Pneumococcal pneumonia and endotoxemia: An experimental and clinical reappraisal.

Streptococcus pneumoniae endotoxemia immune response lipopolysaccharide pneumonia

Journal

European journal of clinical investigation
ISSN: 1365-2362
Titre abrégé: Eur J Clin Invest
Pays: England
ID NLM: 0245331

Informations de publication

Date de publication:
Jan 2024
Historique:
revised: 20 07 2023
received: 12 06 2023
accepted: 02 08 2023
pubmed: 29 8 2023
medline: 29 8 2023
entrez: 29 8 2023
Statut: ppublish

Résumé

Circulating endotoxins could result from bacterial digestive translocation during sepsis, thus contributing to uncontrolled systemic inflammation, leading in turn to organ dysfunction. We addressed this issue in the setting of severe pneumococcal pneumonia. Endotoxemia was measured in a clinically relevant rabbit model of ventilated pneumococcal pneumonia and in 110 patients with bacteraemic pneumonia, using a patented mass spectrometry (LC-MS/MS) method for detection of 3-OH fatty acids (C10, C12, C14, C16 and C18), which are molecules bound to the lipid A motif of LPS. Whereas higher levels of systemic inflammation and organ dysfunctions were found, there was no significant difference in lipopolysaccharide concentrations when infected rabbits were compared to non-infected ones, or when patients were compared to healthy volunteers. Seemingly, endotoxins do not drive the overwhelming inflammation associated with severe forms of pneumococcal pneumonia.

Sections du résumé

BACKGROUND BACKGROUND
Circulating endotoxins could result from bacterial digestive translocation during sepsis, thus contributing to uncontrolled systemic inflammation, leading in turn to organ dysfunction. We addressed this issue in the setting of severe pneumococcal pneumonia.
METHODS METHODS
Endotoxemia was measured in a clinically relevant rabbit model of ventilated pneumococcal pneumonia and in 110 patients with bacteraemic pneumonia, using a patented mass spectrometry (LC-MS/MS) method for detection of 3-OH fatty acids (C10, C12, C14, C16 and C18), which are molecules bound to the lipid A motif of LPS.
RESULTS RESULTS
Whereas higher levels of systemic inflammation and organ dysfunctions were found, there was no significant difference in lipopolysaccharide concentrations when infected rabbits were compared to non-infected ones, or when patients were compared to healthy volunteers.
CONCLUSIONS CONCLUSIONS
Seemingly, endotoxins do not drive the overwhelming inflammation associated with severe forms of pneumococcal pneumonia.

Identifiants

pubmed: 37642230
doi: 10.1111/eci.14077
doi:

Types de publication

Letter

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14077

Subventions

Organisme : (PHRC) 2004/37 (HyaloStrepto project)
Organisme : AOI (Appel d'Offre Interne) from the University hospital of Dijon
Organisme : INSERM (Institut National de la Sante et de la Recherche Medicale - Center de Recherche UMR 1231, Dijon, France), the national research agency (ANR) Investissements d'Avenir Grant (ANR-11 LABX-0021-01, Labex Lipstic, Dijon, France), and the Université Bourgogne Franche Comte (Dijon, France).
Organisme : MSD-Avenir 2018 (Paris, France; sponsorship agreement) (experimental project)

Investigateurs

Delphine Croisier (D)
Sandrine Gohier (S)
Carole Charles (C)
Adrien Guilloteau (A)
Marc Bardou (M)
Ines Ben Guezala (IB)
Jeanne Godon (J)
Pierre-Emmanuel Charles (PE)
Sylvie Nguyen (S)
Thomas Gauthier (T)
Jean-Paul Pais de Barros (JP)
Hélène Choubley (H)
Victoria Bergas (V)
Marine Jacquier (M)
Jennifer Tetu (J)
Jean-Pierre Quenot (JP)
Maxime Luu (M)
Christine Binquet (C)
David Masson (D)
Lionel Piroth (L)
Mathieu Blot (M)

Informations de copyright

© 2023 Stichting European Society for Clinical Investigation Journal Foundation. Published by John Wiley & Sons Ltd.

