Whole-Genome Sequencing to Detect Numerous Campylobacter jejuni Outbreaks and Match Patient Isolates to Sources, Denmark, 2015–2017 (original) (raw)

Abstract

C ampylobacter jejuni is the most frequent cause of bacterial gastroenteritis in industrialized countries worldwide (1,2), including in Denmark, where ≈4,000 Campylobacter infections are reported annually (3). Despite the high notification rates, Campylobacter infections are believed to be highly underdiagnosed (4,5). Denmark's national surveillance system for Campylobacter is based on observation of the number of notified human cases (3); a substantial number of Campylobacter outbreaks may be overlooked because of a lack of routine microbiological typing of isolates. This hypothesis is supported by evidence from a recent study, in which whole-genome sequencing (WGS)-based typing of selected clinical Campylobacter isolates from patients in Denmark identified numerous small outbreak-like clusters (6). This finding suggests that more outbreaks occur in Denmark than the few typically large outbreaks associated with a single event that are detected by the current surveillance system (7-10). To achieve a national surveillance system that will detect ongoing Campylobacter outbreaks in real time, highly discriminatory subtyping of isolates is needed. Thus, we more comprehensively evaluated the frequency of Campylobacter outbreaks among humans in Denmark by using WGS-based typing. To match the clinical isolates with their sources, we compared them with isolates from food and animals, covering the main putative sources of human Campylobacter infections (i.e., contact with or consumption of animals or animal products, primarily contaminated poultry meat). Although Campylobacter infections are primarily foodborne, a recent case-control study in Denmark found that contact with animals and the environment might account for a substantial proportion of domestic infections (11). Several other reported sources of infection include unpasteurized milk, drinking water, bathing water, vegetables, and fruits (1,12-14). WGS offers high-resolution discriminatory subtyping and has been successfully implemented for

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References (35)

