Skip to main content
Top
Published in: Critical Care 2/2011

Open Access 01-04-2011 | Research

Virus-associated hemophagocytic syndrome as a major contributor to death in patients with 2009 influenza A (H1N1) infection

Authors: Gernot Beutel, Olaf Wiesner, Matthias Eder, Carsten Hafer, Andrea S Schneider, Jan T Kielstein, Christian Kühn, Albert Heim, Tina Ganzenmüller, Hans-Heinrich Kreipe, Axel Haverich, Andreas Tecklenburg, Arnold Ganser, Tobias Welte, Marius M Hoeper

Published in: Critical Care | Issue 2/2011

Login to get access

Abstract

Introduction

Virus-associated hemophagocytic syndrome (VAHS) is a severe complication of various viral infections often resulting in multiorgan failure and death. The purpose of this study was to describe baseline characteristics, development of VAHS, related treatments and associated mortality rate of consecutive critically ill patients with confirmed 2009 influenza A (H1N1) infection and respiratory failure.

Methods

We conducted a prospective observational study of 25 critically ill patients with 2009 influenza A (H1N1) infection at a single-center intensive care unit in Germany between 5 October 2009 and 4 January 2010. Demographic data, comorbidities, diagnosis of VAHS, illness progression, treatments and survival data were collected. The primary outcome measure was the development of VAHS and related mortality. Secondary outcome variables included duration of mechanical ventilation, support of extracorporeal membrane oxygenation and duration of viral shedding.

Results

VAHS developed in 9 (36%) of 25 critically ill patients with confirmed 2009 influenza A (H1N1) infection, and 8 (89%) of them died. In contrast, the mortality rate in the remaining 16 patients without VAHS was 25% (P = 0.004 for the survival difference in patients with or without VAHS by log-rank analysis). The patients were relatively young (median age, 45 years; interquartile range (IQR), 35 to 56 years of age); however, 18 patients (72%) presented with one or more risk factors for a severe course of illness. All 25 patients received mechanical ventilation for severe acute respiratory distress syndrome and refractory hypoxemia, with a median duration of mechanical ventilation of 19 days (IQR, 13 to 26 days). An additional 17 patients (68%) required extracorporeal membrane oxygenation for a median of 10 days (IQR, 6 to 19 days).

