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Volume 7, Number 1—February 2001
Synopsis

Quinolone and Macrolide Resistance in Campylobacter jejuni and C. coli: Resistance Mechanisms and Trends in Human Isolates

Jørgen Engberg*Comments to Author , Frank M. Aarestrup†, Diane E. Taylor‡, Peter Gerner-Smidt*, and Irving Nachamkin§
Author affiliations: *Statens Serum Institut, Copenhagen, Denmark; †Frank Aarestrup, Danish Veterinary Laboratory, Copenhagen, Denmark; ‡Diane E. Taylor, University of Alberta, Edmonton, Alberta, Canada; §Irving Nachamkin, University of Pennsylvania, Philadelphia, Pennsylvania, USA

Main Article

Figure 2

Trends for quinolone resistance rates (in percentages) among Campylobacter coli and C. jejuni combined from human sources around the world. The bars represent both nalidixic acid and fluoroquinolone resistance and are based on mean values of resistance from numerous reports (9,17,24,27,39,43,56-58,61-64,72-75,78,88, plus pers. comm. from Feirel G and Rautelin H, and unpub. data from Nachamkin I.).

Figure 2. Trends for quinolone resistance rates (in percentages) among Campylobacter coli and C. jejuni combined from human sources around the world. The bars represent both nalidixic acid and fluoroquinolone resistance and are based on mean values of resistance from numerous reports (9,17,24,27,39,43,56-58,61-64,72-75,78,88, plus pers. comm. from Feirel G and Rautelin H, and unpub. data from Nachamkin I.).

