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Volume 169, Issue 6

Different stages of the infection cycle are enriched for strains with distinct phenotypes and levels of fluoroquinolone resistance Open Access

Abstract

species are the leading cause of bacterial diarrhoea worldwide and consumption of contaminated chicken meat is the most common route of infection. Chickens can be infected with multiple strains of and during the infection cycle this pathogen must survive a wide variety of environments. Numerous studies have reported a high degree of genetic variability in this pathogen that can use antigenic and phase variation to alter the expression of key phenotypes. In this study the phenotypic profile of isolates from freshly slaughtered chickens, chicken products in the supermarket and stool samples from infected patients were compared to identify phenotypic changes during the passage of the bacteria through the infection cycle. Isolates from different stages of the infection cycle had altered phenotypic profiles with isolates from human stool samples showing a lower ability to form a biofilm and an increased ability to associate with epithelial cells . Resistance to fluoroquinolones was found in all cohorts but at a much higher occurrence (94%) in isolates from supermarket chicken. Isolates displaying high levels of resistance to fluoroquinolones also were more likely to display a higher tolerance to growth in the presence of oxygen. In conclusion, isolates with specific phenotypes appear to be overly represented at different stages of the infection cycle suggesting that environmental stresses may be enriched for strains with these phenotypes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): campylobacter , fluoroquinolone resistance and virulence
Funding
This study was supported by the:
  • Irish Research Council for Science, Engineering and Technology (Award GOIPG/2020/823)
    • Principle Award Recipient: GillianCarney
© 2023 The Authors
  • 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.
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2023-06-23
2024-04-27
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References

  1. Young KT, Davis LM, Dirita VJ. Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 2007; 5:665–679 [View Article] [PubMed]
     [Google Scholar]
  2. Elmi A, Nasher F, Dorrell N, Wren B, Gundogdu O. Revisiting Campylobacter jejuni virulence and fitness factors: role in sensing, adapting, and competing. Front Cell Infect Microbiol 2020; 10:607704 [View Article] [PubMed]
     [Google Scholar]
  3. Skarp CPA, Hänninen M-L, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 2016; 22:103–109 [View Article] [PubMed]
     [Google Scholar]
  4. European Food Safety Authority Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008 ‐ Part A: Campylobacter and Salmonella prevalence estimates. EFS2 2010; 8: [View Article]
     [Google Scholar]
  5. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union One Health 2021 Zoonoses Report. EFSA J 2022; 20:e07666 [View Article] [PubMed]
     [Google Scholar]
  6. Lynch H, Franklin-Hayes P, Koolman L, Egan J, Gutierrez M et al. Prevalence and levels of Campylobacter in broiler chicken batches and carcasses in Ireland in 2017-2018. Int J Food Microbiol 2022; 372:109693 [View Article] [PubMed]
     [Google Scholar]
  7. Emanowicz M, Meade J, Bolton D, Golden O, Gutierrez M et al. The impact of key processing stages and flock variables on the prevalence and levels of Campylobacter on broiler carcasses. Food Microbiol 2021; 95:103688 [View Article] [PubMed]
     [Google Scholar]
  8. Park SF. The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol 2002; 74:177–188 [View Article] [PubMed]
     [Google Scholar]
  9. Doyle MP, Roman DJ. Growth and survival of Campylobacter fetus subsp. jejuni as a Function of Temperature and pH. J Food Prot 1981; 44:596–601 [View Article] [PubMed]
     [Google Scholar]
  10. Oh E, McMullen L, Jeon B. High prevalence of hyper-aerotolerant Campylobacter jejuni in retail poultry with potential implication in Human Infection. Front Microbiol 2015; 6:1263 [View Article] [PubMed]
     [Google Scholar]
  11. Oh E, Andrews KJ, McMullen LM, Jeon B. Tolerance to stress conditions associated with food safety in Campylobacter jejuni strains isolated from retail raw chicken. Sci Rep 2019; 9: [View Article]
     [Google Scholar]
  12. Lee H, Lee S, Kim S, Ha J, Lee J et al. The risk of aerotolerant Campylobacter jejuni strains in poultry meat distribution and storage. Microb Pathog 2019; 134:103537 [View Article] [PubMed]
     [Google Scholar]
  13. Sproston EL, Wimalarathna HML, Sheppard SK. Trends in fluoroquinolone resistance in Campylobacter. Microb Genom 2018; 4:e000198 [View Article] [PubMed]
     [Google Scholar]
  14. WHO Prioritization of pathogens to guide discovery, research and development of new antibiotics for drug resistant bacterial infections, including tuberculosis. Geneva Switzerland; 2017
  15. Shen ZQ, Wang Y, Zhang QJ, Shen JZ. Antimicrobial resistance in Campylobacter spp. Microbiol Spectr 2018; 6: [View Article] [PubMed]
     [Google Scholar]
  16. Wieczorek K, Osek J. Antimicrobial resistance mechanisms among Campylobacter. Biomed Res Int 2013; 2013:340605 [View Article] [PubMed]
     [Google Scholar]
  17. Shortt C, Scanlan E, Hilliard A, Cotroneo CE, Bourke B et al. DNA spercoiling regulates the motility of Campylobacter jejuni and is altered by growth in the presence of chicken mucus. mBio 2016; 7:e01227-16 [View Article] [PubMed]
     [Google Scholar]
  18. Scanlan E, Ardill L, Whelan MVX, Shortt C, Nally JE et al. Relaxation of DNA supercoiling leads to increased invasion of epithelial cells and protein secretion by Campylobacter jejuni. Mol Microbiol 2017; 104:92–104 [View Article] [PubMed]
     [Google Scholar]
  19. Whelan MVX, Ardill L, Koide K, Nakajima C, Suzuki Y et al. Acquisition of fluoroquinolone resistance leads to increased biofilm formation and pathogenicity in Campylobacter jejuni. Sci Rep 2019; 9:18216 [View Article] [PubMed]
     [Google Scholar]
  20. Luo N, Pereira S, Sahin O, Lin J, Huang S et al. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc Natl Acad Sci U S A 2005; 102:541–546 [View Article] [PubMed]
     [Google Scholar]
  21. Luo N, Sahin O, Lin J, Michel LO, Zhang QJ. In vivo selection of Campylobacter isolates with high levels of fluoroquinolone resistance associated with gyrA mutations and the function of the CmeABC efflux pump. Antimicrob Agents Chemother 2003; 47:390–394 [View Article] [PubMed]
     [Google Scholar]
  22. Gonzalez I, Grant KA, Richardson PT, Park SF, Collins MD. Specific identification of the enteropathogens Campylobacter jejuni and Campylobacter coli by using a PCR test based on the ceuE gene encoding a putative virulence determinant. J Clin Microbiol 1997; 35:759–763 [View Article] [PubMed]
     [Google Scholar]
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Different stages of the infection cycle are enriched for Campylobacter strains with distinct phenotypes and levels of fluoroquinolone resistance
Microbiology 169, 001349 (2023); https://doi.org/10.1099/mic.0.001349
/content/journal/micro/10.1099/mic.0.001349
/content/journal/micro/10.1099/mic.0.001349
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