Conclusions

The findings of this study raise the possibility that VAHS may be a frequent complication of severe 2009 influenza A (H1N1) infection and represents an important contributor to multiorgan failure and death.
Appendix
Available only for authorised users
Literature
1.
go back to reference Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ, Gubareva LV, Xu X, Bridges CB, Uyeki TM: Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009, 360: 2605-2615. 10.1056/NEJMoa0903810CrossRef Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ, Gubareva LV, Xu X, Bridges CB, Uyeki TM: Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009, 360: 2605-2615. 10.1056/NEJMoa0903810CrossRef
2.
go back to reference Zarocostas J: World Health Organization declares A (H1N1) influenza pandemic. BMJ 2009, 338: b2425. 10.1136/bmj.b2425CrossRefPubMed Zarocostas J: World Health Organization declares A (H1N1) influenza pandemic. BMJ 2009, 338: b2425. 10.1136/bmj.b2425CrossRefPubMed
3.
go back to reference Centers for Disease Control and Prevention (CDC): Update: novel influenza A (H1N1) virus infections-worldwide, May 6, 2009. MMWR Morb Mortal Wkly Rep 2009, 58: 453-458. Centers for Disease Control and Prevention (CDC): Update: novel influenza A (H1N1) virus infections-worldwide, May 6, 2009. MMWR Morb Mortal Wkly Rep 2009, 58: 453-458.
4.
go back to reference Chowell G, Bertozzi SM, Colchero MA, Lopez-Gatell H, Alpuche-Aranda C, Hernandez M, Miller MA: Severe respiratory disease concurrent with the circulation of H1N1 influenza. N Engl J Med 2009, 361: 674-679. 10.1056/NEJMoa0904023CrossRefPubMed Chowell G, Bertozzi SM, Colchero MA, Lopez-Gatell H, Alpuche-Aranda C, Hernandez M, Miller MA: Severe respiratory disease concurrent with the circulation of H1N1 influenza. N Engl J Med 2009, 361: 674-679. 10.1056/NEJMoa0904023CrossRefPubMed
5.
go back to reference Kumar A, Zarychanski R, Pinto R, Cook DJ, Marshall J, Lacroix J, Stelfox T, Bagshaw S, Choong K, Lamontagne F, Turgeon AF, Lapinsky S, Ahern SP, Smith O, Siddiqui F, Jouvet P, Khwaja K, McIntyre L, Menon K, Hutchison J, Hornstein D, Joffe A, Lauzier F, Singh J, Karachi T, Wiebe K, Olafson K, Ramsey C, Sharma S, Dodek P: Critically ill patients with 2009 influenza A (H1N1) infection in Canada. JAMA 2009, 302: 1872-1879. 10.1001/jama.2009.1496CrossRefPubMed Kumar A, Zarychanski R, Pinto R, Cook DJ, Marshall J, Lacroix J, Stelfox T, Bagshaw S, Choong K, Lamontagne F, Turgeon AF, Lapinsky S, Ahern SP, Smith O, Siddiqui F, Jouvet P, Khwaja K, McIntyre L, Menon K, Hutchison J, Hornstein D, Joffe A, Lauzier F, Singh J, Karachi T, Wiebe K, Olafson K, Ramsey C, Sharma S, Dodek P: Critically ill patients with 2009 influenza A (H1N1) infection in Canada. JAMA 2009, 302: 1872-1879. 10.1001/jama.2009.1496CrossRefPubMed
6.
go back to reference Perez-Padilla R, de la Rosa-Zamboni D, Ponce de Leon S, Hernandez M, Quiñones-Falconi F, Bautista E, Ramirez-Venegas A, Rojas-Serrano J, Ormsby CE, Corrales A, Higuera A, Mondragon E, Cordova-Villalobos JA, INER Working Group on Influenza: Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N Engl J Med 2009, 361: 680-689. 10.1056/NEJMoa0904252CrossRefPubMed Perez-Padilla R, de la Rosa-Zamboni D, Ponce de Leon S, Hernandez M, Quiñones-Falconi F, Bautista E, Ramirez-Venegas A, Rojas-Serrano J, Ormsby CE, Corrales A, Higuera A, Mondragon E, Cordova-Villalobos JA, INER Working Group on Influenza: Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N Engl J Med 2009, 361: 680-689. 10.1056/NEJMoa0904252CrossRefPubMed