Main Article

References
  1. Tauxe  RV. Nachamkin I, Blaser MJ, Tompkins LS, editors. Campylobacter jejuni: current status and future trends. Washington: American Society for Microbiology; 1992. p. 9-19.
  2. Blaser  MJ, Mandell  GL, Bennett  JE, Dolin  R, eds. Principles and practice of infectious diseases. 4th ed. New York: Churchill Livingstone Inc.;1995. p. 1948-56.
  3. Allos  BM, Blaser  MJ. Campylobacter jejuni and the expanding spectrum of related infections. Clin Infect Dis. 1995;20:1092–9.PubMedGoogle Scholar
  4. Dryden  MS, Gabb  RJ, Wright  SK. Empirical treatment of severe acute community-acquired gastroenteritis with ciprofloxacin. Clin Infect Dis. 1996;22:1019–25.PubMedGoogle Scholar
  5. Skirrow  MB, Blaser  MJ. Blaser MJ, Smith PD, Ravdin JI, Greenberg HB et al., editors. Infections of gastrointestinal tract. New York: Raven Press; 1995. p. 825-48.
  6. Wistrom  J, Norrby  SR. Fluoroquinolones and bacterial enteritis, when and for whom? J Antimicrob Chemother. 1995;36:23–39. DOIPubMedGoogle Scholar
  7. Piddock  LJ. Quinolone resistance and Campylobacter spp. J Antimicrob Chemother. 1995;36:891–8. DOIPubMedGoogle Scholar
  8. 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;10:953–7. DOIPubMedGoogle Scholar
  9. Endtz  HP, Ruijs  GJ, van Klingeren  B, Jansen  WH, van der Reyden  T, Mouton  RP. Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother. 1991;27:199–208. DOIPubMedGoogle Scholar
  10. Smith  KE, Besser  JM, Hedberg  CW, Leano  FT, Bender  JB, Wicklund  JH, Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. N Engl J Med. 1999;340:1525–32. DOIPubMedGoogle Scholar
  11. Prescott  JF, Baggot  JD. Antimicrobial therapy in veterinary medicine. 2nd ed. Ames (IA): Iowa State University Press; 1993.
  12. Taylor  DE. In: Nachamkin I, Blaser MJ, Tompkins LS, editors. Campylobacter jejuni - current status and future trends. Washington: American Society for Microbiology; 1992. p. 74-86.
  13. Yan  W, Taylor  DE. Characterization of erythromycin resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother. 1991;35:1989–96.PubMedGoogle Scholar
  14. Taylor  DE, 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;41:2621–8.PubMedGoogle Scholar
  15. Trieber  CA, Taylor  DE. In: Mobley HLT, Nachamkin I, McGee D, editors. Abstracts and final program of the 10th International Workshop on Campylobacter, Helicobacter and Rlated Oganisms. Baltimore: University of Maryland School of Medicine; 1999; Abstract CA6. p. 3.
  16. 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;37:457–63.PubMedGoogle Scholar
  17. Ruiz  J, Goni  P, Marco  F, Gallardo  F, Mirelis  B, Jimenez De Anta  T, Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyrA gene mutations in quinolone-resistant clinical isolates. Microbiol Immunol. 1998;42:223–6.PubMedGoogle Scholar
  18. 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;42:3276–8.PubMedGoogle Scholar
  19. Gootz  TD, Martin  BA. Characterization of high-level quinolone resistance in Campylobacter jejuni. Antimicrob Agents Chemother. 1991;35:840–5.PubMedGoogle Scholar
  20. Charvalos  E, Tselentis  Y, Hamzehpour  MM, Köhler  T, Pechere  J-C. Evidence for an efflux pump im multidrug-resistant Campylobacter jejuni. Antimicrob Agents Chemother. 1995;39:2019–22.PubMedGoogle Scholar
  21. van Diest  J, de Jong  A. Overview of quinolone usage for food-producing animals. In: Use of quinolones in food animals and potential impact on human health. Report and proceedings of a WHO meeting. Geneva: World Health Organization; 1999. p.97.
  22. Antibiotic resistance in the European Union associated with therapeutic use of veterinary medicines. Report and qualitative risk assessment by the committee for veterinary medical products. London: The European Agency for the Evaluation of Medical Products; 1999.
  23. Jacobs Reitsma  WF, Kan  CA, Bolder  NM. The induction of quinolone resistance in Campylobacter in broilers by quinolone treatment. Lett Appl Microbiol. 1994; 19228–31.
  24. Aarestrup  FM, Nielsen  EM, Madsen  M, Engberg  J. Antimicrobial susceptibility patterns of thermophilic Campylobacter spp. from humans, pigs, cattle, and broilers in Denmark. Antimicrob Agents Chemother. 1997;41:2244–50.PubMedGoogle Scholar
  25. Bager  F, ed. Danmap 98 - Consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Copenhagen, Denmark: Danish Zoonosis Centre; 1999. p.3.
