Skip to main content
Top
Published in: Critical Care 1/2016

Open Access 01-12-2016 | Research

Neutropenic sepsis is associated with distinct clinical and biological characteristics: a cohort study of severe sepsis

Authors: John P. Reilly, Brian J. Anderson, Kristin M. Hudock, Thomas G. Dunn, Altaf Kazi, Anna Tommasini, Dudley Charles, Michael G. S. Shashaty, Mark E. Mikkelsen, Jason D. Christie, Nuala J. Meyer

Published in: Critical Care | Issue 1/2016

Login to get access

Abstract

Background

Immunocompromised patients who develop sepsis while neutropenic are at high risk for morbidity and mortality; however, it is unknown if neutropenic sepsis is associated with distinct clinical and biological characteristics.

Methods

We conducted a prospective cohort study of patients admitted to the medical intensive care unit of an academic medical center with severe sepsis. Patients were followed for the development of acute respiratory distress syndrome (ARDS), acute kidney injury (AKI), and mortality. Plasma proteins, representing the host inflammatory response, anti-inflammatory response, and endothelial leak were measured in 30 % of subjects. Clinical characteristics and plasma protein concentrations of patients with neutropenia at enrollment were compared to patients without neutropenia.

Results

Of 797 subjects enrolled, 103 (13 %) were neutropenic at ICU admission. The neutropenic subjects were more often in shock, admitted from the hospital ward, had higher APACHE III scores, and more likely bacteremic. Neutropenia was an independent risk factor for AKI (RR 1.28; 95 % CI 1.04, 1.57; p = 0.03), but not ARDS (RR 0.90; 95 % CI 0.70, 1.17; p = 0.42) or 30-day mortality (RR 1.05; 95 % CI 0.85, 1.31; p = 0.65). Neutropenic subjects had higher plasma interleukin (IL)-6 (457 vs. 249 pg/ml; p = 0.03), IL-8 (581 vs. 94 pg/ml; p <0.001), and granulocyte colony-stimulating factor (G-CSF) (3624 vs. 99 pg/ml; p <0.001). Angiopoietin-2 and IL-1 receptor antagonist concentrations did not differ between groups.