7.
go back to reference Louie JK, Acosta M, Winter K, Jean C, Gavali S, Schechter R, Vugia D, Harriman K, Matyas B, Glaser CA, Samuel MC, Rosenberg J, Talarico J, Hatch D, California Pandemic (H1N1) Working Group: Factors associated with death or hospitalization due to pandemic 2009 influenza A (H1N1) infection in California. JAMA 2009, 302: 1896-1902. 10.1001/jama.2009.1583CrossRefPubMed Louie JK, Acosta M, Winter K, Jean C, Gavali S, Schechter R, Vugia D, Harriman K, Matyas B, Glaser CA, Samuel MC, Rosenberg J, Talarico J, Hatch D, California Pandemic (H1N1) Working Group: Factors associated with death or hospitalization due to pandemic 2009 influenza A (H1N1) infection in California. JAMA 2009, 302: 1896-1902. 10.1001/jama.2009.1583CrossRefPubMed
8.
go back to reference To KF, Chan PK, Chan KF, Lee WK, Lam WY, Wong KF, Tang NL, Tsang DN, Sung RY, Buckley TA, Tam JS, Cheng AF: Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 2001, 63: 242-246. 10.1002/1096-9071(200103)63:3<242::AID-JMV1007>3.0.CO;2-NCrossRefPubMed To KF, Chan PK, Chan KF, Lee WK, Lam WY, Wong KF, Tang NL, Tsang DN, Sung RY, Buckley TA, Tam JS, Cheng AF: Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 2001, 63: 242-246. 10.1002/1096-9071(200103)63:3<242::AID-JMV1007>3.0.CO;2-NCrossRefPubMed
9.
go back to reference Henter JI, Chow CB, Leung CW, Lau YL: Cytotoxic therapy for severe avian influenza A (H5N1) infection. Lancet 2006, 367: 870-873. 10.1016/S0140-6736(06)68232-9CrossRefPubMed Henter JI, Chow CB, Leung CW, Lau YL: Cytotoxic therapy for severe avian influenza A (H5N1) infection. Lancet 2006, 367: 870-873. 10.1016/S0140-6736(06)68232-9CrossRefPubMed
10.
go back to reference Henter JI, Palmkvist-Kaijser K, Holzgraefe B, Bryceson YT, Palmer K: Cytotoxic therapy for severe swine flu A/H1N1. Lancet 2010, 376: 2116. 10.1016/S0140-6736(10)61345-1CrossRefPubMed Henter JI, Palmkvist-Kaijser K, Holzgraefe B, Bryceson YT, Palmer K: Cytotoxic therapy for severe swine flu A/H1N1. Lancet 2010, 376: 2116. 10.1016/S0140-6736(10)61345-1CrossRefPubMed
11.
go back to reference Potter MN, Foot AB, Oakhill A: Influenza A and the virus associated haemophagocytic syndrome: cluster of three cases in children with acute leukaemia. J Clin Pathol 1991, 44: 297-299. 10.1136/jcp.44.4.297PubMedCentralCrossRefPubMed Potter MN, Foot AB, Oakhill A: Influenza A and the virus associated haemophagocytic syndrome: cluster of three cases in children with acute leukaemia. J Clin Pathol 1991, 44: 297-299. 10.1136/jcp.44.4.297PubMedCentralCrossRefPubMed
12.
go back to reference Henter JI, Elinder G, Soder O, Hansson M, Andersson B, Andersson U: Hypercytokinemia in familial hemophagocytic lymphohistiocytosis. Blood 1991, 78: 2918-2922.PubMed Henter JI, Elinder G, Soder O, Hansson M, Andersson B, Andersson U: Hypercytokinemia in familial hemophagocytic lymphohistiocytosis. Blood 1991, 78: 2918-2922.PubMed
13.
go back to reference Osugi Y, Hara J, Tagawa S, Takai K, Hosoi G, Matsuda Y, Ohta H, Fujisaki H, Kobayashi M, Sakata N, Kawa-Ha K, Okada S, Tawa A: Cytokine production regulating Th1 and Th2 cytokines in hemophagocytic lymphohistiocytosis. Blood 1997, 89: 4100-4103.PubMed Osugi Y, Hara J, Tagawa S, Takai K, Hosoi G, Matsuda Y, Ohta H, Fujisaki H, Kobayashi M, Sakata N, Kawa-Ha K, Okada S, Tawa A: Cytokine production regulating Th1 and Th2 cytokines in hemophagocytic lymphohistiocytosis. Blood 1997, 89: 4100-4103.PubMed
