1887

Abstract

Members of the genus Campylobacter remain a leading cause of bacterial gastroenteritis worldwide. Infection is usually self-limiting but in severe cases may require antibiotic treatment. In a recent statement by the World Health Organization (WHO) Campylobacter was named as one of the 12 bacteria that pose the greatest threat to human health because they are resistant to antibiotics. In this mini review we describe recent trends in fluoroquinolone (FQ) (particularly ciprofloxacin) resistance in strains of members of the genus Campylobacter isolated from livestock and clinical samples from several countries. Using evidence from phenotyping surveys and putative resistance prediction from DNA sequence data, we discuss the acquisition and spread of FQ resistance and the role of horizontal gene transfer and describe trends in FQ-resistance in samples from livestock and clinical cases. This review emphasises that FQ resistance remains common among isolates of members of the genus Campylobacter from various sources.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000198
2018-07-19
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/mgen/4/8/mgen000198.html?itemId=/content/journal/mgen/10.1099/mgen.0.000198&mimeType=html&fmt=ahah

References

  1. Humphrey T, O'Brien S, Madsen M. Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 2007; 117:237–257 [View Article][PubMed]
    [Google Scholar]
  2. Blaser MJ, Engberg J. Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In Nachamkin I, Szymanski CM, Blaser MJ. (editors) Campylobacter Washington, DC: ASM Press; 2008 pp. 99–121
    [Google Scholar]
  3. Sheppard SK, Dallas JF, MacRae M, McCarthy ND, Sproston EL et al. Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. Int J Food Microbiol 2009; 134:96–103 [View Article][PubMed]
    [Google Scholar]
  4. NARMS Integrated Report 2014; The National Antimicrobial Resistance Monitoring System: Enteric Bacteria. www.fda.gov/downloads/animalveterinary/safetyhealth/antimicrobialresistance/nationalantimicrobialresistancemonitoringsystem/ucm528861.pdf [accessed December 2017]
  5. Wieczorek K, Osek J. Antimicrobial resistance mechanisms among Campylobacter. Biomed Res Int 2013; 2013:1–12
    [Google Scholar]
  6. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014. EFSA J 2016; 14:1–207
    [Google Scholar]
  7. Rossi M, Olkkola S, Roasto M, Kivistö R, Hänninen M et al. Chapter 4: Antimicrobial resistance and Campylobacter jejuni and C. coli. In Chen C, Yan X, Jackson CR. (editors) Antimicrobial Resistance and Food Safety: Methods and Techniques Amsterdam, Netherlands: Elsevier/Academic Press; 2015 pp. 55–75
    [Google Scholar]
  8. Guerrant RL, van Gilder T, Steiner TS, Thielman NM, Slutsker L et al. Infectious Diseases Society of America: practice guidelines for the management of infectious diarrhea. Clin Infect Dis 2001; 32:331–351
    [Google Scholar]
  9. Gupta A, Nelson JM, Barrett TJ, Tauxe RV, Rossiter SP et al. Antimicrobial resistance among Campylobacter strains, United States, 1997–2001. Emerg Infect Dis 2004; 10:1102–1109 [View Article][PubMed]
    [Google Scholar]
  10. Ge B, Wang F, Sjölund-Karlsson M, McDermott PF. Antimicrobial resistance in campylobacter: susceptibility testing methods and resistance trends. J Microbiol Methods 2013; 95:57–67 [View Article][PubMed]
    [Google Scholar]
  11. Allos BM. Campylobacter jejuni Infections: update on emerging issues and trends. Clin Infect Dis 2001; 32:1201–1206 [View Article][PubMed]
    [Google Scholar]
  12. Endtz HP, Ruijs GJ, van Klingeren B, Jansen WH, van der Reyden T et al. Quinolone resistance in campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother 1991; 27:199–208 [View Article][PubMed]
    [Google Scholar]
  13. Nelson JM, Chiller TM, Powers JH, Angulo FJ. Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clin Infect Dis 2007; 44:977–980 [View Article][PubMed]
    [Google Scholar]
  14. 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]
  15. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2015. EFSA J 2017; 15:1–212
    [Google Scholar]
