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Acute hypoxemic respiratory failure in immunocompromised patients: the Efraim multinational prospective cohort study

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Abstract

Background

In immunocompromised patients with acute hypoxemic respiratory failure (ARF), initial management aims primarily to avoid invasive mechanical ventilation (IMV).

Methods

To assess the impact of initial management on IMV and mortality rates, we performed a multinational observational prospective cohort study in 16 countries (68 centers).

Results

A total of 1611 patients were enrolled (hematological malignancies 51.9%, solid tumors 35.2%, systemic diseases 17.3%, and solid organ transplantation 8.8%). The main ARF etiologies were bacterial (29.5%), viral (15.4%), and fungal infections (14.7%), or undetermined (13.2%). On admission, 915 (56.8%) patients were not intubated. They received standard oxygen (N = 496, 53.9%), high-flow oxygen (HFNC, N = 187, 20.3%), noninvasive ventilation (NIV, N = 153, 17.2%), and NIV + HFNC (N = 79, 8.6%). Factors associated with IMV included age (hazard ratio = 0.92/year, 95% CI 0.86–0.99), day-1 SOFA (1.09/point, 1.06–1.13), day-1 PaO2/FiO2 (1.47, 1.05–2.07), ARF etiology (Pneumocystis jirovecii pneumonia (2.11, 1.42–3.14), invasive pulmonary aspergillosis (1.85, 1.21–2.85), and undetermined cause (1.46, 1.09–1.98). After propensity score matching, HFNC, but not NIV, had an effect on IMV rate (HR = 0.77, 95% CI 0.59–1.00, p = 0.05). ICU, hospital, and day-90 mortality rates were 32.4, 44.1, and 56.4%, respectively. Factors independently associated with hospital mortality included age (odds ratio = 1.18/year, 1.09–1.27), direct admission to the ICU (0.69, 0.54–0.87), day-1 SOFA excluding respiratory score (1.12/point, 1.08–1.16), PaO2/FiO2 < 100 (1.60, 1.03–2.48), and undetermined ARF etiology (1.43, 1.04–1.97). Initial oxygenation strategy did not affect mortality; however, IMV was associated with mortality, the odds ratio depending on IMV conditions: NIV + HFNC failure (2.31, 1.09–4.91), first-line IMV (2.55, 1.94–3.29), NIV failure (3.65, 2.05–6.53), standard oxygen failure (4.16, 2.91–5.93), and HFNC failure (5.54, 3.27–9.38).

Conclusion

HFNC has an effect on intubation but not on mortality rates. Failure to identify ARF etiology is associated with higher rates of both intubation and mortality. This suggests that in addition to selecting the appropriate oxygenation device, clinicians should strive to identify the etiology of ARF.

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Acknowledgements

This study was performed on behalf of the “Caring for critically ill immunocompromised patients—Multinational Network (Nine-I). This group includes critical care specialists from 16 countries in Europe, the USA, Canada and South America. The primary aim of this group is to improve and standardize practices in the management of critically ill immunocompromised patients.

Contributors: Antoine Rabbat, Hôpital Cochin, Paris, France; Isabelle Vinatier, CHD de Vendée, La Roche Sur Yon, France; Michael Darmon, CHU, Saint-Etienne, France; Kada Klouche, Laura Platon, CHU, Montpellier, France; Martine Nyunga, CHG Victor Provo, Roubaix, France; Alexandre Demoule, Julien Mayaux, CHU Pitié-Salpétrière, Paris, France; Florent Wallet, CHU, Lyon Sud, France; Akli Chermak, CH Sud Essonne, Etampes, France; Amelie Seguin Réanimation Medicale - CHU de Caen, Caen, France; Caroline Lemaitre, Elise Artaud-Macari, University Hospital, Medical Intensive Care, Rouen, France; Jonas Nelsen, Rigshospitalet, Copenhagen, Denmark; Ann M. Moeller, Herlev University Hospital, UCPH, Herlev, Denmark; Thomas Kaufmann, Department of Critical Care, Groningen, the Netherlands; Dennis Bergmans, Department of Critical Care, Maastricht, the Netherlands; Angélique Spoelstra de Man, Department of Critical Care, Amsterdam, the Netherlands; Ana Paula Pierre de Moraes, Hospital de Câncer do Maranhao, Brazil; William Viana, Hospital Copa d’Or, Brazil; Guilliana Moralez, Hospital GetulioVargas, Rio de Janeiro, Brazil; Thiago Lishoa, Hospital Santa Rita, Santa Casa de Misericordia, Porte Allegre, Brazil; Thiago Domingos Correa, ICU, Hospital Israelita Albert Einstein, São Paulo, Brazil; Belen Encina, Val Hebron, Barcelona, Spain; Gabriel Moreno, Department of Critical Care, Bellitge, Spain; Emilio Rodriguez Luis, Department of Critical Care, Santiago de compostella, Spain; Llorenç Socias Crespi, Department of Critical Care, Palma, Spain; Yadav Hemang, Pulmonary and Critical Care Medicine, Mayo Clinic, Rochester, MN, USA; Anne-Pascale Meert, Institut Jules Bordet, Brussels, Belgique; Dominique Benoit, Ghent University Hospital, Ghent, Belgique; Nina Buchtele, Department of Medicine I, Vienna, Austria; Thomas Staudinger, Department of Medicine I, Vienna, Austria; Gottfried Heinz, Department of Medicine II, Vienna, Austria; Gürkan Sengölge, Department of Medicine III, Vienna, Austria; Christian Zauner, Department of Medicine III, Vienna, Austria; Peter Jaksch, Department of Thoracic Surgery, Vienna, Austria; Karin Amrein, Department of Internal Medicine, Graz, Austria; Aisling Mc Mahon, Department of Critical Care, St James, Dublin, Ireland; Brian Marsh, Department of Critical Care, Mater misericordia, Dublin, Ireland; Balik Martin, Department of Critical Care, Prague, Czech Republic; Karvunidis Thomas, Department of Critical Care, Pielsa, Czech Republic; Pål Klepstad, St. Olavs Hospital, Trondheim, Norway; Anne Kuitunen, Department of Critical Care, Tempere, Finland; Gilda Cinnella, Antonella Cotoia, Ospedali Riuniti, Department of Critical Care, Foggia, Italy; Sumech Shah, Mount Sinai Hospital, Canada.