Conclusions

Neutropenic sepsis is associated with a higher AKI risk and concentrations of inflammatory mediators IL-6, IL-8, and G-CSF relative to non-neutropenic patients. These differences may have implications for future therapies targeting neutropenic sepsis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348(16):1546–54.CrossRefPubMed Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348(16):1546–54.CrossRefPubMed
2.
go back to reference Gaieski DF, Edwards JM, Kallan MJ, Carr BG. Benchmarking the incidence and mortality of severe sepsis in the United States. Crit Care Med. 2013;41(5):1167–74.CrossRefPubMed Gaieski DF, Edwards JM, Kallan MJ, Carr BG. Benchmarking the incidence and mortality of severe sepsis in the United States. Crit Care Med. 2013;41(5):1167–74.CrossRefPubMed
3.
go back to reference Opal SM, Laterre PF, Francois B, LaRosa SP, Angus DC, Mira JP, et al. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial. JAMA. 2013;309(11):1154–62.CrossRefPubMed Opal SM, Laterre PF, Francois B, LaRosa SP, Angus DC, Mira JP, et al. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial. JAMA. 2013;309(11):1154–62.CrossRefPubMed
4.
go back to reference Ranieri VM, Thompson BT, Barie PS, Dhainaut J-F, Douglas IS, Finfer S, et al. Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med. 2012;366(22):2055–64.CrossRefPubMed Ranieri VM, Thompson BT, Barie PS, Dhainaut J-F, Douglas IS, Finfer S, et al. Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med. 2012;366(22):2055–64.CrossRefPubMed
5.
go back to reference 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(7):1303–10.CrossRefPubMed 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(7):1303–10.CrossRefPubMed
6.
go back to reference Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302(21):2323–9.CrossRefPubMed Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302(21):2323–9.CrossRefPubMed
7.
go back to reference Silva E, Cavalcanti AB, Bugano DD, Janes JM, Vallet B, Beale R, et al. Do established prognostic factors explain the different mortality rates in ICU septic patients around the world? Minerva Anestesiol. 2012;78(11):1215–25.PubMed Silva E, Cavalcanti AB, Bugano DD, Janes JM, Vallet B, Beale R, et al. Do established prognostic factors explain the different mortality rates in ICU septic patients around the world? Minerva Anestesiol. 2012;78(11):1215–25.PubMed
8.
go back to reference Tolsma V, Schwebel C, Azoulay E, Darmon M, Souweine B, Vesin A, et al. Sepsis severe or septic shock: outcome according to immune status and immunodeficiency profile. Chest. 2014;146(5):1205–13.CrossRefPubMed Tolsma V, Schwebel C, Azoulay E, Darmon M, Souweine B, Vesin A, et al. Sepsis severe or septic shock: outcome according to immune status and immunodeficiency profile. Chest. 2014;146(5):1205–13.CrossRefPubMed
9.
go back to reference Tate RM, Repine JE. Neutrophils and the adult respiratory distress syndrome. Am Rev Respir Dis. 1983;128(3):552–9.CrossRefPubMed Tate RM, Repine JE. Neutrophils and the adult respiratory distress syndrome. Am Rev Respir Dis. 1983;128(3):552–9.CrossRefPubMed
10.
go back to reference Brown KA, Brain SD, Pearson JD, Edgeworth JD, Lewis SM, Treacher DF. Neutrophils in development of multiple organ failure in sepsis. Lancet. 2006;368(9530):157–69.CrossRefPubMed Brown KA, Brain SD, Pearson JD, Edgeworth JD, Lewis SM, Treacher DF. Neutrophils in development of multiple organ failure in sepsis. Lancet. 2006;368(9530):157–69.CrossRefPubMed
11.
go back to reference Casey LC, Balk RA, Bone RC. Plasma cytokine and endotoxin levels correlate with survival in patients with the sepsis syndrome. Ann Intern Med. 1993;119(8):771–8.CrossRefPubMed Casey LC, Balk RA, Bone RC. Plasma cytokine and endotoxin levels correlate with survival in patients with the sepsis syndrome. Ann Intern Med. 1993;119(8):771–8.CrossRefPubMed
12.
