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Imported falciparum malaria in adults: host- and parasite-related factors associated with severity. The French prospective multicenter PALUREA cohort study

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A Correction to this article was published on 14 November 2017

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Abstract

Purpose

Prospective data on potential factors associated with severity of imported Plasmodium falciparum malaria are lacking. We evaluated whether several host- and parasite-related biomarkers may improve early severity evaluation.

Methods

Prospective multicenter observational study comparing uncomplicated and severe imported falciparum malaria in adults conducted in France in 52 units, from 2007 to 2010. Association of several host- and parasite-related biomarkers with severity of malaria was tested using univariate and multivariate analyses.

Results

Of 295 patients, 140 had uncomplicated malaria and 155 severe malaria (including very severe and less severe cases according to predefined criteria). Curative intravenous quinine treatment was used in 154/155 patients with severe malaria and atovaquone/proguanil in 74 % of patients with uncomplicated malaria. Hospital mortality was 5.2 % (8 patients), all in the severe malaria group. Among host-related biomarkers, CRP, procalcitonin, and sTREM-1 were significantly higher and albumin was significantly lower in severe versus uncomplicated malaria; only the last three biomarkers also differed significantly between the very and less severe malaria groups. Among parasite-related biomarkers, only plasma PfHRP2 was significantly higher in severe versus uncomplicated malaria and in very severe versus less severe malaria; parasitemia did not differ between very and less severe malaria. By multivariate analysis, only lower plasma albumin and higher sTREM-1 were associated with greater severity, with intermediate accuracies.

Conclusions

During imported malaria, the most useful biomarkers associated with severity seem to be plasma albumin and sTREM-1; and among parasite-related parameters, PfHRP2 was more strongly associated with severity than parasitemia was.

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Change history

  • 14 November 2017

    The members of the Palurea Study Group were provided in such a way that they could not be indexed as collaborators on PubMed. The publisher apologizes for this error and is pleased to list the members of the group here:

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Acknowledgments

We thank all the nurses, physicians, and biologists of the PALUREA Study Group (see below) for their excellent care of the patients. We thank Isabelle Hoffmann, Delphine Prieur, Amandine Fauquembergue, and Virginia Olympio from the Unité de Recherche Clinique Paris Nord for coordinating the sample shipments and managing the data. We thank A. Wolfe MD for helping to prepare the manuscript.

Members of the PALUREA Study Group (including authors)

Hopital Bichat Claude Bernard, Paris: M. Wolff, B. Mourvillier, C. Aubron, L. Bouadma and B. Regnier (ICU), S. Matheron, E. d’Ortenzio, R. Matra, E. Bouvet, J. Tourret, J. Dorchies, S. Males, C. Rioux, R. Flicoteaux and P. Yeni (Infectious Diseases Unit), C. Choquet, F. Spingler, E. Kargougou and E. Casalino (Emergency Unit), S. Houze and J. Le Bras (Parasitology and Malaria National Reference Center), M.G. Huisse and V. Ollivier (Hematology), A. Kalloumeh and B. Grandchamp (Biochemistry), F. Tubach, Y. Miri and C. Roy (Département d’Epidémiologie et Recherche Clinique)

Hopital d’Angers: E. Fresnoy, F. Grelon, P. Asfar, A. Kouatchet and A. Mercat (ICU), M.L. Joly-Guillou, M. Kempf and M. Eveillard (Microbiology)

Hopital Paul Morel, Vesoul: P. Daoudal (ICU), A. Royer (Parasitology)

Hopital d’Orleans: I. Runge, A. Mathonnet and T. Boulain (ICU), L. Bret (Parasitology), L. Hocqueloux, J.M. Segalin, C. Mille, M. Niang and T. Prazuck (Infectious Diseases Unit)

Hopital Henri Mondor, Creteil: M. Fortin, F. Schortgen and C. Brun Buisson (ICU), F. Botterel and S. Bretagne (Parasitology)

Hopital de Tourcoing: O. Leroy, H. Georges, A. Meybeck and B. Guery (ICU), P. Patoz and C. Dhennain (Parasitology)

Hopital Charles Nicolle, Rouen: D. Chakarian, K. Azougagh and G. Bonmarchand (ICU), P. Abboud, L. Favennec and JF. Lemeland (Parasitology)

