., Schiffman G., Champlin R. E., Feig S. A., Gale R. P. Pneumococcal vaccination of recipients of bone marrow transplants. Arch Intern Med: 1983; 143 9 1735 1737
44. Roquilly A., Mahe P. J., Seguin P., et al. Hydrocortisone therapy for patients with multiple trauma: the randomized controlled HYPOLYTE study. JAMA: 2011; 305 12 1201 1209
45. Blum C. A., Nigro N., Briel M., et al. Adjunct prednisone therapy for patients with community-acquired pneumonia: a multicentre, double-blind, randomised, placebo-controlled trial. Lancet: 2015; 385 9977 1511 1518
46. Torres A., Sibila O., Ferrer M., et al. Effect of corticosteroids on treatment failure among hospitalized patients with severe community-acquired pneumonia and high inflammatory response: a randomized clinical trial. JAMA: 2015; 313 7 677 686
47. Siraux V., De Backer D., Yalavatti G., et al. Relative adrenal insufficiency in patients with septic shock: comparison of low-dose and conventional corticotropin tests. Crit Care Med: 2005; 33 11 2479 2486
48. Annane D., Sébille V., Charpentier C., et al. Effect of treatment with low doses of hydrocortisone and fludrocortisone on mortality in patients with septic shock. JAMA: 2002; 288 7 862 871
49. Beigel J., Eichacker P. Hydrocortisone and fludrocortisone improved 28-day survival in septic shock and adrenal insufficiency. ACP J Club: 2003; 138 2 44
50. Sprung C. L., Annane D., Keh D., et al. CORTICUS Study Group Hydrocortisone therapy for patients with septic shock. N Engl J Med: 2008; 358 2 111 124
51. Annane D., Bellissant E., Bollaert P. E., et al. Corticosteroids in the treatment of severe sepsis and septic shock in adults: a systematic review. JAMA: 2009; 301 22 2362 2375
52. Minneci P. C., Deans K. J., Eichacker P. Q., Natanson C. The effects of steroids during sepsis depend on dose and severity of illness: an updated meta-analysis. Clin Microbiol Infect: 2009; 15 4 308 318
53. Sligl W. I., Milner D. A. Jr, Sundar S., Mphatswe W., Majumdar S. R. Safety and efficacy of corticosteroids for the treatment of septic shock: a systematic review and meta-analysis. Clin Infect Dis: 2009; 49 1 93 101
54. Torgersen C., Moser P., Luckner G., et al. Macroscopic postmortem findings in 235 surgical intensive care patients with sepsis. Anesth Analg: 2009; 108 6 1841 1847
55. Hotchkiss R. S., Monneret G., Payen D. Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis: 2013; 13 3 260 268
56. Kollef K. E., Schramm G. E., Wills A. R., Reichley R. M., Micek S. T., Kollef M. H. Predictors of 30-day mortality and hospital costs in patients with ventilator-associated pneumonia attributed to potentially antibiotic-resistant gram-negative bacteria. Chest: 2008; 134 2 281 287
57. Otto G. P., Sossdorf M., Claus R. A., et al. The late phase of sepsis is characterized by an increased microbiological burden and death rate. Crit Care: 2011; 15 4 R183
58. Luyt C. E., Combes A., Deback C., et al. Herpes simplex virus lung infection in patients undergoing prolonged mechanical ventilation. Am J Respir Crit Care Med: 2007; 175 9 935 942
59. Osawa R., Singh N. Cytomegalovirus infection in critically ill patients: a systematic review. Crit Care: 2009; 13 3 R68
60. Ziemann M., Sedemund-Adib B., Reiland P., Schmucker P., Hennig H. Increased mortality in long-term intensive care patients with active cytomegalovirus infection. Crit Care Med: 2008; 36 12 3145 3150
61. Jaber S., Chanques G., Borry J., et al. Cytomegalovirus infection in critically ill patients: associated factors and consequences. Chest: 2005; 127 1 233 241
62. Meakins J. L., Pietsch J. B., Bubenick O., et al. Delayed hypersensitivity: indicator of acquired failure of host defenses in sepsis and trauma. Ann Surg: 1977; 186 3 241 250
63. Hotchkiss R. S., Swanson P. E., Freeman B. D., et al. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med: 1999; 27 7 1230 1251
64. Hotchkiss R. S., Tinsley K. W., Swanson P. E., et al. Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J Immunol: 2001; 166 11 6952 6963
