1887

Microbial Genomics logo

Volume 10, Issue 1

Genomic epidemiology of the clinically dominant clonal complex 1 in the population in the UK Open Access

Abstract

is a food-borne pathogen, typically affecting the elderly, immunocompromised patients and pregnant women. The aim of this study was to determine the population structure of clonal complex 1 (CC1) in the UK and describe the genomic epidemiology of this clinically significant CC. We interrogated a working dataset of 4073 sequences of isolated between January 2015 and December 2020 from human clinical specimens, food and/or food-production environments. A minimum spanning tree was reconstructed to determine the population structure of in the UK. Subsequent analysis focused on CC1, as the cause of the highest proportion of invasive listeriosis in humans. Sequencing data was integrated with metadata on food and environmental isolates, and information from patient questionnaires, including age, sex and clinical outcomes. All isolates either belonged to lineage I (=1299/4073, 32%) or lineage II (=2774/4073, 68%), with clinical isolates from human cases more likely to belong to lineage I (=546/928, 59%) and food isolates more likely to belong to lineage II (=2352/3067, 77%). Of the four largest CCs, CC1 (=237) had the highest proportion of isolates from human cases of disease (CC1 =160/237, 67.5 %; CC121 =13/843, 2 %; CC9 =53/360, 15 %; CC2 =69/339, 20%). Within CC1, most cases were female (=95/160, 59%, =0.01771) and the highest proportion of cases were in people >60 years old (39/95, 41%, =1.314×10) with a high number of them aged 20–39 years old (=35/95, 37%) most linked to pregnancy-related listeriosis (=29/35, 83%). Most of the male cases were in men aged over 60 years old (40/65, 62%), and most of the fatal cases in both males and females were identified in this age group (42/55, 76%). Phylogenetic analysis revealed 23 5 SNP single linkage clusters comprising 80/237 (34 %) isolates with cluster sizes ranging from 2 to 19. Five 5 SNP clusters comprised isolates from human cases and an implicated food item. Expanding the analysis to 25 SNP single linkage clusters resolved an additional two clusters linking human cases to a potential food vehicle. Analysis of demographic and clinical outcome data identified CC1 as a clinically significant cause of invasive listeriosis in the elderly population and in women of child-bearing age. Phylogenetic analysis revealed the population structure of CC1 in the UK comprised small, sparsely populated genomic clusters. Only clusters containing isolates from an implicated food vehicle, or food processing or farming environments, were resolved, emphasizing the need for clinical, food and animal-health agencies to share sequencing data in real time, and the importance of a One Health approach to public-health surveillance of listeriosis.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bioinformatics , data analysis , foodborne pathogens , Listeria monocytogenes , surveillance and whole-genome sequencing
Funding
This study was supported by the:
  • National Institute for Health Research Health Protection Research Unit (Award 111815)
    • Principle Award Recipient: ClaireJenkins
© 2024 Crown Copyright
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001155
2024-01-02
2024-04-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/1/mgen001155.html?itemId=/content/journal/mgen/10.1099/mgen.0.001155&mimeType=html&fmt=ahah