go back to reference 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(3):405–12.CrossRefPubMed 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(3):405–12.CrossRefPubMed
13.
go back to reference Pettila 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(9):1220–5.CrossRefPubMed Pettila 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(9):1220–5.CrossRefPubMed
14.
go back to reference Mei J, Liu Y, Dai N, Hoffmann C, Hudock KM, Zhang P, et al. Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J Clin Investig. 2012;122(3):974–86.CrossRefPubMedPubMedCentral Mei J, Liu Y, Dai N, Hoffmann C, Hudock KM, Zhang P, et al. Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J Clin Investig. 2012;122(3):974–86.CrossRefPubMedPubMedCentral
15.
go back to reference Lloyd AR, Biragyn A, Johnston JA, Taub DD, Xu L, Michiel D, et al. Granulocyte-colony stimulating factor and lipopolysaccharide regulate the expression of interleukin 8 receptors on polymorphonuclear leukocytes. J Biol Chem. 1995;270(47):28188–92.CrossRefPubMed Lloyd AR, Biragyn A, Johnston JA, Taub DD, Xu L, Michiel D, et al. Granulocyte-colony stimulating factor and lipopolysaccharide regulate the expression of interleukin 8 receptors on polymorphonuclear leukocytes. J Biol Chem. 1995;270(47):28188–92.CrossRefPubMed
16.
go back to reference Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277(5322):55–60.CrossRefPubMed Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277(5322):55–60.CrossRefPubMed
17.
go back to reference Calfee CS, Gallagher D, Abbott J, Thompson BT, Matthay MA. Plasma angiopoietin-2 in clinical acute lung injury: prognostic and pathogenetic significance. Crit Care Med. 2012;40(6):1731–7.CrossRefPubMedPubMedCentral Calfee CS, Gallagher D, Abbott J, Thompson BT, Matthay MA. Plasma angiopoietin-2 in clinical acute lung injury: prognostic and pathogenetic significance. Crit Care Med. 2012;40(6):1731–7.CrossRefPubMedPubMedCentral
18.
go back to reference 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(11):3034–41.CrossRefPubMedPubMedCentral 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(11):3034–41.CrossRefPubMedPubMedCentral
19.
go back to reference Meyer NJ, Li M, Feng R, Bradfield J, Gallop R, Bellamy S, et al. ANGPT2 genetic variant is associated with trauma-associated acute lung injury and altered plasma angiopoietin-2 isoform ratio. Am J Respir Crit Care Med. 2011;183(10):1344–53.CrossRefPubMedPubMedCentral Meyer NJ, Li M, Feng R, Bradfield J, Gallop R, Bellamy S, et al. ANGPT2 genetic variant is associated with trauma-associated acute lung injury and altered plasma angiopoietin-2 isoform ratio. Am J Respir Crit Care Med. 2011;183(10):1344–53.CrossRefPubMedPubMedCentral
20.
go back to reference van Deuren M, van der Ven-Jongekrijg J, Vannier E, van Dalen R, Pesman G, Bartelink AK, et al. The pattern of interleukin-1beta (IL-1beta) and its modulating agents IL-1 receptor antagonist and IL-1 soluble receptor type II in acute meningococcal infections. Blood. 1997;90(3):1101–8.PubMed van Deuren M, van der Ven-Jongekrijg J, Vannier E, van Dalen R, Pesman G, Bartelink AK, et al. The pattern of interleukin-1beta (IL-1beta) and its modulating agents IL-1 receptor antagonist and IL-1 soluble receptor type II in acute meningococcal infections. Blood. 1997;90(3):1101–8.PubMed
21.
go back to reference Meyer NJ, Feng R, Li M, Zhao Y, Sheu CC, Tejera P, et al. IL1RN coding variant is associated with lower risk of acute respiratory distress syndrome and increased plasma IL-1 receptor antagonist. Am J Respir Crit Care Med. 2013;187(9):950–9.CrossRefPubMedPubMedCentral Meyer NJ, Feng R, Li M, Zhao Y, Sheu CC, Tejera P, et al. IL1RN coding variant is associated with lower risk of acute respiratory distress syndrome and increased plasma IL-1 receptor antagonist. Am J Respir Crit Care Med. 2013;187(9):950–9.CrossRefPubMedPubMedCentral
22.