14.
go back to reference Arico M, Danesino C, Pende D, Moretta L: Pathogenesis of haemophagocytic lymphohistiocytosis. Br J Haematol 2001, 114: 761-769. 10.1046/j.1365-2141.2001.02936.xCrossRefPubMed Arico M, Danesino C, Pende D, Moretta L: Pathogenesis of haemophagocytic lymphohistiocytosis. Br J Haematol 2001, 114: 761-769. 10.1046/j.1365-2141.2001.02936.xCrossRefPubMed
15.
go back to reference Komp DM, McNamara J, Buckley P: Elevated soluble interleukin-2 receptor in childhood hemophagocytic histiocytic syndromes. Blood 1989, 73: 2128-2132.PubMed Komp DM, McNamara J, Buckley P: Elevated soluble interleukin-2 receptor in childhood hemophagocytic histiocytic syndromes. Blood 1989, 73: 2128-2132.PubMed
16.
go back to reference Tang YM, Xu XJ, Song H, Yang SL, Shi SW, Wei J, Pan BH, Zhao FY, Liao C, Luo CF: Early diagnostic and prognostic significance of a specific Th1/Th2 cytokine pattern in children with haemophagocytic syndrome. Br J Haematol 2008, 143: 84-91. 10.1111/j.1365-2141.2008.07298.xCrossRefPubMed Tang YM, Xu XJ, Song H, Yang SL, Shi SW, Wei J, Pan BH, Zhao FY, Liao C, Luo CF: Early diagnostic and prognostic significance of a specific Th1/Th2 cytokine pattern in children with haemophagocytic syndrome. Br J Haematol 2008, 143: 84-91. 10.1111/j.1365-2141.2008.07298.xCrossRefPubMed
17.
go back to reference Panning M, Eickmann M, Landt O, Monazahian M, Olschläger S, Baumgarte S, Reischl U, Wenzel JJ, Niller HH, Günther S, Hollmann B, Huzly D, Drexler JF, Helmer A, Becker S, Matz B, Eis-Hübinger A, Drosten C: Detection of influenza A(H1N1)v virus by real-time RT-PCR. Euro Surveill 2009, 14: 19329.PubMed Panning M, Eickmann M, Landt O, Monazahian M, Olschläger S, Baumgarte S, Reischl U, Wenzel JJ, Niller HH, Günther S, Hollmann B, Huzly D, Drexler JF, Helmer A, Becker S, Matz B, Eis-Hübinger A, Drosten C: Detection of influenza A(H1N1)v virus by real-time RT-PCR. Euro Surveill 2009, 14: 19329.PubMed
18.
go back to reference Filipovich AH: Hemophagocytic lymphohistiocytosis (HLH) and related disorders. Hematology Am Soc Hematol Educ Program 2009, 127-131. Filipovich AH: Hemophagocytic lymphohistiocytosis (HLH) and related disorders. Hematology Am Soc Hematol Educ Program 2009, 127-131.
19.
go back to reference Knaus WA, Draper EA, Wagner DP, Zimmerman JE: APACHE II: a severity of disease classification system. Crit Care Med 1985, 13: 818-829. 10.1097/00003246-198510000-00009CrossRefPubMed Knaus WA, Draper EA, Wagner DP, Zimmerman JE: APACHE II: a severity of disease classification system. Crit Care Med 1985, 13: 818-829. 10.1097/00003246-198510000-00009CrossRefPubMed
20.
go back to reference Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça A, Bruining H, Reinhart CK, Suter PM, Thijs LG: 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. 10.1007/BF01709751CrossRefPubMed Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça A, Bruining H, Reinhart CK, Suter PM, Thijs LG: 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. 10.1007/BF01709751CrossRefPubMed
21.
go back to reference Kidd IM, Down J, Nastouli E, Shulman R, Grant PR, Howell DCJ, Singer M: H1N1 pneumonitis treated with intravenous zanamivir. Lancet 2009, 374: 1036-1036. 10.1016/S0140-6736(09)61528-2CrossRefPubMed Kidd IM, Down J, Nastouli E, Shulman R, Grant PR, Howell DCJ, Singer M: H1N1 pneumonitis treated with intravenous zanamivir. Lancet 2009, 374: 1036-1036. 10.1016/S0140-6736(09)61528-2CrossRefPubMed
22.
