1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 36, 05/Sep/2024
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

The number of cholera cases reported to the World Health Organization (WHO) in 2022 was more than double that of 2021. Nine countries of the WHO European Region reported 51 cases of cholera in 2022 vs five reported cases in 2021.

Aim

We aimed to confirm that the O1 isolates reported by WHO European Region countries in 2022 belonged to the seventh pandemic El Tor lineage (7PET). We also studied their virulence, antimicrobial resistance (AMR) determinants and phylogenetic relationships.

Methods

We used microbial genomics to study the 49 O1 isolates recovered from the 51 European cases. We also used > 1,450 publicly available 7PET genomes to provide a global phylogenetic context for these 49 isolates.

Results

All 46 good-quality genomes obtained belonged to the 7PET lineage. All but two isolates belonged to genomic Wave 3 and were grouped within three sub-lineages, one of which, Pre-AFR15, predominated (34/44). This sub-lineage, corresponding to isolates from several countries in Southern Asia, the Middle East and Eastern or Southern Africa, was probably a major contributor to the global upsurge of cholera cases in 2022. No unusual AMR profiles were inferred from analysis of the AMR gene content of the 46 genomes.

Conclusion

Reference laboratories in high-income countries should use whole genome sequencing to assign O1 isolates formally to the 7PET or non-epidemic lineages. Periodic collaborative genomic studies based on isolates from travellers can provide useful information on the circulating strains and their evolution, particularly as concerns AMR.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.36.2400069
2024-09-05
2024-12-12
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.36.2400069
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/36/eurosurv-29-36-5.html?itemId=/content/10.2807/1560-7917.ES.2024.29.36.2400069&mimeType=html&fmt=ahah

