1887

Microbial Genomics logo

Volume 8, Issue 9

Emerging patterns of fluoroquinolone resistance in in the UK [1998–2018] Open Access

Abstract

( is the most common causative agent of bacterial food poisoning worldwide and is known to be genetically highly diverse. is increasingly resistant to fluoroquinolone antibiotics, but very few studies have investigated variant-specific patterns of resistance across time. Here we use statistical modelling and clustering techniques to investigate patterns of fluoroquinolone resistance amongst 10,359 UK isolates from human disease sampled over 20 years. We observed six distinct patterns of fluoroquinolone sensitivity/resistance in across time, grouping by clonal complex (CC). Some CCs were fully resistant, some shifted from susceptible to resistant following a sigmoidal shape, and some remained susceptible over time. Our findings indicate that the fluoroquinolone resistance patterns of are complicated and cannot be analysed as a single species but divided into variant dynamics so that the factors driving resistance can be thoroughly investigated.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial resistance , Campylobacter jejuni , clonal complex , fluoroquinolones , Generalised Linear Model , Multi-locus sequence typing and statistical modelling
Funding
This study was supported by the:
  • Food Standards Agency (Award FS101013 Oracle: DDT0006Z AT01.07)
    • Principle Award Recipient: DessislavaVeltcheva
  • Biotechnology and Biological Sciences Research Council (Award BB/M011224/1)
    • Principle Award Recipient: DessislavaVeltcheva
© 2022 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.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000875
2022-09-26
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/9/mgen000875.html?itemId=/content/journal/mgen/10.1099/mgen.0.000875&mimeType=html&fmt=ahah

