Diagnosing enterovirus meningitis via blood transcriptomics: an alternative for lumbar puncture?


Journal

Journal of translational medicine
ISSN: 1479-5876
Titre abrégé: J Transl Med
Pays: England
ID NLM: 101190741

Informations de publication

Date de publication:
23 08 2019
Historique:
received: 14 03 2019
accepted: 18 08 2019
entrez: 25 8 2019
pubmed: 25 8 2019
medline: 23 6 2020
Statut: epublish

Résumé

Meningitis can be caused by several viruses and bacteria. Identifying the causative pathogen as quickly as possible is crucial to initiate the most optimal therapy, as acute bacterial meningitis is associated with a significant morbidity and mortality. Bacterial meningitis requires antibiotics, as opposed to enteroviral meningitis, which only requires supportive therapy. Clinical presentation is usually not sufficient to differentiate between viral and bacterial meningitis, thereby necessitating cerebrospinal fluid (CSF) analysis by PCR and/or time-consuming bacterial cultures. However, collecting CSF in children is not always feasible and a rather invasive procedure. In 12 Belgian hospitals, we obtained acute blood samples from children with signs of meningitis (49 viral and 7 bacterial cases) (aged between 3 months and 16 years). After pathogen confirmation on CSF, the patient was asked to give a convalescent sample after recovery. 3' mRNA sequencing was performed to determine differentially expressed genes (DEGs) to create a host transcriptomic profile. Enteroviral meningitis cases displayed the largest upregulated fold change enrichment in type I interferon production, response and signaling pathways. Patients with bacterial meningitis showed a significant upregulation of genes related to macrophage and neutrophil activation. We found several significantly DEGs between enteroviral and bacterial meningitis. Random forest classification showed that we were able to differentiate enteroviral from bacterial meningitis with an AUC of 0.982 on held-out samples. Enteroviral meningitis has an innate immunity signature with type 1 interferons as key players. Our classifier, based on blood host transcriptomic profiles of different meningitis cases, is a possible strong alternative for diagnosing enteroviral meningitis.

Sections du résumé

BACKGROUND
Meningitis can be caused by several viruses and bacteria. Identifying the causative pathogen as quickly as possible is crucial to initiate the most optimal therapy, as acute bacterial meningitis is associated with a significant morbidity and mortality. Bacterial meningitis requires antibiotics, as opposed to enteroviral meningitis, which only requires supportive therapy. Clinical presentation is usually not sufficient to differentiate between viral and bacterial meningitis, thereby necessitating cerebrospinal fluid (CSF) analysis by PCR and/or time-consuming bacterial cultures. However, collecting CSF in children is not always feasible and a rather invasive procedure.
METHODS
In 12 Belgian hospitals, we obtained acute blood samples from children with signs of meningitis (49 viral and 7 bacterial cases) (aged between 3 months and 16 years). After pathogen confirmation on CSF, the patient was asked to give a convalescent sample after recovery. 3' mRNA sequencing was performed to determine differentially expressed genes (DEGs) to create a host transcriptomic profile.
RESULTS
Enteroviral meningitis cases displayed the largest upregulated fold change enrichment in type I interferon production, response and signaling pathways. Patients with bacterial meningitis showed a significant upregulation of genes related to macrophage and neutrophil activation. We found several significantly DEGs between enteroviral and bacterial meningitis. Random forest classification showed that we were able to differentiate enteroviral from bacterial meningitis with an AUC of 0.982 on held-out samples.
CONCLUSIONS
Enteroviral meningitis has an innate immunity signature with type 1 interferons as key players. Our classifier, based on blood host transcriptomic profiles of different meningitis cases, is a possible strong alternative for diagnosing enteroviral meningitis.

Identifiants

pubmed: 31443725
doi: 10.1186/s12967-019-2037-6
pii: 10.1186/s12967-019-2037-6
pmc: PMC6708255
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

282

Références

Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Proc Natl Acad Sci U S A. 2013 Jul 30;110(31):12792-7
pubmed: 23858444
J Infect Dis. 2013 Nov 15;208(10):1664-8
pubmed: 23901082
JAMA. 2016 Aug 23-30;316(8):835-45
pubmed: 27552617
Curr Opin Infect Dis. 2014 Jun;27(3):228-35
pubmed: 24739346
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W645-50
pubmed: 16912992
PLoS One. 2015 Mar 18;10(3):e0120012
pubmed: 25785720
BMC Infect Dis. 2013 Jul 17;13:326
pubmed: 23865742
Cell Host Microbe. 2009 Sep 17;6(3):199-200
pubmed: 19748461
J Clin Virol. 2016 Apr;77:15-20
pubmed: 26875098
Nat Methods. 2015 Apr;12(4):357-60
pubmed: 25751142
Vaccine. 2018 Oct 8;36(42):6282-6289
pubmed: 30205979
Eur J Immunol. 1997 Oct;27(10):2484-9
pubmed: 9368600
JAMA. 2007 Jan 3;297(1):52-60
pubmed: 17200475
JAMA. 2016 Aug 23-30;316(8):846-57
pubmed: 27552618
Pediatr Emerg Care. 2009 Feb;25(2):112-7; quiz 118-20
pubmed: 19225382
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
Front Neurosci. 2013 Mar 18;7:33
pubmed: 23515576
Blood. 2007 Mar 1;109(5):2066-77
pubmed: 17105821
PLoS Med. 2013 Nov;10(11):e1001549
pubmed: 24265599
Arch Dis Child. 2012 Sep;97(9):799-805
pubmed: 22764093
PLoS One. 2013;8(1):e52198
pubmed: 23326326
Pediatrics. 2002 Oct;110(4):712-9
pubmed: 12359784
Eur J Clin Microbiol Infect Dis. 2007 Jun;26(6):403-12
pubmed: 17534678