go back to reference Henter JI, Samuelsson-Horne A, Aricò M, Egeler RM, Elinder G, Filipovich AH, Gadner H, Imashuku S, Komp D, Ladisch S, Webb D, Janka G, Histocyte Society: Treatment of hemophagocytic lymphohistiocytosis with HLH-94 immunochemotherapy and bone marrow transplantation. Blood 2002, 100: 2367-2373. 10.1182/blood-2002-01-0172CrossRefPubMed Henter JI, Samuelsson-Horne A, Aricò M, Egeler RM, Elinder G, Filipovich AH, Gadner H, Imashuku S, Komp D, Ladisch S, Webb D, Janka G, Histocyte Society: Treatment of hemophagocytic lymphohistiocytosis with HLH-94 immunochemotherapy and bone marrow transplantation. Blood 2002, 100: 2367-2373. 10.1182/blood-2002-01-0172CrossRefPubMed
23.
go back to reference Janka GE, Schneider EM: Modern management of children with haemophagocytic lymphohistiocytosis. Br J Haematol 2004, 124: 4-14. 10.1046/j.1365-2141.2003.04726.xCrossRefPubMed Janka GE, Schneider EM: Modern management of children with haemophagocytic lymphohistiocytosis. Br J Haematol 2004, 124: 4-14. 10.1046/j.1365-2141.2003.04726.xCrossRefPubMed
24.
go back to reference Imashuku S, Teramura T, Tauchi H, Ishida Y, Otoh Y, Sawada M, Tanaka H, Watanabe A, Tabata Y, Morimoto A, Hibi S, Henter JI: Longitudinal follow-up of patients with Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis. Haematologica 2004, 89: 183-188.PubMed Imashuku S, Teramura T, Tauchi H, Ishida Y, Otoh Y, Sawada M, Tanaka H, Watanabe A, Tabata Y, Morimoto A, Hibi S, Henter JI: Longitudinal follow-up of patients with Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis. Haematologica 2004, 89: 183-188.PubMed
25.
go back to reference Harms PW, Schmidt LA, Smith LB, Newton DW, Pletneva MA, Walters LL, Tomlins SA, Fisher-Hubbard A, Napolitano LM, Park PK, Blaivas M, Fantone J, Myers JL, Jentzen JM: Autopsy findings in eight patients with fatal H1N1 influenza. Am J Clin Pathol 2010, 134: 27-35. 10.1309/AJCP35KOZSAVNQZWCrossRefPubMed Harms PW, Schmidt LA, Smith LB, Newton DW, Pletneva MA, Walters LL, Tomlins SA, Fisher-Hubbard A, Napolitano LM, Park PK, Blaivas M, Fantone J, Myers JL, Jentzen JM: Autopsy findings in eight patients with fatal H1N1 influenza. Am J Clin Pathol 2010, 134: 27-35. 10.1309/AJCP35KOZSAVNQZWCrossRefPubMed
26.
go back to reference Soto-Abraham MV, Soriano-Rosas J, Diaz-Quinonez A, Silva-Pereyra J, Vazquez-Hernandez P, Torres-Lopez O, Roldan A, Cruz-Gordillo A, Alonso-Viveros P, Navarro-Reynoso F: Pathological changes associated with the 2009 H1N1 virus. N Engl J Med 2009, 361: 2001-2003. 10.1056/NEJMc0907171CrossRefPubMed Soto-Abraham MV, Soriano-Rosas J, Diaz-Quinonez A, Silva-Pereyra J, Vazquez-Hernandez P, Torres-Lopez O, Roldan A, Cruz-Gordillo A, Alonso-Viveros P, Navarro-Reynoso F: Pathological changes associated with the 2009 H1N1 virus. N Engl J Med 2009, 361: 2001-2003. 10.1056/NEJMc0907171CrossRefPubMed
27.
go back to reference Zheng Y, Yang Y, Zhao W, Wang H: Novel swine-origin influenza A (H1N1) virus-associated hemophagocytic syndrome: a first case report. Am J Trop Med Hyg 2010, 82: 743-745. 10.4269/ajtmh.2010.09-0666PubMedCentralCrossRefPubMed Zheng Y, Yang Y, Zhao W, Wang H: Novel swine-origin influenza A (H1N1) virus-associated hemophagocytic syndrome: a first case report. Am J Trop Med Hyg 2010, 82: 743-745. 10.4269/ajtmh.2010.09-0666PubMedCentralCrossRefPubMed
28.
