An unusual two-strain cholera outbreak in Lebanon, 2022-2023: a genomic epidemiology study.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
13 Aug 2024
Historique:
received: 25 01 2024
accepted: 07 08 2024
medline: 14 8 2024
pubmed: 14 8 2024
entrez: 13 8 2024
Statut: epublish

Résumé

Cholera is a life-threatening gastrointestinal infection caused by a toxigenic bacterium, Vibrio cholerae. After a lull of almost 30 years, a first case of cholera was detected in Lebanon in October 2022. The outbreak lasted three months, with 8007 suspected cases (671 laboratory-confirmed) and 23 deaths. In this study, we use phenotypic methods and microbial genomics to study 34 clinical and environmental Vibrio cholerae isolates collected throughout this outbreak. All isolates are identified as V. cholerae O1, serotype Ogawa strains from wave 3 of the seventh pandemic El Tor (7PET) lineage. Phylogenomic analysis unexpectedly reveals the presence of two different strains of the seventh pandemic El Tor (7PET) lineage. The dominant strain has a narrow antibiotic resistance profile and is phylogenetically related to South Asian V. cholerae isolates and derived African isolates from the AFR15 sublineage. The second strain is geographically restricted and extensively drug-resistant. It belongs to the AFR13 sublineage and clusters with V. cholerae isolates collected in Yemen. In conclusion, the 2022-2023 Lebanese cholera outbreak is caused by the simultaneous introduction of two different 7PET strains. Genomic surveillance with cross-border collaboration is therefore crucial for the identification of new introductions and routes of circulation of cholera, improving our understanding of cholera epidemiology.

Identifiants

pubmed: 39138238
doi: 10.1038/s41467-024-51428-0
pii: 10.1038/s41467-024-51428-0
doi:

Substances chimiques

Anti-Bacterial Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6963

Subventions

Organisme : U.S. Department of Health & Human Services | Centers for Disease Control and Prevention (CDC)
ID : 75D301-21-C-12132

Informations de copyright

© 2024. The Author(s).