Author information

Authors and Affiliations

  1. Medical Intensive Care Unit, APHP, Hôpital Saint-Louis, Famirea Study Group, ECSTRA team, and Clinical Epidemiology, UMR 1153, Center of Epidemiology and Biostatistics, Sorbonne Paris Cité, CRESS, INSERM, Paris Diderot Sorbonne University, Paris, France

    Elie Azoulay, Virginie Lemiale & Virginie Souppart

  2. The Department of Intensive Care Medicine (710), Radboud University Medical Center, Nijmegen, The Netherlands

    Peter Pickkers & Pleun Hemelaar

  3. The Department of Critical Care and Graduate Program in Translational Medicine, D’Or Institute for Research and Education, Programa de Pós-Graduação em Clínica Médica, Rio De Janeiro, Brazil

    Marcio Soares & Jorge Salluh

  4. Department of Intensive Care, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark

    Anders Perner & Tine Sylvest Meyhoff

  5. CIBERES, Universitat Autonòma de Barcelona, European Study Group of Infections in Critically Ill Patients (ESGCIP), Barcelona, Spain

    Jordi Rello

  6. Pulmonary and Critical Care Medicine, Mayo Clinic, Rochester, MN, USA

    Philippe R. Bauer

  7. Division of Pulmonary and Critical Care, Penn State University College of Medicine, Hershey, PA, USA

    Andry van de Louw

  8. Department of Intensive Care, Hôpital Erasme, Université Libre de Bruxelles (ULB), Brussels, Belgium

    Fabio Silvio Taccone

  9. Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), St. James’s Hospital, Dublin, Ireland

    Ignacio Martin Loeches

  10. Department of Clinical Medicine, Trinity College, Wellcome Trust-HRB Clinical Research Facility, St James Hospital, Dublin, Ireland

    Ignacio Martin Loeches

  11. Department of Medicine I, Medical University of Vienna, Vienna, Austria

    Peter Schellongowski

  12. Department of Anesthesiology and Intensive Care Medicine and Institute for Medical Humanities, 1st Faculty of Medicine, Charles University in Prague and General University Hospital, Prague, Czech Republic

    Katerina Rusinova

  13. CHU Grenoble Alpes, Service de réanimation médicale, Faculté de Médecine de Grenoble, INSERM, U1042, Université Grenoble-Alpes, Grenoble, France

    Nicolas Terzi

  14. Department of Medicine and Interdepartmental Division of Critical Care Medicine, Sinai Health System, University of Toronto, Toronto, ON, Canada

    Sangeeta Mehta

  15. Agostino Gemelli University Hospital, Università Cattolica del Sacro Cuore, Rome, Italy

    Massimo Antonelli & Luca Montini

  16. Department of Medical Intensive Care Medicine, University Hospital of Angers, Angers, France

    Achille Kouatchet

  17. Department of Emergencies and Critical Care, Oslo University Hospital, Oslo, Norway

    Andreas Barratt-Due

  18. Division of Intensive Care Medicine, Department of Anesthesiology, Intensive Care and Pain Medicine, University of Helsinki and Helsinki University Hospital, Helsinki, Finland

    Miia Valkonen

  19. Department of Critical Care, University Medical Center Groningen, Groningen, The Netherlands

    Precious Pearl Landburg

  20. Center Hospitalier de Versailles, Medical-Surgical Intensive Care Unit, Le Chesnay, France

    Fabrice Bruneel

  21. Department of Anesthesiology I, Herlev University Hospital, Herlev, Denmark

    Ramin Brandt Bukan

  22. Medical ICU, Cochin Hospital, Assistance Publique-Hôpitaux de Paris and University Paris Descartes, Paris, France

    Frédéric Pène

  23. King’s College Hospital, London, SE5 9RS, UK

    Victoria Metaxa

  24. Critical Care Center, CHU Lille, School of Medicine, University of Lille, Lille, France

    Anne Sophie Moreau

  25. Terapia Intensiva, Hospital Maciel, Montevideo, Uruguay

    Gaston Burghi

  26. Normandie Univ, UNIROUEN, EA-3830, Department of Medical Intensive Care, Rouen University Hospital, 76000, Rouen, France