  1. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev. 2015;28:687-720. https://doi.org/ 10.1128/CMR.00006-15
  2. European Food Safety Authority/European Centre for Disease Prevention and Control. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal. 2018;16:5500. https://doi.org/10.2903/j.efsa.2018.5500
  3. Kuhn KG, Nielsen EM, Mølbak K, Ethelberg S. Epidemiology of campylobacteriosis in Denmark 2000-2015. Zoonoses Public Health. 2018;65:59-66. https://doi.org/10.1111/ zph.12367
  4. Havelaar AH, Ivarsson S, Löfdahl M, Nauta MJ. Estimating the true incidence of campylobacteriosis and salmonellosis in the European Union, 2009. Epidemiol Infect. 2013:141:293-302.
  5. Haagsma JA, Geenen PL, Ethelberg S, Fetch A, Hansdotter F, Jansen A, et al. Community incidence of pathogen-specific gastroenteritis: reconstructing the surveillance pyramid for seven pathogens in seven European Union member states. Epidemiol Infect. 2013;141:1625-39.
  6. Joensen KG, Kuhn KG, Müller L, Björkman JT, Torpdahl M, Engberg J, et al. Whole-genome sequencing of Campylobacter jejuni isolated from Danish routine human stool samples reveals surprising degree of clustering. Clin Microbiol Infect. 2018;24:201.e5-201.e8. PMID: 28782648
  7. Gubbels S-M, Kuhn KG, Larsson JT, Adelhardt M, Engberg J, Ingildsen P, et al. A waterborne outbreak with a single clone of Campylobacter jejuni in the Danish town of Køge in May 2010. Scand J Infect Dis. 2012;44:586-94.
  8. Kuhn KG, Falkenhorst G, Emborg H-D, Ceper T, Torpdahl M, Krogfelt KA, et al. Epidemiological and serological investigation of a waterborne Campylobacter jejuni outbreak in a Danish town. Epidemiol Infect. 2017;145:701-9.
  9. Harder-Lauridsen NM, Kuhn KG, Erichsen AC, Mølbak K, Ethelberg S. Gastrointestinal illness among triathletes swimming in non-polluted versus polluted seawater affected by heavy rainfall, Denmark, 2010-2011. PLoS One. 2013;8:e78371. https://doi.org/10.1371/journal. pone.0078371
  10. Engberg J, Gerner-Smidt P, Scheutz F, Møller Nielsen E, On SLW, Mølbak K. Water-borne Campylobacter jejuni infection in a Danish town-a 6-week continuous source outbreak. Clin Microbiol Infect. 1998;4:648-56. https://doi. org/10.1111/ j.1469-0691.1998.tb00348.x
  11. Kuhn KG, Nielsen EM, Mølbak K, Ethelberg S. Determinants of sporadic Campylobacter infections in Denmark: a nationwide case-control study among children and young adults. Clin Epidemiol. 2018;10:1695-707. https://doi.org/ 10.2147/CLEP.S177141
  12. Mughini Gras L, Smid JH, Wagenaar JA, de Boer AG, Havelaar AH, Friesema IHM, et al. Risk factors for campylobacteriosis of chicken, ruminant, and environmental origin: a combined case-control and source attribution analysis. PLoS One. 2012;7:e42599. https://doi.org/10.1371/ journal.pone.0042599
  13. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 3, March 2020
  14. Verhoeff-Bakkenes L, Jansen HAPM, in 't Veld PH, Beumer RR, Zwietering MH, van Leusden FM. Consumption of raw vegetables and fruits: a risk factor for Campylobacter infections. Int J Food Microbiol. 2011;144:406-12. https://doi.org/10.1016/j.ijfoodmicro.2010.10.027
  15. Domingues AR, Pires SM, Halasa T, Hald T. Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections. Epidemiol Infect. 2012;140:970-81. https://doi.org/10.1017/ S0950268811002676
  16. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014; 52:1501-10.
  17. Kvistholm Jensen A, Nielsen EM, Björkman JT, Jensen T, Müller L, Persson S, et al. Whole-genome sequencing used to investigate a nationwide outbreak of listeriosis caused by ready-to-eat delicatessen meat, Denmark, 2014. Clin Infect Dis. 2016;63:64-70. https://doi.org/10.1093/cid/ciw192
  18. Revez J, Llarena A-K, Schott T, Kuusi M, Hakkinen M, Kivistö R, et al. Genome analysis of Campylobacter jejuni strains isolated from a waterborne outbreak. BMC Genomics. 2014;15:768. https://doi.org/10.1186/1471-2164-15-768
  19. Revez J, Zhang J, Schott T, Kivistö R, Rossi M, Hänninen M-L. Genomic variation between Campylobacter jejuni isolates associated with milk-borne-disease outbreaks. 2014;52: 2782-6. https://doi.org/10.1128/JCM.00931-14
  20. Lahti E, Löfdahl M, Ågren J, Hansson I, Olsson Engvall E. Confirmation of a campylobacteriosis outbreak associated with chicken liver pâté using PFGE and WGS. Zoonoses Public Health. 2017;64:14-20. PMID: 27334628
  21. Lahti E, Rehn M, Ockborn G, Hansson I, Ågren J, Engvall EO, et al. Outbreak of campylobacteriosis following a dairy farm visit: confirmation by genotyping. Foodborne Pathog Dis.2017;14:326-32. PMID: 28350214
  22. Clark CG, Berry C, Walker M, Petkau A, Barker DOR, Guan C, et al. Genomic insights from whole genome se- quencing of four clonal outbreak Campylobacter jejuni assessed within the global C. jejuni population. BMC Genomics. 2016;17:990. https://doi.org/10.1186/s12864-016-3340-8
  23. Kovanen SM, Kivistö RI, Rossi M, Schott T, Kärkkäinen U-M, Tuuminen T, et al. Multilocus sequence typing (MLST) and whole-genome MLST of Campylobacter jejuni isolates from human infections in three districts during a seasonal peak in Finland. J Clin Microbiol. 2014; 52:4147-54.
  24. Kovanen S, Kivistö R, Llarena A-K, Zhang J, Kärkkäinen U-M, Tuuminen T, et al. Tracing isolates from domestic human Campylobacter jejuni infections to chicken slaughter batches and swimming water using whole-genome multilocus sequence typing. Int J Food Microbiol. 2016;226:53-60. https://doi.org/10.1016/j.ijfoodmicro.2016.03.009
  25. Pires SM, Christensen J. Source attribution of Campylobacter infections in Denmark-technical report [cited 2019 Jul 3].
  26. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018; 3:124. https://doi.org/10.12688/wellcomeopenres.14826.1
  27. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package [cited 2019 May 3]. https://cran.r-project.org/package=vegan
  28. Lake IR, Colón-González FJ, Takkinen J, Rossi M, Sudre B, Dias JG, et al. Exploring Campylobacter seasonality across Europe using The European Surveillance System (TESSy), 2008 to 2016. Euro Surveill. 2019;24. https://doi.org/ 10.2807/1560-7917.ES.2019.24.13.180028
  29. Sheppard SK, Maiden MCJ. The evolution of Campylobacter jejuni and Campylobacter coli. Cold Spring Harb Perspect Biol. 2015;7:a018119. https://doi.org/10.1101/cshperspect. a018119
  30. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A, Tarr C, et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol. 2016;2:16185. https://doi.org/10.1038/ nmicrobiol.2016.185
  31. Pightling AW, Pettengill JB, Luo Y, Baugher JD, Rand H, Strain E; Interpreting whole-genome sequence analyses of foodborne bacteria for regulatory applications and outbreak investigations. Front Microbiol. 2018;10;9:1482.
  32. Gerner-Smidt P, Besser J, Concepción-Acevedo J, Folster JP, Huffman J, Joseph LA, et al. Whole genome sequencing: bridging one-health surveillance of foodborne diseases. Front Public Health. 2019;7:365.
  33. Frost JA, Gillespie IA, O'Brien SJ. Public health implications of Campylobacter outbreaks in England and Wales, 1995-9: epidemiological and microbiological investigations. Epidemiol Infect. 2002; 128:111-8.
  34. Kramer JM, Frost JA, Bolton FJ, Wareing DR. Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. J Food Prot. 2000;63:1654-9. https://doi.org/ 10.4315/0362-028X-63.12.1654
  35. Address for correspondence: Eva M. Nielsen, Statens Serum Institut, Department of Bacteriology, Mycology & Parasitology, Artillerivej 5 Copenhagen 2300, Denmark; email: emn@ssi.dk