go back to reference Opal SM, Dellinger RP, Vincent JL, Masur H, Angus DC. The next generation of sepsis clinical trial designs: what is next after the demise of recombinant human activated protein C?*. Crit Care Med. 2014;42(7):1714–21.CrossRefPubMedPubMedCentral Opal SM, Dellinger RP, Vincent JL, Masur H, Angus DC. The next generation of sepsis clinical trial designs: what is next after the demise of recombinant human activated protein C?*. Crit Care Med. 2014;42(7):1714–21.CrossRefPubMedPubMedCentral
23.
go back to reference Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, et al. 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(6):864–74.CrossRef Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, et al. 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(6):864–74.CrossRef
24.
go back to reference Reilly JP, Meyer NJ, Shashaty MG, Feng R, Lanken PN, Gallop R, et al. ABO blood type A is associated with increased risk of ARDS in whites following both major trauma and severe sepsis. Chest. 2014;145(4):753–61.CrossRefPubMedPubMedCentral Reilly JP, Meyer NJ, Shashaty MG, Feng R, Lanken PN, Gallop R, et al. ABO blood type A is associated with increased risk of ARDS in whites following both major trauma and severe sepsis. Chest. 2014;145(4):753–61.CrossRefPubMedPubMedCentral
25.
go back to reference Hsieh MM, Everhart JE, Byrd-Holt DD, Tisdale JF, Rodgers GP. Prevalence of neutropenia in the U.S. population: age, sex, smoking status, and ethnic differences. Ann Intern Med. 2007;146(7):486–92.CrossRefPubMed Hsieh MM, Everhart JE, Byrd-Holt DD, Tisdale JF, Rodgers GP. Prevalence of neutropenia in the U.S. population: age, sex, smoking status, and ethnic differences. Ann Intern Med. 2007;146(7):486–92.CrossRefPubMed
26.
go back to reference Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA. 2012;307(23):2526–33.PubMed Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA. 2012;307(23):2526–33.PubMed
27.
go back to reference Mehta R, Kellum J, Shah S, Molitoris B, Ronco C, Warnock D, et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Critical Care. 2007;11(2):R31.CrossRefPubMedPubMedCentral Mehta R, Kellum J, Shah S, Molitoris B, Ronco C, Warnock D, et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Critical Care. 2007;11(2):R31.CrossRefPubMedPubMedCentral
28.
go back to reference Schroder JM, Mrowietz U, Morita E, Christophers E. Purification and partial biochemical characterization of a human monocyte-derived, neutrophil-activating peptide that lacks interleukin 1 activity. J Immunol. 1987;139(10):3474–83.PubMed Schroder JM, Mrowietz U, Morita E, Christophers E. Purification and partial biochemical characterization of a human monocyte-derived, neutrophil-activating peptide that lacks interleukin 1 activity. J Immunol. 1987;139(10):3474–83.PubMed
29.
go back to reference Semerad CL, Liu F, Gregory AD, Stumpf K, Link DC. G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood. Immunity. 2002;17(4):413–23.CrossRefPubMed Semerad CL, Liu F, Gregory AD, Stumpf K, Link DC. G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood. Immunity. 2002;17(4):413–23.CrossRefPubMed
30.
go back to reference Schulte W, Bernhagen J, Bucala R. Cytokines in sepsis: potent immunoregulators and potential therapeutic targets--an updated view. Mediat Inflamm. 2013;2013:165974.CrossRef Schulte W, Bernhagen J, Bucala R. Cytokines in sepsis: potent immunoregulators and potential therapeutic targets--an updated view. Mediat Inflamm. 2013;2013:165974.CrossRef
31.
go back to reference Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 1994;368(6469):339–42.CrossRefPubMed Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 1994;368(6469):339–42.CrossRefPubMed
32.
go back to reference Liu D, Huang P, Li X, Ge M, Luo G, Hei Z. Using inflammatory and oxidative biomarkers in urine to predict early acute kidney injury in patients undergoing liver transplantation. Biomarkers. 2014;19(5):424–9.CrossRefPubMed Liu D, Huang P, Li X, Ge M, Luo G, Hei Z. Using inflammatory and oxidative biomarkers in urine to predict early acute kidney injury in patients undergoing liver transplantation. Biomarkers. 2014;19(5):424–9.CrossRefPubMed