  26. Cabrita  J, Rodriguez  J, Braganca  F, Morgado  C, Pires  I, Penha Goncalves  A. Prevalence, biotypes, plasmid profile and antimicrobial resistance of Campylobacter isolates from wild and domestic animals from Northeast Portugal. J Appl Microbiol. 1992;73:279–85. DOIGoogle Scholar
  27. Saenz  Y, Zarazaga  M, Lantero  M, Gastanares  MJ, Baquero  F, Torres  C. Antibiotic resistance in Campylobacter strains isolated from animals: Foods, and humans in Spain in 1997-1998. Antimicrob Agents Chemother. 2000;44:267–71. DOIPubMedGoogle Scholar
  28. Moore  JE, Madden  RH, Kerr  JR, Wilson  TS, Murphy  PG. Erythromycin-resistant thermophilic Campylobacter species isolated from pigs [see comments]. Vet Rec. 1996;138:306–7.PubMedGoogle Scholar
  29. Nielsen  EM, Nielsen  NL. Serotypes and typability of Campylobacter jejuni and Campylobacter coli isolated from poultry products. Int J Food Microbiol. 1999;46:199–205. DOIPubMedGoogle Scholar
  30. Endtz  HP, Mouton  RP, van der Reyden  T, Ruijs  GJ, Biever  M, van Klingeren  B. Fluoroquinolone resistance in Campylobacter spp. isolated from human stools and poultry products [letter] [see comments]. Lancet. 1990;335:787. DOIPubMedGoogle Scholar
  31. Li  CC, Chiu  CH, Wu  JL, Huang  YC, Lin  TY. Antimicrobial susceptibilities of Campylobacter jejuni and coli by using E-test in Taiwan. Scand J Infect Dis. 1998;30:39–42. DOIPubMedGoogle Scholar
  32. Gaunt  PN, Piddock  LJ. Ciprofloxacin resistant Campylobacter spp. in humans: an epidemiological and laboratory study. J Antimicrob Chemother. 1996;37:47–57. DOIPubMedGoogle Scholar
  33. Skirrow  MB, Blaser  MJ. Nachamkin I, Blaser MJ, Tompkins LS, editors. Campylobacter jejuni: current status and future trends. Washington: American Society for Microbiology; 1992. p. 3-8.
  34. Neimann  J, Engberg  J, Mølbak  K, Wegener  HC. Proceedings of the 4th World Congress on Foodborne Infections and Intoxications. Berlin: Federal Institute for Health Protection of Consumer and Veterinary Medicine; 1998. p. 298-303.
  35. Engberg  J, Gerner-Smidt  P, Scheutz  F, Nielsen  EM, On  SLW, Mølbak  K. Water-borne Campylobacter jejuni infection in a Danish town - a 6-week continuous source outbreak. Clin Microbiol Infect. 1998;4:648–56. DOIPubMedGoogle Scholar
  36. On  SLW, Nielsen  EM, 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;120:231–7. DOIPubMedGoogle Scholar
  37. Nielsen  EM, 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;19:47–56. DOIPubMedGoogle Scholar
  38. Doyle  MP, Jones  DM, Nachamkin  I, Blaser  MJ, Tompkins  LS, eds. Campylobacter jejuni - current status and future trends. Washington DC: American Society for Microbiology; 1992. p. 45-8.
  39. Piddock  LJV. Working Paper 20.09. Geneva: World Health Organization; 1998. p. 1-9.
  40. Gallardo  F, Gascon  J, Ruiz  J, Corachan  M, de Anta  MTJ, Vila  J. Campylobacter jejuni as a cause of traveler's diarrhea: clinical features and antimicrobial susceptibility. J Travel Med. 1998;5:23–6. DOIPubMedGoogle Scholar
  41. Mattila  L, Peltola  H, Siitonen  A, Kyronseppa  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;17:779–82.PubMedGoogle Scholar
  42. Friedman  CR, Yang  S, Rocourt  J, Stamey  K, Vugia  D, Marcus  R, Program and Abstracts of 36th annual meeting of the Infectious Diseases Society of America Denver (CO): The Infectious Diseases Society of America; 1998; Abstract 545 Fr, p. 179.
  43. Rautelin  H, Renkonen  OV, Kosunen  TU. Emergence of fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli in subjects from Finland. Antimicrob Agents Chemother. 1991;35:2065–9.PubMedGoogle Scholar
  44. 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;36:2847–9.PubMedGoogle Scholar
  45. Sjögren  E, Lindblom  GB, Kaijser  B. Norfloxacin resistance in Campylobacter jejuni and Campylobacter coli isolates from Swedish patients. J Antimicrob Chemother. 1997;40:257–61. DOIPubMedGoogle Scholar
  46. Engberg  J, Andersen  S, Skov  R, Aarestrup  FM, Gerner-Smidt  P. Comparison of two agar dilution methods and three agar diffusion methods including the E-test for antibiotic susceptibility testing of thermophilic Campylobacter species. Clin Microbiol Infect. 1999;5:580–4. DOIPubMedGoogle Scholar
  47. Orr  KE, Lightfoot  NF, Sisson  PR, Harkis  BA, Tveddle  JL, Boyd  P, Direct milk excretion of Campylobacter jejuni an a dairy cow causing cases of human enteritis. Epidemiol Infect. 1995; 11415–24.PubMedGoogle Scholar