Hopital Laveran, Marseille: E. Peytel, R. Petrognani, A. Nau, A. Puidupin and J.P. Carpentier (ICU), F. Simon (Infectious Diseases Unit), E. Garnotel and J.L. Moalic (Parasitology)

Hopital Jean Verdier, Bondy: L. Tual, R. Amathieu and G. Dhonneur (ICU), M. N’Diaye and V. Jeantils (Infectious Diseases Unit), C. Chassaignon, A.L. Guillerm, D. Riche, N. Javaud, F. Pevirieri, J. Benkel, D. Luis, M.C. Bon, G. Lenoir and B. Bernot (Emergency Unit), A. Collignon, D. Bemba and I. Poilane (Parasitology)

Hopital de la Pitie Salpetriere, Paris: J.L. Trouillet, C.E. Luyt, M. Mirabel and J. Chastre (ICU), P. Hochedez, A. Perignon and E. Caumes (Infectious Diseases Unit), M. Thellier, and M. Danis (Parasitology), A. Faussart and J. Nafziger (Biology)

Hopital de Limoges: H. Gastinne and N. Pichon (ICU), D. Ajzenberg and M.L. Darde (Parasitology)

Hopital Antoine Beclere, Clamart: F. Jacobs and F. Brivet (ICU), A. Veyradier and A. Marfaing-Koka (Parasitology and Hematology)

Hopital de Grenoble: J.F. Timsit and L. Hammer (ICU), D. Maubon and H. Pelloux (Parasitology)

Hopital Cochin, Paris: F. Pene, J. Charpentier, S. Marque, C. Rousseau and J.P. Mira (ICU)

Hopital André Mignot, Versailles: F. Bruneel, P. Guezennec, G. Troche, and J.P. Bedos (ICU), O. Eloy and C. Palette (Parasitology and Biology), A. Therby, S. Monnier and A. Greder-Bellan (Infectious Diseases Unit)

Hopital de Rangueil, Toulouse: P. Cougot (ICU)

Hopital Emile Muller, Mulhouse: K. Kuteifan, Y. Mootien and P. Guiot (ICU), J.M. Delarbre and M.H. Kiefer (Microbiology and Parasitology)

Hopital Ambroise Paré, Boulogne: B. Page and A. Vieillard Baron (ICU), J. Dunand (Parasitology)

Hopital de Saint Germain en Laye: Y. Loubieres, JL. Ricome (ICU), J.Y. Peltier and Y. Giudicelli (Parasitology and Biology)

Hopital Begin, Saint Mandé: C. Pelletier and J.M. Rousseau (ICU), P. Imbert, C. Rapp, F. Mechai, R. Barruet and T. Debord (Infectious Diseases Unit), J.E. Pilo and J.D. Cavallo (Biology)

Hopital Purpan, Toulouse: O. Angles and M. Genestal (ICU)

Hopital Hotel Dieu, Nantes: C. Bretonnière, L. Nicolet, L. Jalin and D. Villers (ICU), J.P. Talarmin, O. Grossi and F. Raffi (Infectious Diseases Unit), F. Gay-Andrieu and T. Bompoil (Parasitology)

Hopital Pontchaillou, Rennes: C. Camus, A. Gros and Y. Le Tulzo (ICU), M. Revest, F. Fily, J.M. Chapplain, P. Tattevin and C. Michelet (Infectious Diseases Unit), S. Chevrier and C. Guigen (Parasitology)

Hopital Lariboisiere, Paris: B. Megarbane and F. Baud (ICU), J.M. Launay, C. Gourmel and F. Derouin (Biology and Parasitology)

Hopital Saint Louis, Paris: S. de Miranda, G. Thiery, S. Legriel, E. Azoulay and B. Schlemmer (ICU), N. Colin de Verdieres, M. Lagrange-Xelot, S. Gallien, N. De Castro, J. Pavie, M. Lafaurie and J.M. Molina (Infectious Diseases Unit), C. Sarfati and F. Derouin (Parasitology)

Hopital Gui de Chauliac, Montpellier: P. Corne and P. Jonquet (ICU), J.F. Schved, C. Biron and C. Bret (Hematology)

Hopital Lapeyronie, Montpellier: K. Klouche and P. Beraud (ICU), J.P. Cristol (Biology)