References

  1. 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]
     [Google Scholar]
  2. Igwaran A, Okoh AI. Human campylobacteriosis: a public health concern of global importance. Heliyon 2019; 5:e02814 [View Article]
     [Google Scholar]
  3. Tam CC, O’Brien SJ. Economic Cost of Campylobacter, Norovirus and Rotavirus Disease in the United Kingdom. PLoS ONE 2016; 11:e0138526 [View Article] [PubMed]
     [Google Scholar]
  4. Sheppard SK, Maiden MCJ. The evolution of Campylobacter jejuni and Campylobacter coli. Cold Spring Harb Perspect Biol 2015; 7:a018119 [View Article]
     [Google Scholar]
  5. Goddard MR, O’Brien S, Williams N, Guitian J, Grant A et al. A restatement of the natural science evidence base regarding the source, spread and control of Campylobacter species causing human disease. Proc Biol Sci 2022; 289:20220400 [View Article] [PubMed]
     [Google Scholar]
  6. Zhou S-M, Lyons RA, Rahman MA, Holborow A, Brophy S. Predicting hospital readmission for campylobacteriosis from electronic health records: a machine learning and text mining perspective. J Pers Med 2022; 12:86 [View Article] [PubMed]
     [Google Scholar]
  7. Heredia N, García S. Animals as sources of food-borne pathogens: A review. Anim Nutr 2018; 4:250–255 [View Article] [PubMed]
     [Google Scholar]
  8. Yahara K, Méric G, Taylor AJ, de Vries SPW, Murray S et al. Genome-wide association of functional traits linked with Campylobacter jejuni survival from farm to fork. Environ Microbiol 2017; 19:361–380 [View Article] [PubMed]
     [Google Scholar]
  9. Jorgensen F et al. Survey report. A Microbiological survey of campylobacter contamination in fresh whole UK produced chilled chickens at retail sale (2014-15); 2015
  10. Wensley A, Padfield S, Hughes GJ. An outbreak of campylobacteriosis at a hotel in England: the ongoing risk due to consumption of chicken liver dishes. Epidemiol Infect 2020; 148:e32 [View Article] [PubMed]
     [Google Scholar]
  11. Same RG, Tamma PD. ‘Campylobacter infections in children’, pediatrics in review. NIH Public Access 2018; 39:533 [View Article]
     [Google Scholar]
  12. 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]
  13. Tacconelli E et al. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics; 2017 http://www.cdc.gov/drugresistance/threat-report-2013/ accessed 5 April 2022
  14. Food Standards Agency Enhanced Molecular-Based Surveillance and Source Attribution of Campylobacter Infections in the UK 2021 [View Article]
     [Google Scholar]
  15. Sproston EL, Wimalarathna HML, Sheppard SK. Trends in fluoroquinolone resistance in Campylobacter. Microb Genom 2018; 4: [View Article] [PubMed]
     [Google Scholar]
  16. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18:318–327 [View Article] [PubMed]
     [Google Scholar]
  17. Wieczorek K, Osek J. Antimicrobial resistance mechanisms among Campylobacter. Biomed Res Int 2013; 2013:12 [View Article] [PubMed]
     [Google Scholar]
  18. 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]
     [Google Scholar]
  19. Skarp CPA, Hänninen ML, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 2016; 22:103–109 [View Article] [PubMed]
     [Google Scholar]
  20. Dingle KE, Colles FM, Ure R, Wagenaar JA, Duim B et al. Molecular characterization of Campylobacter jejuni clones: A basis for epidemiologic investigation. Emerg Infect Dis 2002; 8:949–955 [View Article] [PubMed]
     [Google Scholar]
  21. 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]
     [Google Scholar]
  22. Kovač J, Čadež N, Stessl B, Stingl K, Gruntar I et al. High genetic similarity of ciprofloxacin-resistant Campylobacter jejuni in central Europe. Front Microbiol 2015; 6:1169 [View Article] [PubMed]
     [Google Scholar]
  23. van Vliet AHM, Thakur S, Prada JM, Mehat JW, La Ragione RM. Genomic screening of antimicrobial resistance markers in UK and US Campylobacter Isolates highlights stability of resistance over an 18-year period. Antimicrob Agents Chemother 2022; 66:e0168721 [View Article] [PubMed]
     [Google Scholar]
  24. 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] [PubMed]
     [Google Scholar]
  25. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  26. Madeira F, Park YM, Lee J, Buso N, Gur T et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 2019; 47:W636–W641 [View Article]
     [Google Scholar]
  27. Han J, Wang Y, Sahin O, Shen Z, Guo B et al. A fluoroquinolone resistance associated mutation in gyrA affects DNA supercoiling in Campylobacter jejuni. Front Cell Infect Microbiol 2012; 2:21 [View Article]
     [Google Scholar]
  28. Team, R. C R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020 https://www.r-project.org/ accessed 19 April 2022
  29. Haldenby S, Bronowski C, Nelson C, Kenny J, Martinez-Rodriguez C et al. Increasing prevalence of a fluoroquinolone resistance mutation amongst Campylobacter jejuni isolates from four human infectious intestinal disease studies in the United Kingdom. PLoS ONE 2020; 15:e0227535 [View Article] [PubMed]
     [Google Scholar]
  30. Cobo-Díaz JF, González del Río P, Álvarez-Ordóñez A. Whole resistome analysis in Campylobacter jejuni and C. coli genomes available in public repositories. Front Microbiol 2021; 12:1155 [View Article]
     [Google Scholar]
  31. 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] [PubMed]