65. Felmet K. A., Hall M. W., Clark R. S., Jaffe R., Carcillo J. A. Prolonged lymphopenia, lymphoid depletion, and hypoprolactinemia in children with nosocomial sepsis and multiple organ failure. J Immunol: 2005; 174 6 3765 3772
66. Boomer J. S., To K., Chang K. C., et al. Immunosuppression in patients who die of sepsis and multiple organ failure. JAMA: 2011; 306 23 2594 2605
67. Döcke W. D., Randow F., Syrbe U., et al. Monocyte deactivation in septic patients: restoration by IFN-gamma treatment. Nat Med: 1997; 3 6 678 681
68. Wasserman D., Ioannovich J. D., Hinzmann R. D., Deichsel G., Steinmann G. G. The Severe Burns Study Group Interferon-gamma in the prevention of severe burn-related infections: a European phase III multicenter trial. Crit Care Med: 1998; 26 3 434 439
69. Polk H. C. Jr, Cheadle W. G., Livingston D. H., et al. A randomized prospective clinical trial to determine the efficacy of interferon-gamma in severely injured patients. Am J Surg: 1992; 163 2 191 196
70. Dries D. J., Jurkovich G. J., Maier R. V., et al. Effect of interferon gamma on infection-related death in patients with severe injuries. A randomized, double-blind, placebo-controlled trial. Arch Surg: 1994; 129 10 1031 1041, discussion 1042
71. Unsinger J., McGlynn M., Kasten K. R., et al. IL-7 promotes T cell viability, trafficking, and functionality and improves survival in sepsis. J Immunol: 2010; 184 7 3768 3779
72. Rosenberg S. A., Sportès C., Ahmadzadeh M., et al. IL-7 administration to humans leads to expansion of CD8+ and CD4+ cells but a relative decrease of CD4+ T-regulatory cells. J Immunother: 2006; 29 3 313 319
73. Venet F., Foray A. P., Villars-Méchin A., et al. IL-7 restores lymphocyte functions in septic patients. J Immunol: 2012; 189 10 5073 5081
74. Unsinger J., Burnham C. A., McDonough J., et al. Interleukin-7 ameliorates immune dysfunction and improves survival in a 2-hit model of fungal sepsis. J Infect Dis: 2012; 206 4 606 616
75. Lévy Y., Sereti I., Tambussi G., et al. Effects of recombinant human interleukin 7 on T-cell recovery and thymic output in HIV-infected patients receiving antiretroviral therapy: results of a phase I/IIa randomized, placebo-controlled, multicenter study. Clin Infect Dis: 2012; 55 2 291 300
76. Willis C. R., Seamons A., Maxwell J., et al. Interleukin-7 receptor blockade suppresses adaptive and innate inflammatory responses in experimental colitis. J Inflamm (Lond): 2012; 9 1 39
77. Hartgring S. A., Willis C. R., Alcorn D., et al. Blockade of the interleukin-7 receptor inhibits collagen-induced arthritis and is associated with reduction of T cell activity and proinflammatory mediators. Arthritis Rheum: 2010; 62 9 2716 2725
78. Bozinovski S., Jones J. E., Vlahos R., Hamilton J. A., Anderson G. P. Granulocyte/macrophage-colony-stimulating factor (GM-CSF) regulates lung innate immunity to lipopolysaccharide through Akt/Erk activation of NFkappa B and AP-1 in vivo. J Biol Chem: 2002; 277 45 42808 42814
79. Nelson S., Heyder A. M., Stone J., et al. A randomized controlled trial of filgrastim for the treatment of hospitalized patients with multilobar pneumonia. J Infect Dis: 2000; 182 3 970 973
80. Root R. K., Lodato R. F., Patrick W., et al. Pneumonia Sepsis Study Group Multicenter, double-blind, placebo-controlled study of the use of filgrastim in patients hospitalized with pneumonia and severe sepsis. Crit Care Med: 2003; 31 2 367 373
81. Meisel C., Schefold J. C., Pschowski R., et al. Granulocyte-macrophage colony-stimulating factor to reverse sepsis-associated immunosuppression: a double-blind, randomized, placebo-controlled multicenter trial. Am J Respir Crit Care Med: 2009; 180 7 640 648
82. Bo L., Wang F., Zhu J., Li J., Deng X. Granulocyte-colony stimulating factor (G-CSF) and granulocyte-macrophage colony stimulating factor (GM-CSF) for sepsis: a meta-analysis. Crit Care: 2011; 15 1 R58