33.
go back to reference Liu KD, Glidden DV, Eisner MD, Parsons PE, Ware LB, Wheeler A, et al. Predictive and pathogenetic value of plasma biomarkers for acute kidney injury in patients with acute lung injury. Crit Care Med. 2007;35(12):2755–61.CrossRefPubMedPubMedCentral Liu KD, Glidden DV, Eisner MD, Parsons PE, Ware LB, Wheeler A, et al. Predictive and pathogenetic value of plasma biomarkers for acute kidney injury in patients with acute lung injury. Crit Care Med. 2007;35(12):2755–61.CrossRefPubMedPubMedCentral
34.
go back to reference Payen D, Lukaszewicz AC, Legrand M, Gayat E, Faivre V, Megarbane B, et al. A multicentre study of acute kidney injury in severe sepsis and septic shock: association with inflammatory phenotype and HLA genotype. PloS One. 2012;7(6), e35838.CrossRefPubMedPubMedCentral Payen D, Lukaszewicz AC, Legrand M, Gayat E, Faivre V, Megarbane B, et al. A multicentre study of acute kidney injury in severe sepsis and septic shock: association with inflammatory phenotype and HLA genotype. PloS One. 2012;7(6), e35838.CrossRefPubMedPubMedCentral
35.
go back to reference Kielar ML, John R, Bennett M, Richardson JA, Shelton JM, Chen L, et al. Maladaptive role of IL-6 in ischemic acute renal failure. J Am Soc Nephrol. 2005;16(11):3315–25.CrossRefPubMed Kielar ML, John R, Bennett M, Richardson JA, Shelton JM, Chen L, et al. Maladaptive role of IL-6 in ischemic acute renal failure. J Am Soc Nephrol. 2005;16(11):3315–25.CrossRefPubMed
36.
go back to reference Nechemia-Arbely Y, Barkan D, Pizov G, Shriki A, Rose-John S, Galun E, et al. IL-6/IL-6R axis plays a critical role in acute kidney injury. J Am Soc Nephrol. 2008;19(6):1106–15.CrossRefPubMedPubMedCentral Nechemia-Arbely Y, Barkan D, Pizov G, Shriki A, Rose-John S, Galun E, et al. IL-6/IL-6R axis plays a critical role in acute kidney injury. J Am Soc Nephrol. 2008;19(6):1106–15.CrossRefPubMedPubMedCentral
37.
go back to reference Ranganathan P, Jayakumar C, Manicassamy S, Ramesh G. CXCR2 knockout mice are protected against DSS-colitis-induced acute kidney injury and inflammation. Am J Physiol Renal Physiol. 2013;305(10):F1422–7.CrossRefPubMedPubMedCentral Ranganathan P, Jayakumar C, Manicassamy S, Ramesh G. CXCR2 knockout mice are protected against DSS-colitis-induced acute kidney injury and inflammation. Am J Physiol Renal Physiol. 2013;305(10):F1422–7.CrossRefPubMedPubMedCentral
38.
go back to reference Kangelaris KN, Prakash A, Liu KD, Aouizerat B, Woodruff PG, Erle DJ, et al. Increased expression of neutrophil-related genes in patients with early sepsis-induced ARDS. Am J Physiol Lung Cell Mol Physiol. 2015;308(11):L1102–13.CrossRefPubMedPubMedCentral Kangelaris KN, Prakash A, Liu KD, Aouizerat B, Woodruff PG, Erle DJ, et al. Increased expression of neutrophil-related genes in patients with early sepsis-induced ARDS. Am J Physiol Lung Cell Mol Physiol. 2015;308(11):L1102–13.CrossRefPubMedPubMedCentral
39.
go back to reference Ognibene FP, Martin SE, Parker MM, Schlesinger T, Roach P, Burch C, et al. Adult respiratory distress syndrome in patients with severe neutropenia. N Engl J Med. 1986;315(9):547–51.CrossRefPubMed Ognibene FP, Martin SE, Parker MM, Schlesinger T, Roach P, Burch C, et al. Adult respiratory distress syndrome in patients with severe neutropenia. N Engl J Med. 1986;315(9):547–51.CrossRefPubMed
40.
go back to reference Mokart D, Guery BP, Bouabdallah R, Martin C, Blache JL, Arnoulet C, et al. Deactivation of alveolar macrophages in septic neutropenic ARDS. Chest. 2003;124(2):644–52.CrossRefPubMed Mokart D, Guery BP, Bouabdallah R, Martin C, Blache JL, Arnoulet C, et al. Deactivation of alveolar macrophages in septic neutropenic ARDS. Chest. 2003;124(2):644–52.CrossRefPubMed