Références

Kritselis I, Tzanetakou V, Adamis G, et al. The level of endotoxemia in sepsis varies in relation to the underlying infection: impact on final outcome. Immunol Lett. 2013;152(2):167-172.
Cangemi R, Della Valle P, Calvieri C, et al. Low-grade endotoxemia and clotting activation in the early phase of pneumonia. Respirology. 2016;21(8):1465-1471.
Cangemi R, Pignatelli P, Carnevale R, et al. Low-grade endotoxemia, gut permeability and platelet activation in community-acquired pneumonia. J Infect. 2016;73(2):107-114.
Sirivongrangson P, Kulvichit W, Payungporn S, et al. Endotoxemia and circulating bacteriome in severe COVID-19 patients. Intensive Care Med Exp. 2020;8(1):72.
Mohammad S, Thiemermann C. Role of metabolic endotoxemia in systemic inflammation and potential interventions. Front Immunol. 2020;11:594150.
van der Poll T, Levi M. Crosstalk between inflammation and coagulation: the lessons of sepsis. Curr Vasc Pharmacol. 2012;10(5):632-638.
Blot M, Jacquier M, Pauchard LA, et al. Adverse mechanical ventilation and pneumococcal pneumonia induce immune and mitochondrial dysfunctions mitigated by mesenchymal stem cells in rabbits. Anesthesiology. 2022;136(2):293-313.
Pais de Barros JP, Gautier T, Sali W, et al. Quantitative lipopolysaccharide analysis using HPLC/MS/MS and its combination with the limulus amebocyte lysate assay. J Lipid Res. 2015;56(7):1363-1369.
Dargent A, Pais De Barros JP, Ksiazek E, et al. Improved quantification of plasma lipopolysaccharide (LPS) burden in sepsis using 3-hydroxy myristate (3HM): a cohort study. Intensive Care Med. 2019;45(11):1678-1680.
Love J, Selker R, Marsman M, et al. JASP: graphical statistical software for common statistical designs. J Stat Softw. 2019;88:1-17.
Cohen J. The detection and interpretation of endotoxaemia. Intensive Care Med. 2000;26(Suppl 1):S51-S56.
Novitsky TJ. Limitations of the limulus amebocyte lysate test in demonstrating circulating lipopolysaccharides. Ann N Y Acad Sci. 1998;851:416-421.
Munford RS. Endotoxemia-menace, marker, or mistake? J Leukoc Biol. 2016;100(4):687-698.
Tamura H, Reich J, Nagaoka I. Outstanding contributions of LAL technology to pharmaceutical and medical science: review of methods, progress, challenges, and future perspectives in early detection and management of bacterial infections and invasive fungal diseases. Biomedicine. 2021;9(5):536.
Guedj K, Uzzan M, Soudan D, et al. I-FABP is decreased in COVID-19 patients, independently of the prognosis. PloS One. 2021;16(4):e0249799.

Auteurs

Jeanne Godon (J)

Department of Infectious Diseases, Dijon-Bourgogne University Hospital, Dijon, France.

Pierre-Emmanuel Charles (PE)

Department of Intensive Care, Dijon-Bourgogne University Hospital, Dijon, France.
Lipness Team, INSERM Research Centre LNC-UMR1231 and LabEx LipSTIC, University of Burgundy, Dijon, France.

Sylvie Nguyen (S)

Lipness Team, INSERM Research Centre LNC-UMR1231 and LabEx LipSTIC, University of Burgundy, Dijon, France.

Jean-Paul Pais de Barros (JP)

Lipidomic Analytic Platform, Dijon, France.

Hélène Choubley (H)

Lipidomic Analytic Platform, Dijon, France.

Marine Jacquier (M)

Department of Intensive Care, Dijon-Bourgogne University Hospital, Dijon, France.
Lipness Team, INSERM Research Centre LNC-UMR1231 and LabEx LipSTIC, University of Burgundy, Dijon, France.

Jennifer Tetu (J)

Laboratory of bacteriology, Dijon-Bourgogne University Hospital, Dijon, France.

Jean-Pierre Quenot (JP)

Department of Intensive Care, Dijon-Bourgogne University Hospital, Dijon, France.
Lipness Team, INSERM Research Centre LNC-UMR1231 and LabEx LipSTIC, University of Burgundy, Dijon, France.
CHU Dijon-Bourgogne, INSERM, Université de Bourgogne CIC 1432 Module Épidémiologie Clinique, Dijon France and LabEx LipSTIC, University of Burgundy, Dijon, France.

Maxime Luu (M)

CHU Dijon-Bourgogne, INSERM, Université de Bourgogne CIC 1432 Module Plurithématique, Dijon, University of Burgundy, Dijon, France.

Christine Binquet (C)

CHU Dijon-Bourgogne, INSERM, Université de Bourgogne CIC 1432 Module Épidémiologie Clinique, Dijon France and LabEx LipSTIC, University of Burgundy, Dijon, France.

David Masson (D)

Lipness Team, INSERM Research Centre LNC-UMR1231 and LabEx LipSTIC, University of Burgundy, Dijon, France.

Lionel Piroth (L)

Department of Infectious Diseases, Dijon-Bourgogne University Hospital, Dijon, France.
CHU Dijon-Bourgogne, INSERM, Université de Bourgogne CIC 1432 Module Épidémiologie Clinique, Dijon France and LabEx LipSTIC, University of Burgundy, Dijon, France.

Mathieu Blot (M)

Department of Infectious Diseases, Dijon-Bourgogne University Hospital, Dijon, France.
Lipness Team, INSERM Research Centre LNC-UMR1231 and LabEx LipSTIC, University of Burgundy, Dijon, France.
CHU Dijon-Bourgogne, INSERM, Université de Bourgogne CIC 1432 Module Épidémiologie Clinique, Dijon France and LabEx LipSTIC, University of Burgundy, Dijon, France.

Classifications MeSH