Références

Clemens, J. D., Nair, G. B., Ahmed, T., Qadri, F. & Holmgren, J. Cholera. Lancet 390, 1539–1549 (2017).
doi: 10.1016/S0140-6736(17)30559-7 pubmed: 28302312
Ganesan, D., Gupta, S. S. & Legros, D. Cholera surveillance and estimation of burden of cholera. Vaccine 38, A13–A17 (2020).
doi: 10.1016/j.vaccine.2019.07.036 pubmed: 31326254
World Health Organization. Cholera Situation in Yemen. WHO-EM/CSR/434/E (World Health Organization, accessed 12 January 2023); https://applications.emro.who.int/docs/WHOEMCSR434E-eng.pdf?ua=1 .
World Health Organization. Disease Outbreak News; Cholera—Haiti (World Health Organization, accessed 25 January 2023); https://www.who.int/emergencies/disease-outbreak-news/item/2022-DON427#:~:text=Between%202%20October%20through%206,ten%20departments%20in%20the%20country .
Harb, H. Compiled Literature Report on Selected Health Conditions in Lebanon (Lebanese Ministry of Public Health, Beirut, Lebanon, 2004).
Lassalle, F. et al. Genomic epidemiology reveals multidrug resistant plasmid spread between Vibrio cholerae lineages in Yemen. Nat. Microbiol. 8, 1787–1798 (2023).
doi: 10.1038/s41564-023-01472-1 pubmed: 37770747 pmcid: 10539172
Mashe, T. et al. Highly resistant cholera outbreak strain in Zimbabwe. N. Engl. J. Med. 383, 687–689 (2020).
doi: 10.1056/NEJMc2004773 pubmed: 32786196
Lebanese Ministry of Public Health. Cholera in Lebanon (Lebanese Ministry of Public Health, accessed 23 July 2023); http://www.moph.gov.lb .
Morita, D. et al. Whole-genome analysis of clinical Vibrio cholerae O1 in Kolkata, India, and Dhaka, Bangladesh, reveals two lineages of circulating strains, indicating variation in genomic attributes. mBio 11, e01227–20 (2020).
doi: 10.1128/mBio.01227-20 pubmed: 33172996 pmcid: 7667034
Mutreja, A. & Dougan, G. Molecular epidemiology and intercontinental spread of cholera. Vaccine 38, A46–A51 (2020).
doi: 10.1016/j.vaccine.2019.07.038 pubmed: 31345641
Weill, F.-X. et al. Genomic history of the seventh pandemic of cholera in Africa. Science (1979) 358, 785–789 (2017).
Mutreja, A. et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477, 462–465 (2011).
doi: 10.1038/nature10392 pubmed: 21866102 pmcid: 3736323
Naha, A. et al. Development and evaluation of a PCR assay for tracking the emergence and dissemination of Haitian variant ctxB in Vibrio cholerae O1 strains isolated from Kolkata, India. J. Clin. Microbiol. 50, 1733–1736 (2012).
doi: 10.1128/JCM.00387-12 pubmed: 22357499 pmcid: 3347119
Domman, D. et al. Integrated view of Vibrio cholerae in the Americas. Science (1979) 358, 789–793 (2017).
Benamrouche, N. et al. Outbreak of imported seventh pandemic Vibrio cholerae O1 El Tor, Algeria, 2018. Emerg. Infect. Dis. 28, 1241–1245 (2022).
doi: 10.3201/eid2806.212451 pubmed: 35608654 pmcid: 9155889
Smith, A. M. et al. Imported cholera cases, South Africa, 2023. Emerg. Infect. Dis. 29, 1687–1690 (2023).
doi: 10.3201/eid2908.230750 pubmed: 37352549 pmcid: 10370840
Chabuka, L. et al. Genomic epidemiology of the cholera outbreak in Malawi 2022–2023. Preprint at medRxiv https://doi.org/10.1101/2023.08.22.23294324 (2023).
Qamar, K. et al. Rise of cholera in Iraq: a rising concern. Ann. Med. Surg. 81, 104355 (2022).
doi: 10.1016/j.amsu.2022.104355
Eneh, S. C. et al. Cholera outbreak in Syria amid humanitarian crisis: the epidemic threat, future health implications, and response strategy—a review. Front. Public Health 11, 1161936 (2023).
doi: 10.3389/fpubh.2023.1161936 pubmed: 37408746 pmcid: 10319003
Weill, F.-X. et al. Genomic insights into the 2016–2017 cholera epidemic in Yemen. Nature 565, 230–233 (2019).
doi: 10.1038/s41586-018-0818-3 pubmed: 30602788 pmcid: 6420076
Kumar, P., Yadav, P., Nema, A., Goel, A. K. & Yadava P. K. Re-emergence of chloramphenicol resistance and associated genetic background in Vibrio cholerae O1. FASEB 31, 907.3–907.3 (2017).
Hoshino, K. et al. Development and evaluation of a multiplex PCR assay for rapid detection of toxigenic Vibrio cholerae O1 and O139. FEMS Immunol. Med. Microbiol. 20, 201–207 (1998).
doi: 10.1111/j.1574-695X.1998.tb01128.x pubmed: 9566491
CLSI M45-ED3. Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria (The Clinical & Laboratory Standards Institute, 2016).
CLSI M100-S30. Performance Standards for Antimicrobial Susceptibility Testing (The Clinical & Laboratory Standards Institute, 2020).
Lefèvre, S. et al. Rapid emergence of extensively drug-resistant Shigella sonnei in France. Nat. Commun. 14, 462 (2023).
doi: 10.1038/s41467-023-36222-8 pubmed: 36709320 pmcid: 9883819
Vaser, R. & Šikić, M. Time- and memory-efficient genome assembly with Raven. Nat. Comput. Sci. 1, 332–336 (2021).
doi: 10.1038/s43588-021-00073-4 pubmed: 38217213
Wick, R. R. & Holt, K. E. Polypolish: short-read polishing of long-read bacterial genome assemblies. PLoS Comput. Biol. 18, e1009802 (2022).
doi: 10.1371/journal.pcbi.1009802 pubmed: 35073327 pmcid: 8812927
Schwengers, O. et al. Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb. Genom. 7, 000685 (2021).
pubmed: 34739369 pmcid: 8743544
Croucher, N. J. et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 43, e15–e15 (2015).
doi: 10.1093/nar/gku1196 pubmed: 25414349
Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
doi: 10.1093/bioinformatics/btl446 pubmed: 16928733
Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).
doi: 10.1093/nar/gkz239 pubmed: 30931475 pmcid: 6602468
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
doi: 10.1089/cmb.2012.0021 pubmed: 22506599 pmcid: 3342519

