1887

Abstract

Campylobacteriosis is the most common cause of acute gastrointestinal bacterial infection in Europe, with most infections linked to the consumption of contaminated food. While previous studies found an increasing rate of antimicrobial resistance (AMR) in spp. over the past decades, the investigation of additional clinical isolates is likely to provide novel insights into the population structure and mechanisms of virulence and drug resistance of this important human pathogen. Therefore, we combined whole-genome sequencing and antimicrobial-susceptibility testing of 340 randomly selected isolates from humans with gastroenteritis, collected in Switzerland over an 18 year period. In our collection, the most common multilocus sequence types (STs) were ST-257 (=44), ST-21 (=36) and ST-50 (=35); the most common clonal complexes (CCs) were CC-21 (=102), CC-257 (=49) and CC-48 (=33). High heterogeneity was observed among STs, with the most abundant STs recurring over the entire study period, while others were observed only sporadically. Source attribution based on ST assigned more than half of the strains to the ‘generalist’ category (=188), 25  % as ‘poultry specialist’ (=83), and only a few to ‘ruminant specialist’ (=11) or ‘wild bird’ origin (=9). The isolates displayed an increased frequency of AMR from 2003 to 2020, with the highest rates of resistance observed for ciprofloxacin and nalidixic acid (49.8 %), followed by tetracycline (36.9 %). Quinolone-resistant isolates carried chromosomal mutations T86I (99.4 %) and T86A (0.6 %), whereas tetracycline-resistant isolates carried ) (79.8 %) or mosaic (20.2 %) genes. A novel chromosomal cassette carrying several resistance genes, including , and (6), and flanked by insertion sequence elements was detected in one isolate. Collectively, our data revealed an increasing prevalence of resistance to quinolones and tetracycline in isolates from Swiss patients over time, linked to clonal expansion of mutants and acquisition of the ) gene. Investigation of source attribution suggests that infections are most likely related to isolates from poultry or generalist backgrounds. These findings are relevant to guide future infection prevention and control strategies.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000941
2023-02-21
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/2/mgen000941.html?itemId=/content/journal/mgen/10.1099/mgen.0.000941&mimeType=html&fmt=ahah

References

  1. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union One Health 2020 zoonoses report. EFSA J 2021; 19:e06406
    [Google Scholar]
  2. Geissler AL, Bustos Carrillo F, Swanson K, Patrick ME, Fullerton KE et al. Increasing Campylobacter infections, outbreaks, and antimicrobial resistance in the United States, 2004-2012. Clin Infect Dis 2017; 65:1624–1631 [View Article]
    [Google Scholar]
  3. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015; 28:687–720 [View Article]
    [Google Scholar]
  4. Luangtongkum T, Jeon B, Han J, Plummer P, Logue CM et al. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol 2009; 4:189–200 [View Article] [PubMed]
    [Google Scholar]
  5. Wei W, Schüpbach G, Held L. Time-series analysis of Campylobacter incidence in Switzerland. Epidemiol Infect 2015; 143:1982–1989 [View Article] [PubMed]
    [Google Scholar]
  6. Yun J, Greiner M, Höller C, Messelhäusser U, Rampp A et al. Association between the ambient temperature and the occurrence of human Salmonella and Campylobacter infections. Sci Rep 2016; 6:28442 [View Article]
    [Google Scholar]
  7. Sibanda N, McKenna A, Richmond A, Ricke SC, Callaway T et al. A review of the effect of management practices on Campylobacter prevalence in poultry farms. Front Microbiol 2018; 9:2002 [View Article]
    [Google Scholar]
  8. Bless PJ, Schmutz C, Suter K, Jost M, Hattendorf J et al. A tradition and an epidemic: determinants of the campylobacteriosis winter peak in Switzerland. Eur J Epidemiol 2014; 29:527–537 [View Article]
    [Google Scholar]
  9. Rosner BM, Gassowski M, Albrecht S, Stark K. Investigating the Campylobacter enteritis winter peak in Germany, 2018/2019. Sci Rep 2021; 11:22902 [View Article]
    [Google Scholar]
  10. Edwards DS, Milne LM, Morrow K, Sheridan P, Verlander NQ et al. Campylobacteriosis outbreak associated with consumption of undercooked chicken liver pâté in the East of England, September 2011: identification of a dose-response risk. Epidemiol Infect 2014; 142:352–357 [View Article] [PubMed]
    [Google Scholar]