References

  1. Quereda JJ, Leclercq A, Moura A, Vales G, Gómez-Martín Á et al. Listeria valentina sp. nov., isolated from a water trough and the faeces of healthy sheep. Int J Syst Evol Microbiol 2020; 70:5868–5879 [View Article] [PubMed]
     [Google Scholar]
  2. Barbuddhe SB, Rawool DB, Doijad SP, Vergis J, Malik SS et al. Ecology of Listeria monocytogenes and Listeria species in India: the occurrence, resistance to biocides, genomic landscape and biocontrol. Environ Microbiol 2022; 24:2759–2780 [View Article] [PubMed]
     [Google Scholar]
  3. Raufu IA, Moura A, Vales G, Ahmed OA, Aremu A et al. Listeria ilorinensis sp. nov., isolated from cow milk cheese in Nigeria. Int J Syst Evol Microbiol 2022; 72:005437 [View Article] [PubMed]
     [Google Scholar]
  4. Carlin CR, Liao J, Weller D, Guo X, Orsi R et al. Listeria cossartiae sp. nov., Listeria immobilis sp. nov., Listeria portnoyi sp. nov. and Listeria rustica sp. nov., isolated from agricultural water and natural environments. Int J Syst Evol Microbiol 2021; 71:004795 [View Article]
     [Google Scholar]
  5. Weis J, Seeliger HPR. Incidence of Listeria monocytogenes in nature. Appl Microbiol 1975; 30:29–32 [View Article] [PubMed]
     [Google Scholar]
  6. Guillet C, Join-Lambert O, Le Monnier A, Leclercq A, Mechaï F et al. Human listeriosis caused by Listeria ivanovii. Emerg Infect Dis 2010; 16:136–138 [View Article] [PubMed]
     [Google Scholar]
  7. Thakur M, Asrani RK, Patial V. Listeria monocytogenes: a food-borne pathogen. In Foodborne Diseases New York: Elsevier; 2018
     [Google Scholar]
  8. Lorber B. Listeria monocytogenes and listeriosis; 2013 www.infectiousdiseaseadvisor.com
  9. Awofisayo A, Amar C, Ruggles R, Elson R, Adak GK et al. Pregnancy-associated listeriosis in England and Wales. Epidemiol Infect 2015; 143:249–256 [View Article] [PubMed]
     [Google Scholar]
  10. Steven Doerr F, Cunha JP. Listeria (listeriosis); 2021 https://www.emedicinehealth.com/listeria_monocytogenes_infection/article_em.htm accessed 26 October 2021
  11. Linnan MJ, Mascola L, Lou XD, Goulet V, May S et al. Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med 1988; 319:823–828 [View Article]
     [Google Scholar]
  12. Goulet V, King LA, Vaillant V, de Valk H. What is the incubation period for listeriosis?. BMC Infect Dis 2013; 13:11 [View Article] [PubMed]
     [Google Scholar]
  13. Angelo KM, Jackson KA, Wong KK, Hoekstra RM, Jackson BR. Assessment of the incubation period for invasive listeriosis. Clin Infect Dis 2016; 63:1487–1489 [View Article] [PubMed]
     [Google Scholar]
  14. WHO Listeriosis; 2018 https://www.who.int/news-room/fact-sheets/detail/listeriosis
  15. FDA Get the facts about Listeria; 2020 https://www.fda.gov/animal-veterinary/animal-health-literacy/get-facts-about-listeria
  16. UK Health Security Agency Listeriosis in England and Wales: Summary for 2020; 2022 https://www.gov.uk/government/publications/listeria-monocytogenes-surveillance-reports/listeriosis-in-england-and-wales-summary-for-2020 accessed 24 October 2022
  17. Seeliger HPR, Höhne K. Serotyping of Listeria monocytogenes and related species. Methods Microbiol 1979; 13:31–49 [View Article]
     [Google Scholar]
  18. Ranjbar R, Halaji M. Epidemiology of Listeria monocytogenes prevalence in foods, animals and human origin from Iran: a systematic review and meta-analysis. BMC Public Health 2018; 18:1057 [View Article] [PubMed]
     [Google Scholar]
  19. Pirone-Davies C, Chen Y, Pightling A, Ryan G, Wang Y et al. Genes significantly associated with lineage II food isolates of Listeria monocytogenes. BMC Genomics 2018; 19:708 [View Article] [PubMed]
     [Google Scholar]
  20. Painset A, Björkman JT, Kiil K, Guillier L, Mariet J-F et al. LiSEQ – whole-genome sequencing of a cross-sectional survey of Listeria monocytogenes in ready-to-eat foods and human clinical cases in Europe. Microb Genom 2019; 5:e000257 [View Article] [PubMed]
     [Google Scholar]
  21. Piffaretti JC, Kressebuch H, Aeschbacher M, Bille J, Bannerman E et al. Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. Proc Natl Acad Sci USA 1989; 86:3818–3822 [View Article] [PubMed]
     [Google Scholar]
  22. Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY et al. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol 2016; 54:333–342 [View Article] [PubMed]
     [Google Scholar]
  23. Laksanalamai P, Huang B, Sabo J, Burall LS, Zhao S et al. Genomic characterization of novel Listeria monocytogenes serotype 4b variant strains. PLoS One 2014; 9:e89024 [View Article] [PubMed]