  48. Pearson  AD, Greenwood  MH, Donaldson  J, Healing  TD, Jones  DM, Shahamat  M, Continuous source outbreak of campylobacteriosis traced to chicken. J Food Prot. 2000;63:309–14.PubMedGoogle Scholar
  49. Owen  RJ, 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;176:345–50. DOIPubMedGoogle Scholar
  50. Funke  G, Baumann  R, Penner  JL, 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;13:612–5. DOIPubMedGoogle Scholar
  51. Segreti  J, Gootz  TD, Goodman  LJ, Parkhurst  GW, Quinn  JP, Martin  BA, High-level quinolone resistance in clinical isolates of Campylobacter jejuni. J Infect Dis. 1992;165:667–70.PubMedGoogle Scholar
  52. 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;26:91–6. DOIPubMedGoogle Scholar
  53. Ellis-Pegler  RB, Hyman  LK, Ingram  RJ, McCarthy  M. A placebo controlled evaluation of lomefloxacin in the treatment of bacterial diarrhoea in the community. J Antimicrob Chemother. 1995;36:259–63. DOIPubMedGoogle Scholar
  54. Molina  J, Casin  I, Hausfater  P, Giretti  E, Welker  Y, Decazes  J, Campylobacter infections in HIV-infected patients: clinical and bacteriological features. AIDS. 1995;9:881–5. DOIPubMedGoogle Scholar
  55. 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 [letter]. Eur J Clin Microbiol Infect Dis. 1993;12:566–8. DOIPubMedGoogle Scholar
  56. Reina  J, Ros  MJ, 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;38:2917–20.PubMedGoogle Scholar
  57. Sanchez  R, Fernandez Baca  V, Diaz  MD, Munoz  P, Rodriguez Creixems  M, Bouza  E. Evolution of susceptibilities of Campylobacter spp. to quinolones and macrolides. Antimicrob Agents Chemother. 1994;38:1879–82.PubMedGoogle Scholar
  58. Feierl  G, Berghold  C, Furpass  T, Marth  E. Further increase in ciprofloxacin-resistant Campylobacter jejuni/coli in Styria, Austria. Clin Microbiol Infect. 1999;5:59–60. DOIPubMedGoogle Scholar
  59. 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;42:2106–8.PubMedGoogle Scholar
  60. Gaudreau  C, Gilbert  H. Mobley HLT, Nachamkin I, McGee D, editors. Abstracts and final program of the 10th International Workshop on Campylobacter, Helicobacter and Related Organisms. Baltimore: University of Maryland School of Medicine; 1999. Abstract CA3, p. 2.
  61. Bager  F, ed. DANMAP 97 - Consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Copenhagen: Danish Zoonosis Centre; 1998. p.3.
  62. Bager  F, ed. DANMAP 99 - Consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Copenhagen: Danish Zoonosis Centre; 2000.
  63. Hänninen  ML, Pajarre  S, Klossner  ML, Rautelin  H. Typing of human Campylobacter jejuni isolates in Finland by pulsed-field gel electrophoresis. J Clin Microbiol. 1998;36:1787–9.PubMedGoogle Scholar
  64. Megraud  F. Les infections à Campylobacter en France (1986-1997). Bulletin Epidémiologique Annuel. 1998;2:83–4.
  65. 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;288:67–73.PubMedGoogle Scholar
  66. Itoh  T, Tadano  K, Obata  H, Shingaki  K, Kai  A, Saito  K, Emergence of quinolone-resistance in clinical isolates of Campylobacter jejuni in Japan. In: Newell DG, Ketley J, Feldman RA, editors. In: Abstracts of the 8th International Workshop on Campylobacters, Helicobacters and Related Organisms; 1995 Jul 10-13; t Winchester, United Kingdom. New Haw, Addlestone, England: Central Veterinary Laboratory; 1995. p. 83.
  67. Piersimoni  C, Crotti  D, Nista  D, Bornigia  G, de Sio  G. Newell DG, et al, editors. Abstracts of the 8th International Workshop on Campylobacters, Helicobacters and Related Organisms; 1995 Jul 10-13; Winchester, United Kingdom. New Haw, Addlestone, England: Central Veterinary Laboratory; 1995; p. 88.
  68. Crotti  D, Medori  MC, Fonzo  G, Del Sante  M, Silvestrini  R. Clinical microbiology of Campylobacter enteritis in our experience. Clin Microbiol Infect. 1999;7(Suppl. 3):267.
  69. Crotti  D, Fonzo  G, D'Annibale  ML, Medori  M. C. Luzzi I, Mobley HLT, et al, In: Mobley HLT, Nachamkin I, McGee D, editors. Abstracts and final program of the 10th International Workshop on Campylobacter, Helicobacter and Related Organisms. Baltimore: University of Maryland School of Medicine; 1999. Abstract CA7. p. 4.
  70. Dowling  J, MacCulloch  D, Morris  AJ. Antimicrobial susceptibility of Campylobacter and Yersinia enterocolitica isolates [letter]. N Z Med J. 1998;111:281.PubMedGoogle Scholar
  71. Lim  YS, Tay  L. A one-year study of enteric Campylobacter infections in Singapore. J Trop Med Hyg. 1992;95:119–23.PubMedGoogle Scholar