  11. 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 [View Article]
    [Google Scholar]
  12. O’Leary MC, Harding O, Fisher L, Cowden J. A continuous common-source outbreak of campylobacteriosis associated with changes to the preparation of chicken liver pâté. Epidemiol Infect 2009; 137:383–388 [View Article]
    [Google Scholar]
  13. Wimalarathna HML, Richardson JF, Lawson AJ, Elson R, Meldrum R et al. Widespread acquisition of antimicrobial resistance among Campylobacter isolates from UK retail poultry and evidence for clonal expansion of resistant lineages. BMC Microbiol 2013; 13:160 [View Article]
    [Google Scholar]
  14. Friis LM, Pin C, Taylor DE, Pearson BM, Wells JM. A role for the tet(O) plasmid in maintaining Campylobacter plasticity. Plasmid 2007; 57:18–28 [View Article] [PubMed]
    [Google Scholar]
  15. Marasini D, Karki AB, Buchheim MA, Fakhr MK. Phylogenetic relatedness among plasmids harbored by Campylobacter jejuni and Campylobacter coli isolated from retail meats. Front Microbiol 2018; 9:2167 [View Article]
    [Google Scholar]
  16. Schmidt-Ott R, Pohl S, Burghard S, Weig M, Gross U. Identification and characterization of a major subgroup of conjugative Campylobacter jejuni plasmids. J Infect 2005; 50:12–21 [View Article] [PubMed]
    [Google Scholar]
  17. Godschalk PCR, Heikema AP, Gilbert M, Komagamine T, Ang CW et al. The crucial role of Campylobacter jejuni genes in anti-ganglioside antibody induction in Guillain-Barre syndrome. J Clin Invest 2004; 114:1659–1665 [View Article] [PubMed]
    [Google Scholar]
  18. Koga M, Gilbert M, Takahashi M, Li J, Koike S et al. Comprehensive analysis of bacterial risk factors for the development of Guillain-Barre syndrome after Campylobacter jejuni enteritis. J Infect Dis 2006; 193:547–555 [View Article] [PubMed]
    [Google Scholar]
  19. Yuki N. Infectious origins of, and molecular mimicry in, Guillain-Barré and Fisher syndromes. Lancet Infect Dis 2001; 1:29–37 [View Article] [PubMed]
    [Google Scholar]
  20. Guirado P, Paytubi S, Miró E, Iglesias-Torrens Y, Navarro F et al. Differential distribution of the wlaN and cgtB genes, associated with Guillain-Barré syndrome, in Campylobacter jejuni isolates from humans, broiler chickens, and wild birds. Microorganisms 2020; 8:325 [View Article]
    [Google Scholar]
  21. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ et al. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 2001; 39:14–23 [View Article] [PubMed]
    [Google Scholar]
  22. Miller WG, On SLW, Wang GL, Fontanoz S, Lastovica AJ et al. Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J Clin Microbiol 2005; 43:2315–2329 [View Article]
    [Google Scholar]
  23. Kelley BR, Ellis JC, Large A, Schneider LG, Jacobson D et al. Whole-genome sequencing and bioinformatic analysis of environmental, agricultural, and human Campylobacter jejuni isolates from East Tennessee. Front Microbiol 2020; 11:571064 [View Article]
    [Google Scholar]
  24. Meistere I, Ķibilds J, Eglīte L, Alksne L, Avsejenko J et al. Campylobacter species prevalence, characterisation of antimicrobial resistance and analysis of whole-genome sequence of isolates from livestock and humans, Latvia, 2008 to 2016. Euro Surveill 2019; 24:1800357 [View Article]
    [Google Scholar]
  25. Revez J, Llarena A-K, Schott T, Kuusi M, Hakkinen M et al. Genome analysis of Campylobacter jejuni strains isolated from a waterborne outbreak. BMC Genomics 2014; 15:768 [View Article]
    [Google Scholar]
  26. Berthenet E, Thépault A, Chemaly M, Rivoal K, Ducournau A et al. Source attribution of Campylobacter jejuni shows variable importance of chicken and ruminants reservoirs in non-invasive and invasive French clinical isolates. Sci Rep 2019; 9:8098 [View Article]
    [Google Scholar]
  27. Woodcock DJ, Krusche P, Strachan NJC, Forbes KJ, Cohan FM et al. Genomic plasticity and rapid host switching can promote the evolution of generalism: a case study in the zoonotic pathogen Campylobacter. Sci Rep 2017; 7:9650 [View Article]
    [Google Scholar]
  28. Seth-Smith HMB, Bonfiglio F, Cuénod A, Reist J, Egli A et al. Evaluation of rapid library preparation protocols for whole genome sequencing based outbreak investigation. Front Public Health 2019; 7:241 [View Article]
    [Google Scholar]
  29. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  30. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
    [Google Scholar]
  31. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  32. Freire B, Ladra S, Parama JR. Memory-efficient assembly using Flye. IEEE/ACM Trans Comput Biol Bioinform 2022; 19:3564–3577 [View Article]