go back to reference ANZIC Influenza Investigators, Webb SA, Pettilä V, Seppelt I, Bellomo R, Bailey M, Cooper DJ, Cretikos M, Davies AR, Finfer S, Harrigan PW, Hart GK, Howe B, Iredell JR, McArthur C, Mitchell I, Morrison S, Nichol AD, Paterson DL, Peake S, Richards B, Stephens D, Turner A, Yung M: Critical care services and 2009 H1N1 influenza in Australia and New Zealand. N Engl J Med 2009, 361: 1925-1934. 10.1056/NEJMoa0908481CrossRef ANZIC Influenza Investigators, Webb SA, Pettilä V, Seppelt I, Bellomo R, Bailey M, Cooper DJ, Cretikos M, Davies AR, Finfer S, Harrigan PW, Hart GK, Howe B, Iredell JR, McArthur C, Mitchell I, Morrison S, Nichol AD, Paterson DL, Peake S, Richards B, Stephens D, Turner A, Yung M: Critical care services and 2009 H1N1 influenza in Australia and New Zealand. N Engl J Med 2009, 361: 1925-1934. 10.1056/NEJMoa0908481CrossRef
29.
go back to reference Falagas ME, Vouloumanou EK, Baskouta E, Rafailidis PI, Polyzos K, Rello J: Treatment options for 2009 H1N1 influenza: evaluation of the published evidence. Int J Antimicrob Agents 2010, 35: 421-430. 10.1016/j.ijantimicag.2010.01.006CrossRefPubMed Falagas ME, Vouloumanou EK, Baskouta E, Rafailidis PI, Polyzos K, Rello J: Treatment options for 2009 H1N1 influenza: evaluation of the published evidence. Int J Antimicrob Agents 2010, 35: 421-430. 10.1016/j.ijantimicag.2010.01.006CrossRefPubMed
30.
go back to reference Hui DS, Lee N, Chan PK: Clinical management of pandemic 2009 influenza A(H1N1) infection. Chest 2010, 137: 916-925. 10.1378/chest.09-2344CrossRefPubMed Hui DS, Lee N, Chan PK: Clinical management of pandemic 2009 influenza A(H1N1) infection. Chest 2010, 137: 916-925. 10.1378/chest.09-2344CrossRefPubMed
31.
go back to reference Quispe-Laime AM, Bracco JD, Barberio PA, Campagne CG, Rolfo VE, Umberger R, Meduri GU: H1N1 influenza A virus-associated acute lung injury: response to combination oseltamivir and prolonged corticosteroid treatment. Intensive Care Med 2010, 36: 33-41. 10.1007/s00134-009-1727-6CrossRefPubMed Quispe-Laime AM, Bracco JD, Barberio PA, Campagne CG, Rolfo VE, Umberger R, Meduri GU: H1N1 influenza A virus-associated acute lung injury: response to combination oseltamivir and prolonged corticosteroid treatment. Intensive Care Med 2010, 36: 33-41. 10.1007/s00134-009-1727-6CrossRefPubMed
32.
go back to reference Confalonieri M, Cifaldi R, Dreas L, Viviani M, Biolo M, Gabrielli M: Methylprednisolone infusion for life-threatening H1N1-virus infection. Ther Adv Respir Dis 2010, 4: 233-237. 10.1177/1753465810376951CrossRefPubMed Confalonieri M, Cifaldi R, Dreas L, Viviani M, Biolo M, Gabrielli M: Methylprednisolone infusion for life-threatening H1N1-virus infection. Ther Adv Respir Dis 2010, 4: 233-237. 10.1177/1753465810376951CrossRefPubMed
33.
go back to reference Woo PC, Tung ET, Chan KH, Lau CC, Lau SK, Yuen KY: Cytokine profiles induced by the novel swine-origin influenza A/H1N1 virus: implications for treatment strategies. J Infect Dis 2010, 201: 346-353. 10.1086/649785CrossRefPubMed Woo PC, Tung ET, Chan KH, Lau CC, Lau SK, Yuen KY: Cytokine profiles induced by the novel swine-origin influenza A/H1N1 virus: implications for treatment strategies. J Infect Dis 2010, 201: 346-353. 10.1086/649785CrossRefPubMed
34.