41.
go back to reference Mokart D, Kipnis E, Guerre-Berthelot P, Vey N, Capo C, Sannini A, et al. Monocyte deactivation in neutropenic acute respiratory distress syndrome patients treated with granulocyte colony-stimulating factor. Crit Care. 2008;12(1):R17.CrossRefPubMedPubMedCentral Mokart D, Kipnis E, Guerre-Berthelot P, Vey N, Capo C, Sannini A, et al. Monocyte deactivation in neutropenic acute respiratory distress syndrome patients treated with granulocyte colony-stimulating factor. Crit Care. 2008;12(1):R17.CrossRefPubMedPubMedCentral
42.
go back to reference Azoulay E, Darmon M, Delclaux C, Fieux F, Bornstain C, Moreau D, et al. Deterioration of previous acute lung injury during neutropenia recovery. Crit Care Med. 2002;30(4):781–6.CrossRefPubMed Azoulay E, Darmon M, Delclaux C, Fieux F, Bornstain C, Moreau D, et al. Deterioration of previous acute lung injury during neutropenia recovery. Crit Care Med. 2002;30(4):781–6.CrossRefPubMed
43.
go back to reference Rhee CK, Kang JY, Kim YH, Kim JW, Yoon HK, Kim SC, et al. Risk factors for acute respiratory distress syndrome during neutropenia recovery in patients with hematologic malignancies. Crit Care. 2009;13(6):R173.CrossRefPubMedPubMedCentral Rhee CK, Kang JY, Kim YH, Kim JW, Yoon HK, Kim SC, et al. Risk factors for acute respiratory distress syndrome during neutropenia recovery in patients with hematologic malignancies. Crit Care. 2009;13(6):R173.CrossRefPubMedPubMedCentral
44.
go back to reference Rinaldo JE, Borovetz H. Deterioration of oxygenation and abnormal lung microvascular permeability during resolution of leukopenia in patients with diffuse lung injury. Am Rev Respir Dis. 1985;131(4):579–83.PubMed Rinaldo JE, Borovetz H. Deterioration of oxygenation and abnormal lung microvascular permeability during resolution of leukopenia in patients with diffuse lung injury. Am Rev Respir Dis. 1985;131(4):579–83.PubMed
45.
go back to reference Karlin L, Darmon M, Thiery G, Ciroldi M, de Miranda S, Lefebvre A, et al. Respiratory status deterioration during G-CSF-induced neutropenia recovery. Bone Marrow Transplant. 2005;36(3):245–50.CrossRefPubMed Karlin L, Darmon M, Thiery G, Ciroldi M, de Miranda S, Lefebvre A, et al. Respiratory status deterioration during G-CSF-induced neutropenia recovery. Bone Marrow Transplant. 2005;36(3):245–50.CrossRefPubMed
46.
go back to reference Terashima T, Klut ME, English D, Hards J, Hogg JC, van Eeden SF. Cigarette smoking causes sequestration of polymorphonuclear leukocytes released from the bone marrow in lung microvessels. Am J Respir Cell Mol Biol. 1999;20(1):171–7.CrossRefPubMed Terashima T, Klut ME, English D, Hards J, Hogg JC, van Eeden SF. Cigarette smoking causes sequestration of polymorphonuclear leukocytes released from the bone marrow in lung microvessels. Am J Respir Cell Mol Biol. 1999;20(1):171–7.CrossRefPubMed
47.
go back to reference Mikacenic C, Hahn WO, Price BL, Harju-Baker S, Katz R, Kain KC, et al. Biomarkers of endothelial activation are associated with poor outcome in critical illness. PloS One. 2015;10(10), e0141251.CrossRefPubMedPubMedCentral Mikacenic C, Hahn WO, Price BL, Harju-Baker S, Katz R, Kain KC, et al. Biomarkers of endothelial activation are associated with poor outcome in critical illness. PloS One. 2015;10(10), e0141251.CrossRefPubMedPubMedCentral
Metadata
Title
Neutropenic sepsis is associated with distinct clinical and biological characteristics: a cohort study of severe sepsis
Authors
John P. Reilly
Brian J. Anderson
Kristin M. Hudock
Thomas G. Dunn
Altaf Kazi
Anna Tommasini
Dudley Charles
Michael G. S. Shashaty
Mark E. Mikkelsen
Jason D. Christie
Nuala J. Meyer
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Critical Care / Issue 1/2016
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/s13054-016-1398-y

Other articles of this Issue 1/2016

Critical Care 1/2016 Go to the issue