  16. PHE (Public Health England) Antimicrobial resistance report for FSA Project FS241044. Forming part of the project: A Microbiological survey of Campylobacter contamination in fresh whole UK produced chilled chickens at retail sale (2014–15); 20161–50 www.food.gov.uk/sites/default/files/media/document/fs241044finreport.pdf [accessed December 2017]
  17. Gaudreau C, Boucher F, Gilbert H, Bekal S. Antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli isolates obtained in Montreal, Quebec, Canada, from 2002 to 2013. J Clin Microbiol 2014; 52:2644–2646 [View Article][PubMed]
    [Google Scholar]
  18. 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]
  19. Regulation (EC) No 1831/2003 of the European parliament and of the council of 22 September 2003 on additives for use in animal nutrition. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32003R1831&from=EN [accessed December 2017]
  20. Castanon JI. History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci 2007; 86:2466–2471 [View Article][PubMed]
    [Google Scholar]
  21. WHO (World Health Organisation) Antimicrobial Resistance: Global Report on Surveillance Geneva, Switzerland: World Health Organization; 2014 pp. 1–232 http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748_eng.pdf?ua=1 [accessed December 2017]
    [Google Scholar]
  22. ECDC (European Centre for Disease Prevention and Control) EU Protocol for Harmonised Monitoring of Antimicrobial Resistance in Human Salmonella and Campylobacter Isolates Technical Document, ECDC; 2016 pp. 1–14 https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/antimicrobial-resistance-Salmonella-Campylobacter-harmonised-monitoring.pdf [accessed May 2018]
    [Google Scholar]
  23. EFSA (European Food Safety Authority) Manual for Reporting on Antimicrobial Resistance Within The framework of Directive 2003/99/EC and Decision 2013/652/EU for Information Deriving from The year 2015 EFSA Supporting Publication; EN990 2016 pp. 1–35 https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/sp.efsa.2016.EN-990 [accessed May 2018]
    [Google Scholar]
  24. Nguyen TN, Hotzel H, Njeru J, Mwituria J, El-Adawy H et al. Antimicrobial resistance of Campylobacter isolates from small scale and backyard chicken in Kenya. Gut Pathog 2016; 8:39 [View Article][PubMed]
    [Google Scholar]
  25. Zhou J, Zhang M, Yang W, Fang Y, Wang G et al. A seventeen-year observation of the antimicrobial susceptibility of clinical Campylobacter jejuni and the molecular mechanisms of erythromycin-resistant isolates in Beijing, China. Int J Infect Dis 2016; 42:28–33 [View Article][PubMed]
    [Google Scholar]
  26. Jacoby GA. Mechanisms of resistance to quinolones. Clin Infect Dis 2005; 41:S120–S126 [View Article][PubMed]
    [Google Scholar]
  27. Smith JL, Fratamico PM. Fluoroquinolone resistance in Campylobacter. J Food Prot 2010; 73:1141–1152 [View Article][PubMed]
    [Google Scholar]
  28. Yang W, Zhang M, Zhou J, Pang L, Wang G et al. The molecular mechanisms of ciprofloxacin resistance in clinical Campylobacter jejuni and their genotyping characteristics in Beijing, China. Foodborne Pathog Dis 2017; 14:386–392 [View Article][PubMed]
    [Google Scholar]
  29. Wang Y, Huang WM, Taylor DE. Cloning and nucleotide sequence of the Campylobacter jejuni gyrA gene and characterization of quinolone resistance mutations. Antimicrob Agents Chemother 1993; 37:457–463 [View Article][PubMed]
    [Google Scholar]
  30. Payot S, Bolla JM, Corcoran D, Fanning S, Mégraud F et al. Mechanisms of fluoroquinolone and macrolide resistance in Campylobacter spp. Microbes Infect 2006; 8:1967–1971 [View Article][PubMed]
    [Google Scholar]
  31. Engberg J, Aarestrup FM, Taylor DE, Gerner-Smidt P, Nachamkin I. Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg Infect Dis 2001; 7:24–34 [View Article][PubMed]
    [Google Scholar]
  32. Yan M, Sahin O, Lin J, Zhang Q. Role of the CmeABC efflux pump in the emergence of fluoroquinolone-resistant Campylobacter under selection pressure. J Antimicrob Chemother 2006; 58:1154–1159 [View Article][PubMed]
    [Google Scholar]
  33. Tang Y, Sahin O, Pavlovic N, Lejeune J, Carlson J et al. Rising fluoroquinolone resistance in Campylobacter isolated from feedlot cattle in the United States. Sci Rep 2017; 7:494 [View Article][PubMed]
    [Google Scholar]