Hopital Pellegrin, Bordeaux: D. Gruson, B. Herpe, M. Delacre and Y. Castaing (ICU), P. Fialon and P. Vincendeau (Parasitology)

Hopital Avicenne, Bobigny: F. Vincent, P. Karoubi and Y. Cohen (ICU), H. Cordel, V. Prendki, J. Cailhol, S. Abgrall, H. Gros, C. Fantinato and O. Bouchaud (Infectious Diseases Unit), F. Cymbalista, Y. Senghor and R. Durand (Parasitology)

Hopital Delafontaine, Saint Denis: N. Memain, M. Thuong, C. Adrie, L. Darques, G. Moret and F. Fraisse (ICU), N. Godineau and C. Chaplain (Parasitology), M. Prevel and R.J. Mary (Emergency Unit)

Hopital Victor Dupouy, Argenteuil: G. Plantefeve, G. Bleichner and H. Mentec (ICU), F. Leturdu (Biology and Parasitology)

Hopital de l’Archet, Nice: H. Hyvernat and G. Bernardin (ICU), P. Delaunay and P. Marty (Parasitology)

Hopital Saint Antoine, Paris: J.L. Baudel, E. Maury and G. Offenstadt (ICU), J.L. Meynard J. Pacanowski, Z. Ouazene, D. Bollens, M.C. Meyohas, L. Fonquerine and P.M. Girard (Infectious Diseases Unit), G. Belkadi, D. Magne and P. Roux (Parasitology)

Hopital Louis Mourier, Colombes: L. Rusel, J.D. Ricard and D. Dreyfuss (ICU), E. Mortier and P. Vinceneux (Infectious Diseases Unit), M. Bloch and G. Galeazzi (Parasitology).

Hopital de la Côte de Nacre, Caen: P. Charbonneau (ICU), C. Duhamel and R. Leclercq (Parasitology)

Hopital d’Aulnay sous-Bois: J.L. Delassus and D. Malbec (Infectious Diseases Unit), D. Lusina and H. Broutier (Parasitology)

Hopital Necker, Paris: C. Charlier, F. Lanternier, H. Coignard and O. Lortholary (Infectious Diseases Unit), M.E. Bougnoux (Parasitology)

Centre Médical de l’Institut Pasteur de Paris: P.H. Consigny and A. Simons de Fanti (Infectious Diseases Unit), A.S. Leguern (Parasitology)

Hôpital de Nancy: S. Gibot (ICU) and F. Massin (Immunology)

Author information

Authors and Affiliations

  1. Service de Réanimation Médico-Chirurgicale, Centre Hospitalier de Versailles, 177 rue de Versailles, 78157, Le Chesnay, France

    Fabrice Bruneel

  2. Université Paris Diderot, Sorbonne Paris Cité, UMR 1123, 75018, Paris, France

    Florence Tubach

  3. Département d’Epidémiologie et Recherche Clinique, CIC-EC 1425, AP-HP, Hôpital Bichat, 75018, Paris, France

    Florence Tubach & Carine Roy

  4. INSERM, CIC-EC 1425, U1123, 75018, Paris, France

    Florence Tubach & Carine Roy

  5. Service de Réanimation, Centre Hospitalier Universitaire Cochin Saint-Vincent de Paul, AP-HP, 75014, Paris, France

    Jean-Paul Mira

  6. Service de Parasitologie, Centre Hospitalier Universitaire Bichat-Claude Bernard, AP-HP, 75018, Paris, France

    Sandrine Houze & Jacques Le Bras

  7. Service de Réanimation Médicale, Hôpital Central, Centre Hospitalier Universitaire de Nancy, 54035, Nancy, France

    Sebastien Gibot

  8. Unité d’Hémato-Immunologie, Centre Hospitalier Universitaire Bichat-Claude Bernard, AP-HP, 75018, Paris, France

    Marie-Genevieve Huisse

  9. Service de Réanimation Médicale et Toxicologique, Centre Hospitalier Universitaire Lariboisière, AP-HP, 75010, Paris, France

    Bruno Megarbane

  10. Service d’Accueil des Urgences, Centre Hospitalier Universitaire Bichat-Claude Bernard, AP-HP, 75018, Paris, France

    Christophe Choquet

  11. Service de Réanimation Médicale, Centre Hospitalier Universitaire Gui de Chauliac, 34295, Montpellier, France

    Philippe Corne

  12. Service d’Anesthésiologie et Réanimation, Hôpital d’Instruction des Armées Laveran, 13384, Marseille, France

    Eric Peytel

  13. Service de Réanimation Médicale Polyvalente, Centre Hospitalier Universitaire de Nantes, Hotel Dieu, 44093, Nantes, France