     [Google Scholar]
  24. Maiden MCJ, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 2013; 11:728–736 [View Article] [PubMed]
     [Google Scholar]
  25. Moura A, Lefrancq N, Wirth T, Leclercq A, Borges V et al. Emergence and global spread of Listeria monocytogenes main clinical clonal complex. Sci Adv 2021; 7:eabj9805 [View Article] [PubMed]
     [Google Scholar]
  26. Toledo V, den Bakker HC, Hormazábal JC, González-Rocha G, Bello-Toledo H et al. Genomic diversity of Listeria monocytogenes isolated from clinical and non-clinical samples in Chile. Genes 2018; 9:396 [View Article] [PubMed]
     [Google Scholar]
  27. Hilliard A, Leong D, O’Callaghan A, Culligan EP, Morgan CA et al. Genomic characterization of Listeria monocytogenes isolates associated with clinical listeriosis and the food production environment in Ireland. Genes 2018; 9:171 [View Article] [PubMed]
     [Google Scholar]
  28. Rivas L, Paine S, Dupont P-Y, Tiong A, Horn B et al. Genome typing and epidemiology of human listeriosis in New Zealand, 1999 to 2018. J Clin Microbiol 2021; 59:e0084921 [View Article] [PubMed]
     [Google Scholar]
  29. Maury MM, Tsai Y-H, Charlier C, Touchon M, Chenal-Francisque V et al. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet 2016; 48:308–313 [View Article] [PubMed]
     [Google Scholar]
  30. Quereda JJ, Morón-García A, Palacios-Gorba C, Dessaux C, García-Del Portillo F et al. Pathogenicity and virulence of Listeria monocytogenes: a trip from environmental to medical microbiology. Virulence 2021; 12:2509–2545 [View Article] [PubMed]
     [Google Scholar]
  31. Public Health England The Health Protection (Notification) Regulations 2010; 2010 https://www.legislation.gov.uk/uksi/2010/659/made accessed 20 February 2023
  32. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008; 4:e1000146 [View Article] [PubMed]
     [Google Scholar]
  33. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ 2016; 4:e2308 [View Article]
     [Google Scholar]
  34. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article]
     [Google Scholar]
  35. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [View Article] [PubMed]
     [Google Scholar]
  36. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. Corrigendum to: IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:2461 [View Article] [PubMed]
     [Google Scholar]
  37. Dallman T, Ashton P, Schafer U, Jironkin A, Painset A et al. SnapperDB: a database solution for routine sequencing analysis of bacterial isolates. Bioinformatics 2018; 34:3028–3029 [View Article] [PubMed]
     [Google Scholar]
  38. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
     [Google Scholar]
  39. Guidi F, Chiaverini A, Repetto A, Lorenzetti C, Centorotola G et al. Hyper-virulent Listeria monocytogenes strains associated with respiratory infections in central Italy. Front Cell Infect Microbiol 2021; 11:765540 [View Article] [PubMed]
     [Google Scholar]
  40. Cotter PD, Draper LA, Lawton EM, Daly KM, Groeger DS et al. Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog 2008; 4:e1000144 [View Article] [PubMed]
     [Google Scholar]
  41. Disson O, Moura A, Lecuit M. Making sense of the biodiversity and virulence of Listeria monocytogenes. Trends Microbiol 2021; 29:811–822 [View Article] [PubMed]
     [Google Scholar]
  42. Morgand M, Leclercq A, Maury MM, Bracq-Dieye H, Thouvenot P et al. Listeria monocytogenes-associated respiratory infections: a study of 38 consecutive cases. Clin Microbiol Infect 2018; 24:1339 [View Article] [PubMed]
     [Google Scholar]
  43. Patas K, Mavridis T, Psarra K, Papadopoulos VE, Mandilara G et al. Neurolisteriosis in a previously asymptomatic patient with serum IgM deficiency: a case report. BMC Neurol 2020; 20:323 [View Article] [PubMed]
     [Google Scholar]
  44. Charlier C, Poirée S, Delavaud C, Khoury G, Richaud C et al. Imaging of human neurolisteriosis: a prospective study of 71 cases. Clin Infect Dis 2018; 67:1419–1426 [View Article] [PubMed]
     [Google Scholar]
  45. Koopmans MM, Engelen-Lee J, Brouwer MC, Jaspers V, Man WK et al. Characterization of a Listeria monocytogenes meningitis mouse model. J Neuroinflammation 2018; 15:257 [View Article] [PubMed]
     [Google Scholar]
  46. Charlier C, Kermorvant-Duchemin E, Perrodeau E, Moura A, Maury MM et al. Neonatal listeriosis presentation and outcome: a prospective study of 189 cases. Clin Infect Dis 2022; 74:8–16 [View Article] [PubMed]