  72. Navarro  F, Miro  E, Mirelis  B, Prats  G. Campylobacter spp. antibiotic susceptibility [letter; comment]. J Antimicrob Chemother. 1993;32:906–7. DOIPubMedGoogle Scholar
  73. Hoge  CW, Gambel  JM, Srijan  A, Pitarangsi  C, Echeverria  P. Trends in antibiotic resistance among diarrheal pathogens isolated in Thailand over 15 years. Clin Infect Dis. 1998;26:341–5. DOIPubMedGoogle Scholar
  74. Murphy  GS Jr, Echeverria  P, Jackson  LR, Arness  MK, 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;22:868–9.PubMedGoogle Scholar
  75. Frost  JA, Thwaites  RT. Drug resistance in C. jejuni, C. coli and C. lari isolated from humans in Wales and North West England during 1997. Working Paper 20.10b. Geneva: World Health Organization; 1998.
  76. Baker  CN. The E-Test and Campylobacter jejuni. Diagn Microbiol Infect Dis. 1992;15:469–72. DOIPubMedGoogle Scholar
  77. National Antimicrobial resistance monitoring system NARMS - 1997 annual report revised. Atlanta: Centers for Disease Control and Prevention; 1998.
  78. Nachamkin  I. Antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli to ciprofloxacin, erythromycin and tetracycline from 1982 to 1992. Med Microbiol Lett. 1992;2:300–5.
  79. Hirschl  AM, Wolf  D, Berger  J, Rotter  ML. In vitro susceptibility of Campylobacter jejuni and Campylobacter coli isolated in Austria to erythromycin and ciprofloxacin. Zentralbl Bakteriol. 1990;272:443–7.PubMedGoogle Scholar
  80. Feierl  G, Pschaid  A, Sixl  B, Marth  E. Increase of ciprofloxacin resistance in Campylobacter species in Styria, Austria. Int J Med Microbiol Virol Parasitol Infect Dis. 1994;281:471–4.PubMedGoogle Scholar
  81. Stobberingh  E, van den Bogaard  A, Mevius  D, Endtz  H. Examples of in-vitro quinolone resistance prevalence trends in humans and animal isolates of food-borne Salmonella and Campylobacter. Working Paper 20.09. Geneva: World Health Organization; 1998.
  82. Perez Trallero  E, Urbieta  M, Lopategui  CL, Zigorraga  C, Ayestaran  I. Antibiotics in veterinary medicine and public health [letter; comment]. Lancet. 1993;342:1371–2. DOIPubMedGoogle Scholar
  83. Reina  J. Resistance to fluoroquinolones in Salmonella non-typhi and Campylobacter spp. [letter; comment]. Lancet. 1992;340:1035–6. DOIPubMedGoogle Scholar
  84. Kuschner  RA, Trofa  AF, Thomas  RJ, Hoge  CW, Pitarangsi  C, Amato  S, Use of azithromycin for the treatment of Campylobacter enteritis in travelers to Thailand, an area where ciprofloxacin resistance is prevalent. Clin Infect Dis. 1995;21:536–41.PubMedGoogle Scholar
  85. Bowler  I, Day  D. Emerging quinolone resistance in campylobacters [letter; comment]. Lancet. 1992;340:245. DOIPubMedGoogle Scholar
  86. McIntyre  M, Lyons  M. Resistance to ciprofloxacin in Campylobacter spp. [letter; comment]. Lancet. 1993;341:188. DOIPubMedGoogle Scholar
  87. Bowler  IC, Connor  M, Lessing  MP, Day  D. Quinolone resistance and Campylobacter species [letter]. J Antimicrob Chemother. 1996;38:315. DOIPubMedGoogle Scholar
  88. Sam  WIC, Lyons  MM, Waghorn  DJ. Increasing rates of ciprofloxacin resistant Campylobacter [Letter]. J Clin Pathol. 1999;52:709. DOIPubMedGoogle Scholar
  89. Shah  PM, Schafer  V, Knothe  H. Medical and veterinary use of antimicrobial agents: implications for public health. A clinician's view on antimicrobial resistance. Vet Microbiol. 1993;35:269–74. DOIPubMedGoogle Scholar
  90. 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;11:1163–6. DOIPubMedGoogle Scholar
  91. 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;21:634–8.PubMedGoogle Scholar
  92. Threlfall  EJ, Ward  LR, Rowe  B. Resistance to ciprofloxacin in non-typhoidal salmonellas from humans in England and Wales - the current situation. Clin Microbiol Infect. 1999;5:130–4. DOIPubMedGoogle Scholar
  93. Mølbak  K, Baggesen  DL, Aarestrup  FM, Ebbesen  JM, Engberg  J, Frydendahl  K, An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype Typhimurium DT 104. N Engl J Med. 1999;341:1420–5. DOIPubMedGoogle Scholar
  94. Pedersen  KB, Aarestrup  FM, Jensen  NE, Bager  F, Jensen  LB, Jorsal  SE, The need for a veterinary antibiotic policy. Vet Rec 1999;(July 10):50-3.
  95. Use of quinolones in food animals and potential impact on human health. Report of a WHO meeting, Geneva, Switzerland, 2-5 June 1998. Geneva: World Health Organization; 1998.

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