    Daniel Villers

  14. Service de Réanimation Médicale et Infectieuse, Centre Hospitalier Universitaire de Rennes, Hôpital Pontchaillou, 35033, Rennes, France

    Christophe Camus

  15. Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire Avicenne, AP-HP, 93009, Bobigny, France

    Olivier Bouchaud

  16. Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de la Pitié-Salpêtrière, AP-HP, 75013, Paris, France

    Eric Caumes

  17. Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Saint- Antoine, AP-HP, 75012, Paris, France

    Pierre-Marie Girard

  18. Service de Maladies Infectieuses et Tropicales, Hôpital d’Instruction des Armées Laveran, 13384, Marseille, France

    Fabrice Simon

  19. Unité de Biochimie Clinique, Centre Hospitalier Universitaire Bichat-Claude Bernard, AP-HP, 75018, Paris, France

    Antoine Kalloumeh

  20. Service de Parasitologie, Centre Hospitalier Universitaire Avicenne, AP-HP, 93009, Bobigny, France

    Remy Durand

  21. Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire Bichat-Claude Bernard, AP-HP, 75018, Paris, France

    Sophie Matheron

  22. Service de Réanimation Médicale et Infectieuse, Centre Hospitalier Universitaire Bichat-Claude Bernard, AP-HP, 75018, Paris, France

    Michel Wolff

Authors
  1. Fabrice Bruneel
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  2. Florence Tubach
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  3. Jean-Paul Mira
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  4. Sandrine Houze
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  5. Sebastien Gibot
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  6. Marie-Genevieve Huisse
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  7. Bruno Megarbane
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  8. Christophe Choquet
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  9. Philippe Corne
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  10. Eric Peytel
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  11. Daniel Villers
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  12. Christophe Camus
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  13. Olivier Bouchaud
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  14. Eric Caumes
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  15. Pierre-Marie Girard
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  16. Fabrice Simon
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  17. Antoine Kalloumeh
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  18. Carine Roy
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  19. Remy Durand
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  20. Jacques Le Bras
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  21. Sophie Matheron
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  22. Michel Wolff
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Consortia

The PALUREA Study Group

Corresponding author

Correspondence to Fabrice Bruneel.

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Conflicts of interest

Fabrice Bruneel, Florence Tubach, Jean-Paul Mira, Sandrine Houze, Sebastien Gibot, Marie-Genevieve Huisse, Bruno Megarbane, Christophe Choquet, Philippe Corne, Eric Peytel, Daniel Villers, Christophe Camus, Olivier Bouchaud, Eric Caumes, Pierre-Marie Girard, Fabrice Simon, Antoine Kalloumeh, Carine Roy, Remy Durand, Jacques Le Bras, Sophie Matheron, Michel Wolff : No conflict.

Funding

This work was supported by a research grant from the French Ministry of Health (Programme Hospitalier de Recherche Clinique, PHRC—#AOR05007). The sponsor was the public organization Département de la Recherche Clinique et du Développement, Assistance Publique—Hôpitaux de Paris.

The trial is registered on ClinicalTrials.gov (#NCT00372684).

Additional information

The members of the PALUREA Study Group are listed in full in the Acknowledgments and in the electronic supplementary material (ESM 3).

Take-home message: Mortality in patients with severe imported malaria treated with intravenous quinine was still about 5 % despite the optimal healthcare setting. P. falciparum itself induces very high levels of inflammation biomarkers. The most useful biomarkers of severity may be plasma albumin and sTREM-1, while among parasite parameters PfHRP2 was a better marker for severity of imported malaria than parasitemia.

A correction to this article is available online at https://doi.org/10.1007/s00134-017-4978-7.

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Bruneel, F., Tubach, F., Mira, JP. et al. Imported falciparum malaria in adults: host- and parasite-related factors associated with severity. The French prospective multicenter PALUREA cohort study. Intensive Care Med 42, 1588–1596 (2016). https://doi.org/10.1007/s00134-016-4356-x

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  • DOI: https://doi.org/10.1007/s00134-016-4356-x

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