     [Google Scholar]
  47. ECDC Listeriosis Annual Epidemiological Report for 2021 Stockholm: European Centre for Disease Prevention and Control; 2021
     [Google Scholar]
  48. Pohl AM, Pouillot R, Bazaco MC, Wolpert BJ, Healy JM et al. Differences among incidence rates of invasive listeriosis in the U.S. FoodNet population by age, sex, race/ethnicity, and pregnancy status, 2008–2016. Foodborne Pathog Dis 2019; 16:290–297 [View Article] [PubMed]
     [Google Scholar]
  49. Public Health England Listeriosis in England and Wales: Summary for 2018; 2018 https://www.gov.uk/government/publications/listeria-monocytogenes-surveillance-reports/listeriosis-in-england-and-wales-summary-for-2018 accessed 9 July 2021
  50. Public Health England Listeria cases being investigated; 2019 https://www.gov.uk/government/news/listeria-cases-being-investigated accessed 12 July 2021
  51. Dreyer M, Aguilar-Bultet L, Rupp S, Guldimann C, Stephan R et al. Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis. Sci Rep 2016; 6:36419 [View Article] [PubMed]
     [Google Scholar]
  52. Papić B, Pate M, Félix B, Kušar D. Genetic diversity of Listeria monocytogenes strains in ruminant abortion and rhombencephalitis cases in comparison with the natural environment. BMC Microbiol 2019; 19:299 [View Article] [PubMed]
     [Google Scholar]
  53. Public Health England Listeriosis in England and Wales: Summary for 2019; 2019 https://www.gov.uk/government/publications/listeria-monocytogenes-surveillance-reports/listeriosis-in-england-and-wales-summary-for-2019
  54. Charlier C, Disson O, Lecuit M. Maternal-neonatal listeriosis. Virulence 2020; 11:391–397 [View Article] [PubMed]
     [Google Scholar]
  55. Chattaway MA, Chandra N, Painset A, Shah V, Lamb P et al. Genomic approaches used to investigate an atypical outbreak of Salmonella Adjame. Microb Genom 2019; 5:e000248 [View Article] [PubMed]
     [Google Scholar]
  56. Dallman TJ, Greig DR, Gharbia SE, Jenkins C. Phylogenetic structure of Shiga toxin-producing Escherichia coli O157:H7 from sub-lineage to SNPs. Microb Genom 2021; 7:e000544 [View Article] [PubMed]
     [Google Scholar]
  57. Sherdley R. Potentially deadly bug was found at butchers and was traced back to ‘potted beef; 2022 https://www.nottinghampost.com/news/local-news/potentially-deadly-bug-found-butchers-6703874
  58. Food Safety News Former butcher fined after Listeria outbreak link; his family now running shop; Food Safety News; 2022
  59. Maury MM, Bracq-Dieye H, Huang L, Vales G, Lavina M et al. Author Correction: Hypervirulent Listeria monocytogenes clones’ adaptation to mammalian gut accounts for their association with dairy products. Nat Commun 2019; 10:3619 [View Article] [PubMed]
     [Google Scholar]
  60. Cantinelli T, Chenal-Francisque V, Diancourt L, Frezal L, Leclercq A et al. “Epidemic clones” of Listeria monocytogenes are widespread and ancient clonal groups. J Clin Microbiol 2013; 51:3770–3779 [View Article] [PubMed]
     [Google Scholar]
  61. Palacios-Gorba C, Moura A, Gomis J, Leclercq A, Gómez-Martín Á et al. Ruminant-associated Listeria monocytogenes isolates belong preferentially to dairy-associated hypervirulent clones: a longitudinal study in 19 farms. Environ Microbiol 2021; 23:7617–7631 [View Article] [PubMed]
     [Google Scholar]
  62. Steckler AJ, Cardenas-Alvarez MX, Townsend Ramsett MK, Dyer N, Bergholz TM. Genetic characterization of Listeria monocytogenes from ruminant listeriosis from different geographical regions in the U.S. Vet Microbiol 2018; 215:93–97 [View Article] [PubMed]
     [Google Scholar]
  63. de Valk H, Vaillant V, Jacquet C, Rocourt J, Le Querrec F et al. Two consecutive nationwide outbreaks of listeriosis in France, October 1999–February 2000. Am J Epidemiol 2001; 154:944–950 [View Article] [PubMed]
     [Google Scholar]
  64. Leong D, Alvarez-Ordóñez A, Jordan K. Monitoring occurrence and persistence of Listeria monocytogenes in foods and food processing environments in the Republic of Ireland. Front Microbiol 2014; 5:436 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001155
Loading
Genomic epidemiology of the clinically dominant clonal complex 1 in the Listeria monocytogenes population in the UK
M Gen 10, 001155 (2024); https://doi.org/10.1099/mgen.0.001155
/content/journal/mgen/10.1099/mgen.0.001155
/content/journal/mgen/10.1099/mgen.0.001155
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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