    [Google Scholar]
  33. Wick RR, Holt KE. Polypolish: short-read polishing of long-read bacterial genome assemblies. PLoS Comput Biol 2022; 18:e1009802 [View Article]
    [Google Scholar]
  34. Zimin AV, Salzberg SL. The genome polishing tool POLCA makes fast and accurate corrections in genome assemblies. PLoS Comput Biol 2020; 16:e1007981 [View Article]
    [Google Scholar]
  35. Moser S, Seth-Smith H, Egli A, Kittl S, Overesch G. Campylobacter jejuni from canine and bovine cases of campylobacteriosis express high antimicrobial resistance rates against (fluoro)quinolones and tetracyclines. Pathogens 2020; 9:691 [View Article]
    [Google Scholar]
  36. Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ et al. Validating the AMRFinder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother 2019; 63:e00483-19 [View Article]
    [Google Scholar]
  37. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article] [PubMed]
    [Google Scholar]
  38. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 2017; 45:D566–D573 [View Article] [PubMed]
    [Google Scholar]
  39. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
    [Google Scholar]
  40. 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 [View Article] [PubMed]
    [Google Scholar]
  41. Epping L, Walther B, Piro RM, Knüver M-T, Huber C et al. Genome-wide insights into population structure and host specificity of Campylobacter jejuni. Sci Rep 2021; 11:10358 [View Article]
    [Google Scholar]
  42. Hudson LK, Andershock WE, Yan R, Golwalkar M, M’ikanatha NM et al. Phylogenetic analysis reveals source attribution patterns for Campylobacter spp. in Tennessee and Pennsylvania. Microorganisms 2021; 9:2300 [View Article]
    [Google Scholar]
  43. Peters S, Pascoe B, Wu Z, Bayliss SC, Zeng X et al. Campylobacter jejuni genotypes are associated with post-infection irritable bowel syndrome in humans. Commun Biol 2021; 4:1015 [View Article]
    [Google Scholar]
  44. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  45. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom 2018; 4:e000206 [View Article]
    [Google Scholar]
  46. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  47. 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]
    [Google Scholar]
  48. Price MN, Dehal PS, Arkin AP, Poon AFY. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article]
    [Google Scholar]
  49. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  50. Hadfield J, Croucher NJ, Goater RJ, Abudahab K, Aanensen DM et al. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 2018; 34:292–293 [View Article] [PubMed]
    [Google Scholar]
  51. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis – 10 years on. Nucleic Acids Res 2016; 44:D694–D697 [View Article]
    [Google Scholar]
  52. Robinson L, Liaw J, Omole Z, Xia D, van Vliet AHM et al. Bioinformatic analysis of the Campylobacter jejuni type VI secretion system and effector prediction. Front Microbiol 2021; 12:694824 [View Article]
    [Google Scholar]
  53. Didelot X, Croucher NJ, Bentley SD, Harris SR, Wilson DJ. Bayesian inference of ancestral dates on bacterial phylogenetic trees. Nucleic Acids Res 2018; 46:e134 [View Article] [PubMed]
    [Google Scholar]
  54. Duchêne S, Holt KE, Weill F-X, Le Hello S, Hawkey J et al. Genome-scale rates of evolutionary change in bacteria. Microb Genom 2016; 2:e000094 [View Article]
    [Google Scholar]
  55. Huddleston JP, Raushel FM. Functional characterization of cj1427, a unique ping-pong dehydrogenase responsible for the oxidation of GDP-D-glycero-alpha-D-manno-heptose in Campylobacter jejuni. Biochemistry 2020; 59:1328–1337
    [Google Scholar]
  56. Cody AJ, McCarthy NM, Wimalarathna HL, Colles FM, Clark L et al. A longitudinal 6-year study of the molecular epidemiology of clinical Campylobacter isolates in Oxfordshire, United Kingdom. J Clin Microbiol 2012; 50:3193–3201 [View Article]
    [Google Scholar]
  57. Habib I, Miller WG, Uyttendaele M, Houf K, De Zutter L. Clonal population structure and antimicrobial resistance of Campylobacter jejuni in chicken meat from Belgium. Appl Environ Microbiol 2009; 75:4264–4272 [View Article] [PubMed]
    [Google Scholar]
  58. Sopwith W, Birtles A, Matthews M, Fox A, Gee S et al. Identification of potential environmentally adapted Campylobacter jejuni strain, United Kingdom. Emerg Infect Dis 2008; 14:1769–1773 [View Article]
    [Google Scholar]