References

  1. Clemens JD, Nair GB, Ahmed T, Qadri F, Holmgren J. Cholera. Lancet. 2017;390(10101):1539-49.  https://doi.org/10.1016/S0140-6736(17)30559-7  PMID: 28302312 
  2. Hu D, Liu B, Feng L, Ding P, Guo X, Wang M, et al. Origins of the current seventh cholera pandemic. Proc Natl Acad Sci USA. 2016;113(48):E7730-9.  https://doi.org/10.1073/pnas.1608732113  PMID: 27849586 
  3. World Health Organization (WHO). Weekly Epidemiological Record, 2023, vol. 98, 38. Geneva: WHO; 22 Sep 2023. Available from: https://iris.who.int/bitstream/handle/10665/372986/WER9838-eng-fre.pdf?sequence=1&isAllowed=y
  4. Rouard C, Njamkepo E, Quilici M-L, Weill F-X. Contribution of microbial genomics to cholera epidemiology. C R Biol. 2022;345(1):37-56.  https://doi.org/10.5802/crbiol.77  PMID: 35787619 
  5. Rubin DHF, Zingl FG, Leitner DR, Ternier R, Compere V, Marseille S, et al. Reemergence of Cholera in Haiti. N Engl J Med. 2022;387(25):2387-9.  https://doi.org/10.1056/NEJMc2213908  PMID: 36449726 
  6. Mavian CN, Tagliamonte MS, Alam MT, Sakib SN, Cash MN, Moir M, et al. Ancestral origin and dissemination dynamics of reemerging toxigenic Vibrio cholerae, Haiti. Emerg Infect Dis. 2023;29(10):2072-82.  https://doi.org/10.3201/eid2910.230554  PMID: 37735743 
  7. Lassalle F, Al-Shalali S, Al-Hakimi M, Njamkepo E, Bashir IM, Dorman MJ, et al. Genomic epidemiology reveals multidrug resistant plasmid spread between Vibrio cholerae lineages in Yemen. Nat Microbiol. 2023;8(10):1787-98.  https://doi.org/10.1038/s41564-023-01472-1  PMID: 37770747 
  8. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature. 2011;477(7365):462-5.  https://doi.org/10.1038/nature10392  PMID: 21866102 
  9. Weill F-X, Domman D, Njamkepo E, Tarr C, Rauzier J, Fawal N, et al. Genomic history of the seventh pandemic of cholera in Africa. Science. 2017;358(6364):785-9.  https://doi.org/10.1126/science.aad5901  PMID: 29123067 
  10. Domman D, Quilici M-L, Dorman MJ, Njamkepo E, Mutreja A, Mather AE, et al. Integrated view of Vibrio cholerae in the Americas. Science. 2017;358(6364):789-93.  https://doi.org/10.1126/science.aao2136  PMID: 29123068 
  11. Oprea M, Njamkepo E, Cristea D, Zhukova A, Clark CG, Kravetz AN, et al. The seventh pandemic of cholera in Europe revisited by microbial genomics. Nat Commun. 2020;11(1):5347.  https://doi.org/10.1038/s41467-020-19185-y  PMID: 33093464 
  12. World Health Organization (WHO). Multi-country outbreak of cholera, External situation report number 9. Geneva: WHO; 7 Dec 2023. Available from: https://www.who.int/publications/m/item/multi-country-outbreak-of-cholera--external-situation-report--9---7-december-2023
  13. Global Task Force on Cholera Control (GTFCC). Public heath surveillance for cholera - Guidance document. Geneva: GTFCC; 2024. Available from: https://www.gtfcc.org/wp-content/uploads/2024/04/public-health-surveillance-for-cholera-guidance-document-2024.pdf
  14. Russini V, Giancola ML, Brunetti G, Calbi C, Anzivino E, Nisii C, et al. A cholera case Imported from Bangladesh to Italy: clinico-epidemiological management and molecular characterization in a non-endemic country. Trop Med Infect Dis. 2023;8(5):266.  https://doi.org/10.3390/tropicalmed8050266  PMID: 37235314 
  15. Criscuolo A, Brisse S. AlienTrimmer: a tool to quickly and accurately trim off multiple short contaminant sequences from high-throughput sequencing reads. Genomics. 2013;102(5-6):500-6.  https://doi.org/10.1016/j.ygeno.2013.07.011  PMID: 23912058 
  16. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014;15(3):R46.  https://doi.org/10.1186/gb-2014-15-3-r46  PMID: 24580807 
  17. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-77.  https://doi.org/10.1089/cmb.2012.0021  PMID: 22506599 
  18. Weill F-X, Domman D, Njamkepo E, Almesbahi AA, Naji M, Nasher SS, et al. Genomic insights into the 2016-2017 cholera epidemic in Yemen. Nature. 2019;565(7738):230-3.  https://doi.org/10.1038/s41586-018-0818-3  PMID: 30602788 
  19. Smith AM, Sekwadi P, Erasmus LK, Lee CC, Stroika SG, Ndzabandzaba S, et al. Imported cholera cases, South Africa, 2023. Emerg Infect Dis. 2023;29(8):1687-90.  https://doi.org/10.3201/eid2908.230750  PMID: 37352549 
  20. Klinzing DC, Choi SY, Hasan NA, Matias RR, Tayag E, Geronimo J, et al. Hybrid Vibrio cholerae El Tor lacking SXT identified as the cause of a cholera outbreak in the Philippines. MBio. 2015;6(2):e00047-15.  https://doi.org/10.1128/mBio.00047-15  PMID: 25900650 
  21. Ha S-M, Chalita M, Yang S-J, Yoon S-H, Cho K, Seong WK, et al. Comparative genomic analysis of the 2016 Vibrio cholerae outbreak in South Korea. Front Public Health. 2019;7:228.  https://doi.org/10.3389/fpubh.2019.00228  PMID: 31475130 
  22. Greenhill AR, Mutreja A, Bulach D, Belousoff MJ, Jonduo MH, Collins DA, et al. Wave 2 strains of atypical Vibrio cholerae El Tor caused the 2009-2011 cholera outbreak in Papua New Guinea. Microb Genom. 2019;5(3):e000256.  https://doi.org/10.1099/mgen.0.000256  PMID: 30810520 
  23. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43(3):e15-15.  https://doi.org/10.1093/nar/gku1196  PMID: 25414349 
  24. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688-90.  https://doi.org/10.1093/bioinformatics/btl446  PMID: 16928733 
  25. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47(W1):W256-9.  https://doi.org/10.1093/nar/gkz239  PMID: 30931475 
  26. Hounmanou YMG, Njamkepo E, Rauzier J, Gallandat K, Jeandron A, Kamwiziku G, et al. Genomic Microevolution of Vibrio cholerae O1, Lake Tanganyika Basin, Africa. Emerg Infect Dis. 2023;29(1):149-53.  https://doi.org/10.3201/eid2901.220641  PMID: 36573719 