     [Google Scholar]
  32. Cody AJ, Clarke L, Bowler ICJW, Dingle KE. Ciprofloxacin-resistant campylobacteriosis in the UK. Lancet 2010; 376:1987 [View Article] [PubMed]
     [Google Scholar]
  33. Arning N, Sheppard SK, Bayliss S, Clifton DA, Wilson DJ. Machine learning to predict the source of campylobacteriosis using whole genome data. PLoS Genet 2021; 17:10 [View Article] [PubMed]
     [Google Scholar]
  34. Mourkas E, Yahara K, Bayliss SC, Calland JK, Johansson H et al. Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter. Microbiology 2021 [View Article]
     [Google Scholar]
  35. Dearlove BL, Cody AJ, Pascoe B, Méric G, Wilson DJ et al. Rapid host switching in generalist Campylobacter strains erodes the signal for tracing human infections. ISME J 2016; 10:721–729 [View Article] [PubMed]
     [Google Scholar]
  36. Colles FM, Jones TA, McCarthy ND, Sheppard SK, Cody AJ et al. Campylobacter infection of broiler chickens in a free-range environment. Environ Microbiol 2008; 10:2042–2050 [View Article] [PubMed]
     [Google Scholar]
  37. Calland JK, Pascoe B, Bayliss SC, Mourkas E, Berthenet E et al. Quantifying bacterial evolution in the wild: a birthday problem for Campylobacter lineages. PLOS Genet 2021; 17:e1009829 [View Article]
     [Google Scholar]
  38. Cody AJ, Colles FM et al. Where does campylobacter come from? A molecular odyssey’, advances in experimental medicine and biology. Europe PMC Funders 2010; 659:47 [View Article]
     [Google Scholar]
  39. Pascoe B, Méric G, Yahara K, Wimalarathna H, Murray S et al. Local genes for local bacteria: Evidence of allopatry in the genomes of transatlantic Campylobacter populations. Mol Ecol 2017; 26:4497–4508 [View Article]
     [Google Scholar]
  40. Mäesaar M, Meremäe K, Ivanova M, Roasto M. Antimicrobial resistance and multilocus sequence types of Campylobacter jejuni isolated from Baltic broiler chicken meat and Estonian human patients. Poult Sci 2018; 97:3645–3651 [View Article]
     [Google Scholar]
  41. European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J 2018; 16:e05500 [View Article] [PubMed]
     [Google Scholar]
  42. García-Fernández A, Dionisi AM, Arena S, Iglesias-Torrens Y, Carattoli A et al. Human Campylobacteriosis in Italy: emergence of multi-drug resistance to Ciprofloxacin, Tetracycline, and Erythromycin. Front Microbiol 2018; 9:1906 [View Article]
     [Google Scholar]
  43. Luber P, Wagner J, Hahn H, Bartelt E. Antimicrobial resistance in Campylobacter jejuni and Campylobacter coli strains isolated in 1991 and 2001-2002 from poultry and humans in Berlin, Germany. Antimicrob Agents Chemother 2003; 47:3825–3830 [View Article]
     [Google Scholar]
  44. Tenhagen B-A, Flor M, Alt K, Knüver M-T, Buhler C et al. Association of antimicrobial resistance in Campylobacter spp. in Broilers and Turkeys with antimicrobial use. Antibiotics (Basel) 2021; 10:673 [View Article] [PubMed]
     [Google Scholar]
  45. Zawack K, Li M, Booth JG, Love W, Lanzas C et al. Monitoring antimicrobial resistance in the food supply chain and its implications for FDA policy initiatives. Antimicrob Agents Chemother 2016; 60:5302–5311 [View Article] [PubMed]
     [Google Scholar]
  46. Centers for Disease Control Antibiotic Resistance Threats in the United States, 2019 2019 [View Article]
     [Google Scholar]
  47. Rodrigues JA, Cha W, Mosci RE, Mukherjee S, Newton DW et al. Epidemiologic Associations Vary Between Tetracycline and Fluoroquinolone Resistant Campylobacter jejuni Infections. Front Public Health 2021; 9:820 [View Article]
     [Google Scholar]
  48. Pollett S, Rocha C, Zerpa R, Patiño L, Valencia A et al. Campylobacter antimicrobial resistance in Peru: a ten-year observational study. BMC Infect Dis 2012; 12:193 [View Article]
     [Google Scholar]
  49. Wallace RL, Bulach DM, Jennison AV, Valcanis M, McLure A et al. Molecular characterization of Campylobacter spp. recovered from beef, chicken, lamb and pork products at retail in Australia. PLOS ONE 2020; 15:e0236889 [View Article] [PubMed]
     [Google Scholar]
  50. Abraham S, Sahibzada S, Hewson K, Laird T, Abraham R et al. Emergence of fluoroquinolone-resistant Campylobacter jejuni and Campylobacter coli among Australian chickens in the absence of fluoroquinolone use. Appl Environ Microbiol 2020; 86:e02765-19 [View Article]
     [Google Scholar]
  51. Humphrey TJ, Jørgensen F, Frost JA, Wadda H, Domingue G et al. Prevalence and subtypes of ciprofloxacin-resistant Campylobacter spp. in commercial poultry flocks before, during, and after treatment with fluoroquinolones. Antimicrob AGENTS Chemother 2005; 49:690–698 [View Article] [PubMed]
     [Google Scholar]
  52. Yang Y, Feye KM, Shi Z, Pavlidis HO, Kogut M et al. A historical review on antibiotic resistance of foodborne Campylobacter. Front Microbiol 2019; 10:1509 [View Article] [PubMed]
     [Google Scholar]
  53. 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; 9:1–13 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000875
Loading
Emerging patterns of fluoroquinolone resistance in Campylobacter jejuni in the UK [1998–2018]
M Gen 8, 000875 (2022); https://doi.org/10.1099/mgen.0.000875
/content/journal/mgen/10.1099/mgen.0.000875
/content/journal/mgen/10.1099/mgen.0.000875
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

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