  34. Yao H, Shen Z, Wang Y, Deng F, Liu D et al. Emergence of a potent multidrug efflux pump variant that enhances Campylobacter resistance to multiple antibiotics. MBio 2016; 7:e01543-16 [View Article][PubMed]
    [Google Scholar]
  35. Ge B, McDermott PF, White DG, Meng J. Role of efflux pumps and topoisomerase mutations in fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother 2005; 49:3347–3354 [View Article][PubMed]
    [Google Scholar]
  36. Han J, Sahin O, Barton YW, Zhang Q. Key role of Mfd in the development of fluoroquinolone resistance in Campylobacter jejuni. PLoS Pathog 2008; 4:e1000083 [View Article][PubMed]
    [Google Scholar]
  37. Griggs DJ, Johnson MM, Frost JA, Humphrey T, Jørgensen F et al. Incidence and mechanism of ciprofloxacin resistance in Campylobacter spp. isolated from commercial poultry flocks in the United Kingdom before, during, and after fluoroquinolone treatment. Antimicrob Agents Chemother 2005; 49:699–707 [View Article][PubMed]
    [Google Scholar]
  38. Wimalarathna HM, 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]
  39. 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]
  40. Cha W, Mosci RE, Wengert SL, Venegas Vargas C, Rust SR et al. Comparing the genetic diversity and antimicrobial resistance profiles of Campylobacter jejuni recovered from cattle and humans. Front Microbiol 2017; 8:818 [View Article][PubMed]
    [Google Scholar]
  41. 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]
  42. Kinana AD, Cardinale E, Tall F, Bahsoun I, Sire JM et al. Genetic diversity and quinolone resistance in Campylobacter jejuni isolates from poultry in Senegal. Appl Environ Microbiol 2006; 72:3309–3313 [View Article][PubMed]
    [Google Scholar]
  43. Kittl S, Kuhnert P, Hächler H, Korczak BM. Comparison of genotypes and antibiotic resistance of Campylobacter jejuni isolated from humans and slaughtered chickens in Switzerland. J Appl Microbiol 2011; 110:513–520 [View Article][PubMed]
    [Google Scholar]
  44. 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]
  45. Technical University of Denmark - National Food Institute Comparative Genomics of Quinolone-Resistant and Susceptible Campylobacter Jejuni of Poultry Origin from Major Poultry Producing European Countries (GENCAMP) EFSA supporting publication; EN-1398 2018 pp. 35
    [Google Scholar]
  46. Wang Y, Dong Y, Deng F, Liu D, Yao H et al. Species shift and multidrug resistance of Campylobacter from chicken and swine, China, 2008–14. J Antimicrob Chemother 2016; 71:666–669 [View Article][PubMed]
    [Google Scholar]
  47. Sheppard SK, McCarthy ND, Falush D, Maiden MC. Convergence of Campylobacter species: implications for bacterial evolution. Science 2008; 320:237–239 [View Article][PubMed]
    [Google Scholar]
  48. Sheppard SK, Didelot X, Jolley KA, Darling AE, Pascoe B et al. Progressive genome-wide introgression in agricultural Campylobacter coli. Mol Ecol 2013; 22:1051–1064 [View Article][PubMed]
    [Google Scholar]
  49. Chen Y, Mukherjee S, Hoffmann M, Kotewicz ML, Young S et al. Whole-genome sequencing of gentamicin-resistant Campylobacter coli isolated from U.S. retail meats reveals novel plasmid-mediated aminoglycoside resistance genes. Antimicrob Agents Chemother 2013; 57:5398–5405 [View Article][PubMed]
    [Google Scholar]
  50. Zhao S, Tyson GH, Chen Y, Li C, Mukherjee S et al. Whole-genome sequencing analysis accurately predicts antimicrobial resistance phenotypes in Campylobacter spp. Appl Environ Microbiol 2015; 82:459–466 [View Article][PubMed]
    [Google Scholar]
  51. Ellington MJ, Ekelund O, Aarestrup FM, Canton R, Doumith M et al. The role of whole genome sequencing in antimicrobial susceptibility testing of bacteria: report from the EUCAST subcommittee. Clin Microbiol Infect 2017; 23:2–22 [View Article][PubMed]
    [Google Scholar]
  52. Jolley KA, Maiden MC. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article][PubMed]
    [Google Scholar]
  53. Riley A, Eshaghi A, Olsha R, Allen VG, Patel SN. Antibiotic susceptibility of clinical isolates of Campylobacter jejuni and Campylobacter coli in Ontario, Canada during 2011–2013. Diagn Microbiol Infect Dis 2015; 83:292–294 [View Article][PubMed]
    [Google Scholar]
  54. NARMS Now: Human Data. www.cdc.gov/narmsnow/ [accessed December 2017]
  55. 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][PubMed]