Auteurs

Antoine Abou Fayad (A)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon.

Rayane Rafei (R)

Laboratoire Microbiologie, Santé et Environnement (LMSE), Doctoral School of Sciences and Technology, Faculty of Public Health, Lebanese University, Tripoli, Lebanon.

Elisabeth Njamkepo (E)

Institut Pasteur, Université Paris Cité, Unité des Bactéries pathogènes entériques, Centre National de Référence des vibrions et du choléra, Paris, F-75015, France.

Jana Ezzeddine (J)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon.

Hadi Hussein (H)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon.

Solara Sinno (S)

World Health Organization, Beirut, Lebanon.

Jose-Rita Gerges (JR)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon.

Sara Barada (S)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon.

Ahmad Sleiman (A)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon.

Moubadda Assi (M)

World Health Organization, Beirut, Lebanon.

Maryo Baakliny (M)

Epidemiological Surveillance Unit, Ministry of Public Health, Beirut, Lebanon.

Lama Hamedeh (L)

Department of Pathology and Laboratory Medicine, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.

Rami Mahfouz (R)

Department of Pathology and Laboratory Medicine, Faculty of Medicine, American University of Beirut, Beirut, Lebanon.

Fouad Dabboussi (F)

Laboratoire Microbiologie, Santé et Environnement (LMSE), Doctoral School of Sciences and Technology, Faculty of Public Health, Lebanese University, Tripoli, Lebanon.

Rita Feghali (R)

Department of Laboratory Medicine, Rafik Hariri University Hospital, Beirut, 2010, Lebanon.

Zeina Mohsen (Z)

Department of Laboratory Medicine, Rafik Hariri University Hospital, Beirut, 2010, Lebanon.

Alisar Rady (A)

World Health Organization, Beirut, Lebanon.

Nada Ghosn (N)

Epidemiological Surveillance Unit, Ministry of Public Health, Beirut, Lebanon.

Firas Abiad (F)

Epidemiological Surveillance Unit, Ministry of Public Health, Beirut, Lebanon.

Abdinasir Abubakar (A)

World Health Organization, Beirut, Lebanon.

Amal Barakat (A)

Infectious Hazard Management, Department of Health Emergency World Health Organisation, Eastern Mediterranean Regional Office Cairo, Cairo, Egypt.

Nadia Wauquier (N)

Cholera Programme, Department of Health Emergency Interventions, World Health Organisation, Geneva, Switzerland.

Marie-Laure Quilici (ML)

Institut Pasteur, Université Paris Cité, Unité des Bactéries pathogènes entériques, Centre National de Référence des vibrions et du choléra, Paris, F-75015, France.

Monzer Hamze (M)

Laboratoire Microbiologie, Santé et Environnement (LMSE), Doctoral School of Sciences and Technology, Faculty of Public Health, Lebanese University, Tripoli, Lebanon. mhamze@monzerhamze.com.

François-Xavier Weill (FX)

Institut Pasteur, Université Paris Cité, Unité des Bactéries pathogènes entériques, Centre National de Référence des vibrions et du choléra, Paris, F-75015, France. francois-xavier.weill@pasteur.fr.

Ghassan M Matar (GM)

Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon. gmatar@aub.edu.lb.
Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon. gmatar@aub.edu.lb.
World Health Organization (WHO) Collaborating Center for Reference and Research on Bacterial Pathogens, Beirut, Lebanon. gmatar@aub.edu.lb.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

[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

Classifications MeSH