go back to reference McILwain RB, Timpa JG, Kurundkar AR, Holt DW, Kelly DR, Hartman YE, Neel ML, Karnatak RK, Schelonka RL, Anantharamaiah GM, Killingsworth CR, Maheshwari A: Plasma concentrations of inflammatory cytokines rise rapidly during ECMO-related SIRS due to the release of preformed stores in the intestine. Lab Invest 2010, 90: 128-139. 10.1038/labinvest.2009.119PubMedCentralCrossRefPubMed McILwain RB, Timpa JG, Kurundkar AR, Holt DW, Kelly DR, Hartman YE, Neel ML, Karnatak RK, Schelonka RL, Anantharamaiah GM, Killingsworth CR, Maheshwari A: Plasma concentrations of inflammatory cytokines rise rapidly during ECMO-related SIRS due to the release of preformed stores in the intestine. Lab Invest 2010, 90: 128-139. 10.1038/labinvest.2009.119PubMedCentralCrossRefPubMed
35.
go back to reference Henter JI, Horne A, Aricó M, Egeler RM, Filipovich AH, Imashuku S, Ladisch S, McClain K, Webb D, Winiarski J, Janka G: HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 2007, 48: 124-131. 10.1002/pbc.21039CrossRefPubMed Henter JI, Horne A, Aricó M, Egeler RM, Filipovich AH, Imashuku S, Ladisch S, McClain K, Webb D, Winiarski J, Janka G: HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 2007, 48: 124-131. 10.1002/pbc.21039CrossRefPubMed
36.
go back to reference Imashuku S, Hibi S, Ohara T, Iwai A, Sako M, Kato M, Arakawa H, Sotomatsu M, Kataoka S, Asami K, Hasegawa D, Kosaka Y, Sano K, Igarashi N, Maruhashi K, Ichimi R, Kawasaki H, Maeda N, Tanizawa A, Arai K, Abe T, Hisakawa H, Miyashita H, Henter JI: Effective control of Epstein-Barr virus-related hemophagocytic lymphohistiocytosis with immunochemotherapy. Blood 1999, 93: 1869-1874.PubMed Imashuku S, Hibi S, Ohara T, Iwai A, Sako M, Kato M, Arakawa H, Sotomatsu M, Kataoka S, Asami K, Hasegawa D, Kosaka Y, Sano K, Igarashi N, Maruhashi K, Ichimi R, Kawasaki H, Maeda N, Tanizawa A, Arai K, Abe T, Hisakawa H, Miyashita H, Henter JI: Effective control of Epstein-Barr virus-related hemophagocytic lymphohistiocytosis with immunochemotherapy. Blood 1999, 93: 1869-1874.PubMed
37.
go back to reference Imashuku S, Kuriyama K, Teramura T, Ishii E, Kinugawa N, Kato M, Sako M, Hibi S: Requirement for etoposide in the treatment of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis. J Clin Oncol 2001, 19: 2665-2673.PubMed Imashuku S, Kuriyama K, Teramura T, Ishii E, Kinugawa N, Kato M, Sako M, Hibi S: Requirement for etoposide in the treatment of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis. J Clin Oncol 2001, 19: 2665-2673.PubMed
38.
go back to reference Imashuku S, Kuriyama K, Sakai R, Nakao Y, Masuda S, Yasuda N, Kawano F, Yakushijin K, Miyagawa A, Nakao T, Teramura T, Tabata Y, Morimoto A, Hibi S: Treatment of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis (EBV-HLH) in young adults: a report from the HLH Study Center. Med Pediatr Oncol 2003, 41: 103-109. 10.1002/mpo.10314CrossRefPubMed Imashuku S, Kuriyama K, Sakai R, Nakao Y, Masuda S, Yasuda N, Kawano F, Yakushijin K, Miyagawa A, Nakao T, Teramura T, Tabata Y, Morimoto A, Hibi S: Treatment of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis (EBV-HLH) in young adults: a report from the HLH Study Center. Med Pediatr Oncol 2003, 41: 103-109. 10.1002/mpo.10314CrossRefPubMed
Metadata
Title
Virus-associated hemophagocytic syndrome as a major contributor to death in patients with 2009 influenza A (H1N1) infection
Authors
Gernot Beutel
Olaf Wiesner
Matthias Eder
Carsten Hafer
Andrea S Schneider
Jan T Kielstein
Christian Kühn
Albert Heim
Tina Ganzenmüller
Hans-Heinrich Kreipe
Axel Haverich
Andreas Tecklenburg
Arnold Ganser
Tobias Welte
Marius M Hoeper
Publication date
01-04-2011
Publisher
BioMed Central
Published in
Critical Care / Issue 2/2011
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/cc10073

Other articles of this Issue 2/2011

Critical Care 2/2011 Go to the issue