    [Google Scholar]
  56. Sifré E, Salha BA, Ducournau A, Floch P, Chardon H et al. EUCAST recommendations for antimicrobial susceptibility testing applied to the three main Campylobacter species isolated in humans. J Microbiol Methods 2015; 119:206–213 [View Article][PubMed]
    [Google Scholar]
  57. Lluque A, Riveros M, Prada A, Ochoa TJ, Ruiz J. Virulence and antimicrobial resistance in Campylobacter spp. from a Peruvian pediatric cohort. Scientifica 2017; 2017:1–8 [View Article][PubMed]
    [Google Scholar]
  58. Cody AJ, Clarke L, Bowler IC, Dingle KE. Ciprofloxacin-resistant campylobacteriosis in the UK. Lancet 2010; 376:1987 [View Article][PubMed]
    [Google Scholar]
  59. Moore JE, Millar BC, McMahon MA, McDowell DA, Rooney PJ. Antimicrobial resistance in campylobacter isolates from sporadic cases of acute human gastroenteritis in Northern Ireland. Ulster Med J 2009; 78:139[PubMed]
    [Google Scholar]
  60. Karikari AB, Obiri-Danso K, Frimpong EH, Krogfelt KA. Antibiotic resistance of Campylobacter recovered from faeces and carcasses of healthy livestock. Biomed Res Int 2017; 2017:1–9 [View Article][PubMed]
    [Google Scholar]
  61. Zhang T, Dong J, Cheng Y, Lu Q, Luo Q et al. Genotypic diversity, antimicrobial resistance and biofilm-forming abilities of Campylobacter isolated from chicken in Central China. Gut Pathog 2017; 9:62 [View Article][PubMed]
    [Google Scholar]
  62. Pergola S, Franciosini MP, Comitini F, Ciani M, de Luca S et al. Genetic diversity and antimicrobial resistance profiles of Campylobacter coli and Campylobacter jejuni isolated from broiler chicken in farms and at time of slaughter in central Italy. J Appl Microbiol 2017; 122:1348–1356 [View Article][PubMed]
    [Google Scholar]
  63. Szczepanska B, Andrzejewska M, Spica D, Klawe JJ. Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from children and environmental sources in urban and suburban areas. BMC Microbiol 2017; 17:80 [View Article][PubMed]
    [Google Scholar]
  64. Zhang T, Luo Q, Chen Y, Li T, Wen G et al. Molecular epidemiology, virulence determinants and antimicrobial resistance of Campylobacter spreading in retail chicken meat in Central China. Gut Pathog 2016; 8:48 [View Article][PubMed]
    [Google Scholar]
  65. Thanner S, Drissner D, Walsh F. Antimicrobial resistance in agriculture. MBio 2016; 7:e02227-15 [View Article][PubMed]
    [Google Scholar]
  66. Sheppard SK, Dallas JF, Strachan NJ, MacRae M, McCarthy ND et al. Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 2009; 48:1072–1078 [View Article][PubMed]
    [Google Scholar]
  67. Zhao S, Young SR, Tong E, Abbott JW, Womack N et al. Antimicrobial resistance of Campylobacter isolates from retail meat in the United States between 2002 and 2007. Appl Environ Microbiol 2010; 76:7949–7956 [View Article][PubMed]
    [Google Scholar]
  68. FSA (Food Standards Agency) FSA report for the UK survey of Campylobacter and Salmonella contamination of fresh chicken at retail sale. FSA Project B18025 20091–97 http://webarchive.nationalarchives.gov.uk/20140403130456/http://www.foodbase.org.uk/admintools/reportdocuments/351-1-676_B18025.pdf [accessed December 2017]
    [Google Scholar]
  69. Nichols GL, Richardson JF, Sheppard SK, Lane C, Sarran C. Campylobacter epidemiology: a descriptive study reviewing 1 million cases in England and Wales between 1989 and 2011. BMJ Open 2012; 2:e001179 [View Article][PubMed]
    [Google Scholar]
  70. Garcia-Migura L, Hendriksen RS, Fraile L, Aarestrup FM. Antimicrobial resistance of zoonotic and commensal bacteria in Europe: the missing link between consumption and resistance in veterinary medicine. Vet Microbiol 2014; 170:1–9 [View Article][PubMed]
    [Google Scholar]
  71. Melnyk AH, Wong A, Kassen R. The fitness costs of antibiotic resistance mutations. Evol Appl 2015; 8:273–283 [View Article][PubMed]
    [Google Scholar]
  72. Zeitouni S, Kempf I. Fitness cost of fluoroquinolone resistance in Campylobacter coli and Campylobacter jejuni. Microb Drug Resist 2011; 17:171–179 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000198
Loading
/content/journal/mgen/10.1099/mgen.0.000198
Loading

Data & Media loading...

Supplements

Supplementary File 1

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