    Christophe Girault

  27. ICU, Fundação Pio XII, Hospital de Câncer de Barretos, Barretos, Brazil

    Ulysses V. A. Silva

  28. Medical Intensive Care Unit, La Source Hospital, CHR Orléans, Orléans, France

    François Barbier

  29. Intensive Care Department, University of Southern Denmark, Odense, Denmark

    Lene B. Nielsen

  30. Department of Anaesthesia and Intensive Care, Odense University Hospital, Odense, Denmark

    Lene B. Nielsen

  31. Medical Intensive Care Unit, Hôtel Dieu-HME-University Hospital of Nantes, Nantes, France

    Benjamin Gaborit

  32. Réanimation Polyvalente et Département d’Anesthésie et de Réanimation, Institut Paoli-Calmettes, Marseille, France

    Djamel Mokart

  33. ECSTRA Team, Biostatistics and Clinical Epidemiology, UMR 1153, INSERM, Paris Diderot Sorbonne University and Service de Biostatistique et Information Médicale AP-HP, Hôpital Saint-Louis, Paris, France

    Sylvie Chevret

Authors
  1. Elie Azoulay
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  2. Peter Pickkers
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  3. Marcio Soares
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  4. Anders Perner
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  5. Jordi Rello
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  6. Philippe R. Bauer
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  7. Andry van de Louw
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  8. Pleun Hemelaar
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  9. Virginie Lemiale
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  10. Fabio Silvio Taccone
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  11. Ignacio Martin Loeches
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  12. Tine Sylvest Meyhoff
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  13. Jorge Salluh
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  14. Peter Schellongowski
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  15. Katerina Rusinova
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  16. Nicolas Terzi
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  17. Sangeeta Mehta
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  18. Massimo Antonelli
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  19. Achille Kouatchet
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  20. Andreas Barratt-Due
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  21. Miia Valkonen
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  22. Precious Pearl Landburg
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  23. Fabrice Bruneel
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  25. Frédéric Pène
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  26. Victoria Metaxa
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  27. Anne Sophie Moreau
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  28. Virginie Souppart
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  29. Gaston Burghi
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  30. Christophe Girault
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  31. Ulysses V. A. Silva
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  32. Luca Montini
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  33. François Barbier
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  34. Lene B. Nielsen
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  35. Benjamin Gaborit
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  36. Djamel Mokart
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  37. Sylvie Chevret
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Consortia

for the Efraim investigators and the Nine-I study group

  • Antoine Rabbat
  • , Isabelle Vinatier
  • , Michael Darmon
  • , Kada Klouche
  • , Laura Platon
  • , Laura Platon
  • , Alexandre Demoule
  • , Julien Mayaux
  • , Florent Wallet
  • , Akli Chermak
  • , Caroline Lemaitre
  • , Elise Artaud-Macari
  • , Jonas Nelsen
  • , Ann M. Moeller
  • , Thomas Kaufmann
  • , Dennis Bergmans
  • , Angélique Spoelstra de Man
  • , Ana Paula Pierre de Moraes
  • , William Viana
  • , Guilliana Moralez
  • , Thiago Lishoa
  • , Belen Encina
  • , Gabriel Moreno
  • , Emilio Rodriguez Luis
  • , Llorenç Socias Crespi
  • , Yadav Hemang
  • , Anne-Pascale Meert
  • , Dominique Benoit
  • , Nina Buchtele
  • , Thomas Staudinger
  • , Gottfried Heinz
  • , Gürkan Sengölge
  • , Christian Zauner
  • , Peter Jaksch
  • , Karin Amrein
  • , Aisling McMahon
  • , Brian Marsh
  • , Balik Martin
  • , Karvunidis Thomas
  • , Pål Klepstad
  • , Anne Kuitunen
  • , Gilda Cinnella
  • , Antonella Cotoia
  •  & Sumech Shah

Corresponding author

Correspondence to Elie Azoulay.

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Conflicts of interest

The authors declare no conflict of interest in relation to this study.

Additional information

The members of the Efraim investigators and the Nine-I study group are listed in the Acknowledgements and in ESM 2.

All authors substantially contributed to the design of the study, acquisition, analysis, and interpretation of data, drafted and revised the manuscript for important intellectual content, approved the final version, and agreed to be accountable for all aspects of the work.

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Azoulay, E., Pickkers, P., Soares, M. et al. Acute hypoxemic respiratory failure in immunocompromised patients: the Efraim multinational prospective cohort study. Intensive Care Med 43, 1808–1819 (2017). https://doi.org/10.1007/s00134-017-4947-1

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