  27. Abou Fayad A, Rafei R, Njamkepo E, Ezzeddine J, Hussein H, Sinno S, et al. An unusual two-strain cholera outbreak in Lebanon, 2022-2023: a genomic epidemiology study. Nat Commun. 2024;15(1):6963.  https://doi.org/10.1038/s41467-024-51428-0  PMID: 39138238 
  28. Monir MM, Islam MT, Mazumder R, Mondal D, Nahar KS, Sultana M, et al. Genomic attributes of Vibrio cholerae O1 responsible for 2022 massive cholera outbreak in Bangladesh. Nat Commun. 2023;14(1):1154.  https://doi.org/10.1038/s41467-023-36687-7  PMID: 36859426 
  29. World Health Organization (WHO). International Health Regulations. 3rd ed. Geneva: WHO; 2005. Available from: https://iris.who.int/handle/10665/246107
  30. Smith AM, Weill F-X, Njamkepo E, Ngomane HM, Ramalwa N, Sekwadi P, et al. Emergence of Vibrio cholerae O1 sequence type 75, South Africa, 2018-2020. Emerg Infect Dis. 2021;27(11):2927-31.  https://doi.org/10.3201/eid2711.211144  PMID: 34670657 
  31. Satchell KJF, Jones CJ, Wong J, Queen J, Agarwal S, Yildiz FH. Phenotypic analysis reveals that the 2010 Haiti cholera epidemic is linked to a hypervirulent strain. Infect Immun. 2016;84(9):2473-81.  https://doi.org/10.1128/IAI.00189-16  PMID: 27297393 
  32. World Health Organization Regional Office for the Eastern Mediterranean (WHO/Eastern Mediterranean). Epidemic and pandemic-prone diseases: Acute watery diarrhoea/cholera updates (16-31 March 2023). Cairo: WHO; Mar 2023. Available from: https://www.emro.who.int/pandemic-epidemic-diseases/cholera/acutewatery-diarrhoeacholera-updates-1631-march-2023.html
  33. Raza M, Fatima A, Habiba U, Shah HH. Public health implications of severe floods in Pakistan: assessing the devastating impact on health and the economy. Front Environ Sci. 2023;11:1091998.  https://doi.org/10.3389/fenvs.2023.1091998 
  34. Mashe T, Domman D, Tarupiwa A, Manangazira P, Phiri I, Masunda K, et al. Highly resistant cholera outbreak strain in Zimbabwe. N Engl J Med. 2020;383(7):687-9.  https://doi.org/10.1056/NEJMc2004773  PMID: 32786196 
  35. Global Task Force on Cholera Control (GTFCC). Interim Technical Note - Use of antibiotics for the treatment and control of cholera. Geneva: GTFCC; 2022. Available from: https://www.gtfcc.org/wp-content/uploads/2019/10/gtfcc-technical-note-on-use-of-antibiotics-for-the-treatment-of-cholera-1.pdf
Genomic analysis of Vibrio cholerae O1 isolates from cholera cases, Europe, 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Caroline+Rouard&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rouard Caroline</a>, <a href="/search?value1=David+R+Greig&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Greig David R</a>, <a href="/search?value1=Thamida+Tauhid&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tauhid Thamida</a>, <a href="/search?value1=Susann+Dupke&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dupke Susann</a>, <a href="/search?value1=Elisabeth+Njamkepo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Njamkepo Elisabeth</a>, <a href="/search?value1=Ettore+Amato&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Amato Ettore</a>, <a href="/search?value1=Boas+van+der+Putten&option1=author&noRedirect=true" class="nonDisambigAuthorLink">van der Putten Boas</a>, <a href="/search?value1=Umaer+Naseer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Naseer Umaer</a>, <a href="/search?value1=Marion+Blaschitz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Blaschitz Marion</a>, <a href="/search?value1=Georgia+D+Mandilara&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mandilara Georgia D</a>, <a href="/search?value1=James++Cohen+Stuart&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cohen Stuart James </a>, <a href="/search?value1=Alexander+Indra&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Indra Alexander</a>, <a href="/search?value1=Harold+No%C3%ABl&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Noël Harold</a>, <a href="/search?value1=Theologia+Sideroglou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sideroglou Theologia</a>, <a href="/search?value1=Florian+Heger&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Heger Florian</a>, <a href="/search?value1=Maaike+van+den+Beld&option1=author&noRedirect=true" class="nonDisambigAuthorLink">van den Beld Maaike</a>, <a href="/search?value1=Astrid+Louise+Wester&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wester Astrid Louise</a>, <a href="/search?value1=Marie-Laure+Quilici&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Quilici Marie-Laure</a>, <a href="/search?value1=Holger+C+Scholz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Scholz Holger C</a>, <a href="/search?value1=Inga+Fr%C3%B6ding&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fröding Inga</a>, <a href="/search?value1=Claire+Jenkins&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jenkins Claire</a>, <a href="/search?value1=Fran%C3%A7ois-Xavier+Weill&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Weill François-Xavier</a></span>. Genomic analysis of Vibrio cholerae O1 isolates from cholera cases, Europe, 2022. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(36):pii=2400069. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.36.2400069" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.36.2400069</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 31 Jan 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 06 May 2024 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.36.2400069
/content/10.2807/1560-7917.ES.2024.29.36.2400069
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error