Auteurs

Esther Bartholomeus (E)

Center of Medical Genetics, University of Antwerp/Antwerp University Hospital, Edegem, Belgium.
AUDACIS, Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium.

Nicolas De Neuter (N)

AUDACIS, Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium.
Adrem Data Lab, Department of Mathematics and Computer Science, University of Antwerp, Antwerp, Belgium.
Biomedical Informatics Research Network Antwerp (Biomina), University of Antwerp, Antwerp, Belgium.

Annelies Lemay (A)

Department of Paediatrics, AZ Turnhout, Turnhout, Belgium.

Luc Pattyn (L)

Department of Paediatrics, AZ Turnhout, Turnhout, Belgium.

David Tuerlinckx (D)

Université Catholique de Louvain/CHU UCL Namur, Site Dinant, Service de Pédiatrie, Dinant, Belgium.

David Weynants (D)

Department of Paediatrics, CHU ULC Namur Ste Elisabeth, Namur, Belgium.

Koen Van Lede (K)

Department of Paediatrics, AZ Nikolaas, Sint-Niklaas, Belgium.

Gerlant van Berlaer (G)

Department of Emergency Medicine/Pediatric Care, University Hospital Brussels, Jette, Belgium.

Dominique Bulckaert (D)

Department of Emergency Medicine/Pediatric Care, University Hospital Brussels, Jette, Belgium.

Tine Boiy (T)

Department of Paediatrics, Antwerp University Hospital, Edegem, Belgium.

Ann Vander Auwera (A)

Department of Paediatrics, GZA Sint-Augustinus, Wilrijk, Belgium.

Marc Raes (M)

Department of Paediatrics, Jessa Hospital, Hasselt, Belgium.

Dimitri Van der Linden (D)

Paediatric Infectious Diseases, Department of Paediatrics, CHU ULC Cliniques Universitaires Saint-Luc, UCLouvain, Brussels, Belgium.

Helene Verhelst (H)

Department of Paediatric Rheumatology, University Hospital, Ghent, Belgium.

Susanne Van Steijn (S)

Department of Paediatrics, ZNA Paola, Antwerp, Belgium.

Tijl Jonckheer (T)

Department of Paediatrics, GZA Sint-Vincentius, Antwerp, Belgium.

Joke Dehoorne (J)

Department of Paediatric Rheumatology, University Hospital, Ghent, Belgium.

Rik Joos (R)

Department of Paediatric Rheumatology, University Hospital, Ghent, Belgium.
Antwerp Center for Paediatric Rheumatology and AutoInflammatory Diseases, Antwerp, Belgium.

Hilde Jansens (H)

Department of Laboratory Medicine, Antwerp University Hospital, Edegem, Belgium.

Arvid Suls (A)

Center of Medical Genetics, University of Antwerp/Antwerp University Hospital, Edegem, Belgium.
AUDACIS, Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium.

Pierre Van Damme (P)

Centre for the Evaluation of Vaccination (CEV), Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, Belgium.

Kris Laukens (K)

AUDACIS, Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium.
Adrem Data Lab, Department of Mathematics and Computer Science, University of Antwerp, Antwerp, Belgium.
Biomedical Informatics Research Network Antwerp (Biomina), University of Antwerp, Antwerp, Belgium.

Geert Mortier (G)

Center of Medical Genetics, University of Antwerp/Antwerp University Hospital, Edegem, Belgium.

Pieter Meysman (P)

AUDACIS, Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium.
Adrem Data Lab, Department of Mathematics and Computer Science, University of Antwerp, Antwerp, Belgium.
Biomedical Informatics Research Network Antwerp (Biomina), University of Antwerp, Antwerp, Belgium.

Benson Ogunjimi (B)

AUDACIS, Antwerp Unit for Data Analysis and Computation in Immunology and Sequencing, University of Antwerp, Antwerp, Belgium. benson.ogunjimi@uantwerpen.be.
Department of Paediatrics, Antwerp University Hospital, Edegem, Belgium. benson.ogunjimi@uantwerpen.be.
Antwerp Center for Paediatric Rheumatology and AutoInflammatory Diseases, Antwerp, Belgium. benson.ogunjimi@uantwerpen.be.
Centre for Health Economics Research & Modeling Infectious Diseases (CHERMID), Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, Belgium. benson.ogunjimi@uantwerpen.be.
Antwerp Center for Translational Immunology and Virology (ACTIV), Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, 00323/8213251, Antwerp, Belgium. benson.ogunjimi@uantwerpen.be.
Department of Pediatrics, University Hospital Brussels, Jette, Belgium. benson.ogunjimi@uantwerpen.be.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH