Skip to main content
PMC home page
Emerging Infectious Diseases logoLink to Emerging Infectious Diseases
. 2001 Jan-Feb;7(1):24–34. doi: 10.3201/eid0701.010104

Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates.

J Engberg 1, F M Aarestrup 1, D E Taylor 1, P Gerner-Smidt 1, I Nachamkin 1
PMCID: PMC2631682  PMID: 11266291

Abstract

The incidence of human Campylobacter jejuni and C. coli infections has increased markedly in many parts of the world in the last decade as has the number of quinolone-resistant and, to a lesser extent, macrolide-resistant Campylobacter strains causing infections. We review macrolide and quinolone resistance in Campylobacter and track resistance trends in human clinical isolates in relation to use of these agents in food animals. Susceptibility data suggest that erythromycin and other macrolides should remain the drugs of choice in most regions, with systematic surveillance and control measures maintained, but fluoroquinolones may now be of limited use in the empiric treatment of Campylobacter infections in many regions.

Full Text

The Full Text of this article is available as a PDF (105.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aarestrup F. M., Nielsen E. M., Madsen M., Engberg J. Antimicrobial susceptibility patterns of thermophilic Campylobacter spp. from humans, pigs, cattle, and broilers in Denmark. Antimicrob Agents Chemother. 1997 Oct;41(10):2244–2250. doi: 10.1128/aac.41.10.2244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adler-Mosca H., Lüthy-Hottenstein J., Martinetti Lucchini G., Burnens A., Altwegg M. Development of resistance to quinolones in five patients with campylobacteriosis treated with norfloxacin or ciprofloxacin. Eur J Clin Microbiol Infect Dis. 1991 Nov;10(11):953–957. doi: 10.1007/BF02005451. [DOI] [PubMed] [Google Scholar]
  3. Allos B. M., Blaser M. J. Campylobacter jejuni and the expanding spectrum of related infections. Clin Infect Dis. 1995 May;20(5):1092–1101. doi: 10.1093/clinids/20.5.1092. [DOI] [PubMed] [Google Scholar]
  4. Baker C. N. The E-Test and Campylobacter jejuni. Diagn Microbiol Infect Dis. 1992 Jul;15(5):469–472. doi: 10.1016/0732-8893(92)90092-8. [DOI] [PubMed] [Google Scholar]
  5. Berghold Christian, Fürpaß Therasia, Marth Egon. Further increase in ciprofloxacin-resistant Campylobacter jejuni/coli in Styria, Austria. Clin Microbiol Infect. 1999 Jan;5(1):59–60. doi: 10.1111/j.1469-0691.1999.tb00102.x. [DOI] [PubMed] [Google Scholar]
  6. Bowler I. C., Connor M., Lessing M. P., Day D. Quinolone resistance and Campylobacter species. J Antimicrob Chemother. 1996 Aug;38(2):315–315. doi: 10.1093/jac/38.2.315. [DOI] [PubMed] [Google Scholar]
  7. Cabrita J., Rodrigues J., Bragança F., Morgado C., Pires I., Gonçalves A. P. Prevalence, biotypes, plasmid profile and antimicrobial resistance of Campylobacter isolated from wild and domestic animals from northeast Portugal. J Appl Bacteriol. 1992 Oct;73(4):279–285. doi: 10.1111/j.1365-2672.1992.tb04978.x. [DOI] [PubMed] [Google Scholar]
  8. Charvalos E., Tselentis Y., Hamzehpour M. M., Köhler T., Pechere J. C. Evidence for an efflux pump in multidrug-resistant Campylobacter jejuni. Antimicrob Agents Chemother. 1995 Sep;39(9):2019–2022. doi: 10.1128/aac.39.9.2019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chatzipanagiotou S., Papavasiliou E., Malamou-Lada E. Isolation of Campylobacter jejuni strains resistant to nalidixic acid and fluoroquinolones from children with diarrhea in Athens, Greece. Eur J Clin Microbiol Infect Dis. 1993 Jul;12(7):566–568. doi: 10.1007/BF01970969. [DOI] [PubMed] [Google Scholar]
  10. Dowling J., MacCulloch D., Morris A. J. Antimicrobial susceptibility of Campylobacter and Yersinia enterocolitica isolates. N Z Med J. 1998 Jul 24;111(1070):281–281. [PubMed] [Google Scholar]
  11. Dryden M. S., Gabb R. J., Wright S. K. Empirical treatment of severe acute community-acquired gastroenteritis with ciprofloxacin. Clin Infect Dis. 1996 Jun;22(6):1019–1025. doi: 10.1093/clinids/22.6.1019. [DOI] [PubMed] [Google Scholar]
  12. Ellis-Pegler R. B., Hyman L. K., Ingram R. J., McCarthy M. A placebo controlled evaluation of lomefloxacin in the treatment of bacterial diarrhoea in the community. J Antimicrob Chemother. 1995 Jul;36(1):259–263. doi: 10.1093/jac/36.1.259. [DOI] [PubMed] [Google Scholar]
  13. Endtz H. P., Mouton R. P., van der Reyden T., Ruijs G. J., Biever M., van Klingeren B. Fluoroquinolone resistance in Campylobacter spp isolated from human stools and poultry products. Lancet. 1990 Mar 31;335(8692):787–787. doi: 10.1016/0140-6736(90)90897-e. [DOI] [PubMed] [Google Scholar]
  14. Endtz H. P., Ruijs G. J., van Klingeren B., Jansen W. H., van der Reyden T., Mouton R. P. Quinolone resistance in campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother. 1991 Feb;27(2):199–208. doi: 10.1093/jac/27.2.199. [DOI] [PubMed] [Google Scholar]
  15. Engberg Jørgen, Andersen Sigrid, Skov Robert, Aarestrup Frank Møller, Gerner-Smidt Peter. Comparison of two agar dilution methods and three agar diffusion methods, including the Etest, for antibiotic susceptibility testing of thermophilic Campylobacter species. Clin Microbiol Infect. 1999 Sep;5(9):580–584. doi: 10.1111/j.1469-0691.1999.tb00440.x. [DOI] [PubMed] [Google Scholar]
  16. Engberg Jørgen, Gerner-Smidt Peter, Scheutz Flemming, Møller Nielsen Eva, On Stephen Louis William, Mølbak Kåre. Water-borne Campylobacter jejuni infection in a Danish town---a 6-week continuous source outbreak. Clin Microbiol Infect. 1998 Jan;4(11):648–656. doi: 10.1111/j.1469-0691.1998.tb00348.x. [DOI] [PubMed] [Google Scholar]
  17. Feierl G., Pschaid A., Sixl B., Marth E. Increase of ciprofloxacin resistance in Campylobacter species in Styria, Austria. Zentralbl Bakteriol. 1994 Nov;281(4):471–474. doi: 10.1016/s0934-8840(11)80333-6. [DOI] [PubMed] [Google Scholar]
  18. Funke G., Baumann R., Penner J. L., Altwegg M. Development of resistance to macrolide antibiotics in an AIDS patient treated with clarithromycin for Campylobacter jejuni diarrhea. Eur J Clin Microbiol Infect Dis. 1994 Jul;13(7):612–615. doi: 10.1007/BF01971317. [DOI] [PubMed] [Google Scholar]
  19. Gallardo F., Gascón J., Ruiz J., Corachan M., Jimenez de Anta M., Vila J. Campylobacter jejuni as a cause of traveler's diarrhea: clinical features and antimicrobial susceptibility. J Travel Med. 1998 Mar;5(1):23–26. doi: 10.1111/j.1708-8305.1998.tb00451.x. [DOI] [PubMed] [Google Scholar]
  20. Gaudreau C., Gilbert H. Antimicrobial resistance of clinical strains of Campylobacter jejuni subsp. jejuni isolated from 1985 to 1997 in Quebec, Canada. Antimicrob Agents Chemother. 1998 Aug;42(8):2106–2108. doi: 10.1128/aac.42.8.2106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gibreel A., Sjögren E., Kaijser B., Wretlind B., Sköld O. Rapid emergence of high-level resistance to quinolones in Campylobacter jejuni associated with mutational changes in gyrA and parC. Antimicrob Agents Chemother. 1998 Dec;42(12):3276–3278. doi: 10.1128/aac.42.12.3276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gootz T. D., Martin B. A. Characterization of high-level quinolone resistance in Campylobacter jejuni. Antimicrob Agents Chemother. 1991 May;35(5):840–845. doi: 10.1128/aac.35.5.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hirschl A. M., Wolf D., Berger J., Rotter M. L. In vitro susceptibility of Campylobacter jejuni and Campylobacter coli isolated in Austria to erythromycin and ciprofloxacin. Zentralbl Bakteriol. 1990 Apr;272(4):443–447. doi: 10.1016/s0934-8840(11)80045-9. [DOI] [PubMed] [Google Scholar]
  24. Hoge C. W., Gambel J. M., Srijan A., Pitarangsi C., Echeverria P. Trends in antibiotic resistance among diarrheal pathogens isolated in Thailand over 15 years. Clin Infect Dis. 1998 Feb;26(2):341–345. doi: 10.1086/516303. [DOI] [PubMed] [Google Scholar]
  25. Hänninen M. L., Pajarre S., Klossner M. L., Rautelin H. Typing of human Campylobacter jejuni isolates in Finland by pulsed-field gel electrophoresis. J Clin Microbiol. 1998 Jun;36(6):1787–1789. doi: 10.1128/jcm.36.6.1787-1789.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kuschner R. A., Trofa A. F., Thomas R. J., Hoge C. W., Pitarangsi C., Amato S., Olafson R. P., Echeverria P., Sadoff J. C., Taylor D. N. Use of azithromycin for the treatment of Campylobacter enteritis in travelers to Thailand, an area where ciprofloxacin resistance is prevalent. Clin Infect Dis. 1995 Sep;21(3):536–541. doi: 10.1093/clinids/21.3.536. [DOI] [PubMed] [Google Scholar]
  27. Li C. C., Chiu C. H., Wu J. L., Huang Y. C., Lin T. Y. Antimicrobial susceptibilities of Campylobacter jejuni and coli by using E-test in Taiwan. Scand J Infect Dis. 1998;30(1):39–42. doi: 10.1080/003655498750002286. [DOI] [PubMed] [Google Scholar]
  28. Lim Y. S., Tay L. A one-year study of enteric Campylobacter infections in Singapore. J Trop Med Hyg. 1992 Apr;95(2):119–123. [PubMed] [Google Scholar]
  29. Mattila L., Peltola H., Siitonen A., Kyrönseppä H., Simula I., Kataja M. Short-term treatment of traveler's diarrhea with norfloxacin: a double-blind, placebo-controlled study during two seasons. Clin Infect Dis. 1993 Oct;17(4):779–782. doi: 10.1093/clinids/17.4.779. [DOI] [PubMed] [Google Scholar]
  30. Molina J., Casin I., Hausfater P., Giretti E., Welker Y., Decazes J., Garrait V., Lagrange P., Modaï J. Campylobacter infections in HIV-infected patients: clinical and bacteriological features. AIDS. 1995 Aug;9(8):881–885. doi: 10.1097/00002030-199508000-00008. [DOI] [PubMed] [Google Scholar]
  31. Moore J. E., Madden R. H., Kerr J. R., Wilson T. S., Murphy P. G. Erythromycin-resistant thermophilic Campylobacter species isolated from pigs. Vet Rec. 1996 Mar 30;138(13):306–307. doi: 10.1136/vr.138.13.306. [DOI] [PubMed] [Google Scholar]
  32. Murphy G. S., Jr, Echeverria P., Jackson L. R., Arness M. K., LeBron C., Pitarangsi C. Ciprofloxacin- and azithromycin-resistant Campylobacter causing traveler's diarrhea in U.S. troops deployed to Thailand in 1994. Clin Infect Dis. 1996 May;22(5):868–869. doi: 10.1093/clinids/22.5.868. [DOI] [PubMed] [Google Scholar]
  33. Mølbak K., Baggesen D. L., Aarestrup F. M., Ebbesen J. M., Engberg J., Frydendahl K., Gerner-Smidt P., Petersen A. M., Wegener H. C. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype typhimurium DT104. N Engl J Med. 1999 Nov 4;341(19):1420–1425. doi: 10.1056/NEJM199911043411902. [DOI] [PubMed] [Google Scholar]
  34. Navarro F., Miró E., Mirelis B., Prats G. Campylobacter spp antibiotic susceptibility. J Antimicrob Chemother. 1993 Dec;32(6):906–907. doi: 10.1093/jac/32.6.906. [DOI] [PubMed] [Google Scholar]
  35. Nielsen E. M., Engberg J., Madsen M. Distribution of serotypes of Campylobacter jejuni and C. coli from Danish patients, poultry, cattle and swine. FEMS Immunol Med Microbiol. 1997 Sep;19(1):47–56. doi: 10.1111/j.1574-695X.1997.tb01071.x. [DOI] [PubMed] [Google Scholar]
  36. Nielsen E. M., Nielsen N. L. Serotypes and typability of Campylobacter jejuni and Campylobacter coli isolated from poultry products. Int J Food Microbiol. 1999 Feb 18;46(3):199–205. doi: 10.1016/s0168-1605(98)00194-9. [DOI] [PubMed] [Google Scholar]
  37. On S. L., Nielsen E. M., Engberg J., Madsen M. Validity of SmaI-defined genotypes of Campylobacter jejuni examined by SalI, KpnI, and BamHI polymorphisms: evidence of identical clones infecting humans, poultry, and cattle. Epidemiol Infect. 1998 Jun;120(3):231–237. doi: 10.1017/s0950268898008668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Orr K. E., Lightfoot N. F., Sisson P. R., Harkis B. A., Tweddle J. L., Boyd P., Carroll A., Jackson C. J., Wareing D. R., Freeman R. Direct milk excretion of Campylobacter jejuni in a dairy cow causing cases of human enteritis. Epidemiol Infect. 1995 Feb;114(1):15–24. doi: 10.1017/s0950268800051876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Owen R. J., Leeton S. Restriction fragment length polymorphism analysis of the flaA gene of Campylobacter jejuni for subtyping human, animal and poultry isolates. FEMS Microbiol Lett. 1999 Jul 15;176(2):345–350. doi: 10.1111/j.1574-6968.1999.tb13682.x. [DOI] [PubMed] [Google Scholar]
  40. Pearson A. D., Greenwood M. H., Donaldson J., Healing T. D., Jones D. M., Shahamat M., Feltham R. K., Colwell R. R. Continuous source outbreak of campylobacteriosis traced to chicken. J Food Prot. 2000 Mar;63(3):309–314. doi: 10.4315/0362-028x-63.3.309. [DOI] [PubMed] [Google Scholar]
  41. Perez-Trallero E., Urbieta M., Lopategui C. L., Zigorraga C., Ayestaran I. Antibiotics in veterinary medicine and public health. Lancet. 1993 Nov 27;342(8883):1371–1372. doi: 10.1016/0140-6736(93)92285-2. [DOI] [PubMed] [Google Scholar]
  42. Piddock L. J. Quinolone resistance and Campylobacter spp. J Antimicrob Chemother. 1995 Dec;36(6):891–898. doi: 10.1093/jac/36.6.891. [DOI] [PubMed] [Google Scholar]
  43. Rautelin H., Renkonen O. V., Kosunen T. U. Emergence of fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli in subjects from Finland. Antimicrob Agents Chemother. 1991 Oct;35(10):2065–2069. doi: 10.1128/aac.35.10.2065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Reina J., Borrell N., Serra A. Emergence of resistance to erythromycin and fluoroquinolones in thermotolerant Campylobacter strains isolated from feces 1987-1991. Eur J Clin Microbiol Infect Dis. 1992 Dec;11(12):1163–1166. doi: 10.1007/BF01961137. [DOI] [PubMed] [Google Scholar]
  45. Reina J. Resistance to fluoroquinolones in Salmonella non-typhi and Campylobacter spp. Lancet. 1992 Oct 24;340(8826):1035–1036. doi: 10.1016/0140-6736(92)93046-p. [DOI] [PubMed] [Google Scholar]
  46. Reina J., Ros M. J., Serra A. Susceptibilities to 10 antimicrobial agents of 1,220 Campylobacter strains isolated from 1987 to 1993 from feces of pediatric patients. Antimicrob Agents Chemother. 1994 Dec;38(12):2917–2920. doi: 10.1128/aac.38.12.2917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Ruiz J., Goñi P., Marco F., Gallardo F., Mirelis B., Jimenez De Anta T., Vila J. Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyrA gene mutations in quinolone-resistant clinical isolates. Microbiol Immunol. 1998;42(3):223–226. doi: 10.1111/j.1348-0421.1998.tb02274.x. [DOI] [PubMed] [Google Scholar]
  48. Sam W. I., Lyons M. M., Waghorn D. J. Increasing rates of ciprofloxacin resistant campylobacter. J Clin Pathol. 1999 Sep;52(9):709–709. doi: 10.1136/jcp.52.9.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Segreti J., Gootz T. D., Goodman L. J., Parkhurst G. W., Quinn J. P., Martin B. A., Trenholme G. M. High-level quinolone resistance in clinical isolates of Campylobacter jejuni. J Infect Dis. 1992 Apr;165(4):667–670. doi: 10.1093/infdis/165.4.667. [DOI] [PubMed] [Google Scholar]
  50. Shah P. M., Schäfer V., Knothe H. Medical and veterinary use of antimicrobial agents: implications for public health. A clinician's view on antimicrobial resistance. Vet Microbiol. 1993 Jun;35(3-4):269–274. doi: 10.1016/0378-1135(93)90151-v. [DOI] [PubMed] [Google Scholar]