  59. Sproston EL, Wimalarathna HML, Sheppard SK. Trends in fluoroquinolone resistance in Campylobacter. Microb Genom 2018; 4:e000198 [View Article]
    [Google Scholar]
  60. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 2017; 15:e05077 [View Article]
    [Google Scholar]
  61. Gibreel A, Taylor DE. Macrolide resistance in Campylobacter jejuni and Campylobacter coli. J Antimicrob Chemother 2006; 58:243–255 [View Article] [PubMed]
    [Google Scholar]
  62. Olkkola S, Juntunen P, Heiska H, Hyytiäinen H, Hänninen M-L. Mutations in the rpsL gene are involved in streptomycin resistance in Campylobacter coli. Microb Drug Resist 2010; 16:105–110 [View Article] [PubMed]
    [Google Scholar]
  63. Hormeño L, Ugarte-Ruiz M, Palomo G, Borge C, Florez-Cuadrado D et al. ant(6)-I genes encoding aminoglycoside O-nucleotidyltransferases are widely spread among streptomycin resistant strains of Campylobacter jejuni and Campylobacter coli. Front Microbiol 2018; 9:2515 [View Article]
    [Google Scholar]
  64. Gibreel A, Sköld O, Taylor DE. Characterization of plasmid-mediated aphA-3 kanamycin resistance in Campylobacter jejuni. Microb Drug Resist 2004; 10:98–105 [View Article] [PubMed]
    [Google Scholar]
  65. Liu D, Li X, Liu W, Yao H, Liu Z et al. Characterization of multiresistance gene cfr(C) variants in Campylobacter from China. J Antimicrob Chemother 2019; 74:2166–2170 [View Article] [PubMed]
    [Google Scholar]
  66. Jain D, Prasad KN, Sinha S, Husain N. Differences in virulence attributes between cytolethal distending toxin positive and negative Campylobacter jejuni strains. J Med Microbiol 2008; 57:267–272 [View Article] [PubMed]
    [Google Scholar]
  67. Johansson C, Nilsson A, Kaden R, Rautelin H. Differences in virulence gene expression between human blood and stool Campylobacter coli clade 1 ST828CC isolates. Gut Pathog 2019; 11:42 [View Article]
    [Google Scholar]
  68. Bacon DJ, Alm RA, Burr DH, Hu L, Kopecko DJ et al. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 2000; 68:4384–4390 [View Article] [PubMed]
    [Google Scholar]
  69. Louwen RPL, van Belkum A, Wagenaar JA, Doorduyn Y, Achterberg R et al. Lack of association between the presence of the pVir plasmid and bloody diarrhea in Campylobacter jejuni enteritis. J Clin Microbiol 2006; 44:1867–1868 [View Article] [PubMed]
    [Google Scholar]
  70. Ellström P, Hansson I, Nilsson A, Rautelin H, Olsson Engvall E. Lipooligosaccharide locus classes and putative virulence genes among chicken and human Campylobacter jejuni isolates. BMC Microbiol 2016; 16:116 [View Article]
    [Google Scholar]
  71. Harrison D, Corry JEL, Tchórzewska MA, Morris VK, Hutchison ML. Freezing as an intervention to reduce the numbers of campylobacters isolated from chicken livers. Lett Appl Microbiol 2013; 57:206–213 [View Article] [PubMed]
    [Google Scholar]
  72. Rokney A, Valinsky L, Moran-Gilad J, Vranckx K, Agmon V et al. Genomic epidemiology of Campylobacter jejuni transmission in Israel. Front Microbiol 2018; 9:2432 [View Article]
    [Google Scholar]
  73. Gripp E, Hlahla D, Didelot X, Kops F, Maurischat S et al. Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 2011; 12:584 [View Article] [PubMed]
    [Google Scholar]
  74. Ragimbeau C, Colin S, Devaux A, Decruyenaere F, Cauchie H-M et al. Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A. BMC Microbiol 2014; 14:205 [View Article] [PubMed]
    [Google Scholar]
  75. Sheppard SK, Colles F, Richardson J, Cody AJ, Elson R et al. Host association of Campylobacter genotypes transcends geographic variation. Appl Environ Microbiol 2010; 76:5269–5277 [View Article] [PubMed]
    [Google Scholar]
  76. Sheppard SK, Colles FM, McCarthy ND, Strachan NJC, Ogden ID et al. Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Mol Ecol 2011; 20:3484–3490 [View Article] [PubMed]
    [Google Scholar]
  77. Crofts AA, Poly FM, Ewing CP, Kuroiwa JM, Rimmer JE et al. Campylobacter jejuni transcriptional and genetic adaptation during human infection. Nat Microbiol 2018; 3:494–502 [View Article] [PubMed]
    [Google Scholar]
  78. Thépault A, Méric G, Rivoal K, Pascoe B, Mageiros L et al. Genome-wide identification of host-segregating epidemiological markers for source attribution in Campylobacter jejuni. Appl Environ Microbiol 2017; 83:e03085-16 [View Article]
    [Google Scholar]
  79. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.000941
Loading
/content/journal/mgen/10.1099/mgen.0.000941
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF

Supplementary material 4

EXCEL
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