  51. Sjögren E., Kaijser B., Werner M. Antimicrobial susceptibilities of Campylobacter jejuni and Campylobacter coli isolated in Sweden: a 10-year follow-up report. Antimicrob Agents Chemother. 1992 Dec;36(12):2847–2849. doi: 10.1128/aac.36.12.2847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Sjögren E., Lindblom G. B., Kaijser B. Norfloxacin resistance in Campylobacter jejuni and Campylobacter coli isolates from Swedish patients. J Antimicrob Chemother. 1997 Aug;40(2):257–261. doi: 10.1093/jac/40.2.257. [DOI] [PubMed] [Google Scholar]
  53. Smith K. E., Besser J. M., Hedberg C. W., Leano F. T., Bender J. B., Wicklund J. H., Johnson B. P., Moore K. A., Osterholm M. T. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. Investigation Team. N Engl J Med. 1999 May 20;340(20):1525–1532. doi: 10.1056/NEJM199905203402001. [DOI] [PubMed] [Google Scholar]
  54. Sáenz Y., Zarazaga M., Lantero M., Gastanares M. J., Baquero F., Torres C. Antibiotic resistance in Campylobacter strains isolated from animals, foods, and humans in Spain in 1997-1998. Antimicrob Agents Chemother. 2000 Feb;44(2):267–271. doi: 10.1128/aac.44.2.267-271.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Sánchez R., Fernández-Baca V., Díaz M. D., Muñoz P., Rodríguez-Créixems M., Bouza E. Evolution of susceptibilities of Campylobacter spp. to quinolones and macrolides. Antimicrob Agents Chemother. 1994 Sep;38(9):1879–1882. doi: 10.1128/aac.38.9.1879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Taylor D. E., Ge Z., Purych D., Lo T., Hiratsuka K. Cloning and sequence analysis of two copies of a 23S rRNA gene from Helicobacter pylori and association of clarithromycin resistance with 23S rRNA mutations. Antimicrob Agents Chemother. 1997 Dec;41(12):2621–2628. doi: 10.1128/aac.41.12.2621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tee W., Mijch A. Campylobacter jejuni bacteremia in human immunodeficiency virus (HIV)-infected and non-HIV-infected patients: comparison of clinical features and review. Clin Infect Dis. 1998 Jan;26(1):91–96. doi: 10.1086/516263. [DOI] [PubMed] [Google Scholar]
  58. Tee W., Mijch A., Wright E., Yung A. Emergence of multidrug resistance in Campylobacter jejuni isolates from three patients infected with human immunodeficiency virus. Clin Infect Dis. 1995 Sep;21(3):634–638. doi: 10.1093/clinids/21.3.634. [DOI] [PubMed] [Google Scholar]
  59. Threlfall E. John, Ward Linda R., Rowe Bernard. Resistance to ciprofloxacin in non-typhoidal salmonellas from humans in England and Wales-the current situation. Clin Microbiol Infect. 1999 Mar;5(3):130–134. doi: 10.1111/j.1469-0691.1999.tb00525.x. [DOI] [PubMed] [Google Scholar]
  60. Varga J., Fodor L. Biochemical characteristics, serogroup distribution, antibiotic susceptibility and age-related significance of Campylobacter strains causing diarrhoea in humans in Hungary. Zentralbl Bakteriol. 1998 Jul;288(1):67–73. doi: 10.1016/s0934-8840(98)80101-1. [DOI] [PubMed] [Google Scholar]
  61. Wang Y., Huang W. M., Taylor D. E. Cloning and nucleotide sequence of the Campylobacter jejuni gyrA gene and characterization of quinolone resistance mutations. Antimicrob Agents Chemother. 1993 Mar;37(3):457–463. doi: 10.1128/aac.37.3.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Wiström J., Norrby S. R. Fluoroquinolones and bacterial enteritis, when and for whom? J Antimicrob Chemother. 1995 Jul;36(1):23–39. doi: 10.1093/jac/36.1.23. [DOI] [PubMed] [Google Scholar]
  63. Yan W., Taylor D. E. Characterization of erythromycin resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother. 1991 Oct;35(10):1989–1996. doi: 10.1128/aac.35.10.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Emerging Infectious Diseases are provided here courtesy of Centers for Disease Control and Prevention

RESOURCES