Ciprofloxacin resistance among human Campylobacter isolates 1991–2004: an update

K. E. Dingle1,2,*, L. Clarke2 and I. C. J. W. Bowler2

1 Nuffield Department of Clinical Laboratory Sciences, Oxford University, Level 7 John Radcliffe Hospital, Oxford OX3 9DU, UK; 2 Department of Microbiology, Level 7 John Radcliffe Hospital, Oxford Radcliffe Hospitals NHS Trust, Oxford OX3 9DU, UK


* Corresponding author. Tel: +44-1865-220870; Fax: +44-1865-764192; E-mail: kate.dingle{at}ndcls.ox.ac.uk

Keywords: antibiotic resistance , epidemiology , Campylobacter

Sir,

We read with interest the report of increasing erythromycin resistance in Campylobacter isolated from humans in Northern Ireland.1 We have been monitoring antimicrobial resistance in Campylobacter of human origin in Oxfordshire since 1991,2 and our findings differ from those of Rao et al.1 in several respects.

Our laboratory serves a relatively stable population of around 600 000. About 60% of stools received for culture are from patients visiting their general practitioner (GP), and the rest are from hospital inpatients. Approximately 13 000 stool samples are submitted each year, ranging from 10441 in 1991 to 14070 in 2000. The proportion of stools from which a Campylobacter sp. was isolated has followed broadly the total number of stools submitted (Figure 1). A Campylobacter sp. was cultured from 5.7% of stools submitted since 2000, with 637–904 isolations in each of the last 5 years. Peak incidence was 150 cases per 100 000 population in 2000, an attack rate three times greater than in Northern Ireland. Such a disparity could be due to differences in the rate of Campylobacter gastroenteritis, sampling thresholds by GPs or laboratory methodology. As in Northern Ireland, the number of Campylobacter isolations in Oxfordshire has decreased since 2000 (Figure 1). This is consistent with national observations, total UK Campylobacter isolations peaking in 2000.3



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Figure 1. Campylobacter isolated in 1991–2004. Black bars represent numbers of ciprofloxacin-susceptible isolates and white bars represent numbers of ciprofloxacin-resistant isolates. Numbers above the bars indicate the percentage of ciprofloxacin-resistant isolates per year. The white dotted line indicates the percentage of total stool samples received at the laboratory from which a Campylobacter was cultured.

 
Rao et al.1 reported a striking increase in the prevalence of erythromycin-resistant strains in Northern Ireland from <2% in 1999 to 11.3% in 2002. Ciprofloxacin resistance remained steady at 13%. In contrast, the level of erythromycin resistance detected in Oxfordshire remained <2.2% between 1991 and 2004, while ciprofloxacin resistance increased from 3.1 to 25.1% (Figure 1). Both laboratories assessed resistance using disc diffusion with 1 µg ciprofloxacin, but 15 µg erythromycin was employed in Northern Ireland compared with 5 µg in Oxford. The Sentinel Surveillance Scheme Collaborators4 found 19% of Campylobacter isolated from April 2000–May 2001 in the UK were resistant to ciprofloxacin compared with 20.9% in Oxfordshire for the same time period. They also reported that 55% of ciprofloxacin-resistant Campylobacter isolated from UK patients were acquired overseas. During 2004, 87/634 (13.7%) Oxfordshire cases reported recent foreign travel to their GP and 60.6% of their isolates were resistant. Ciprofloxacin resistance in Campylobacter isolated from patients where no foreign travel was reported has increased steadily in Oxfordshire, from 1.4% in 1991 to 19.3% in 2004. This suggests an increase in the proportion of patients and GPs not reporting foreign travel and/or an increasing incidence of ciprofloxacin resistance in isolates of UK origin.

Rao et al.1 speculate that the increasing erythromycin resistance seen in human isolates in Northern Ireland is linked to a similar increase in isolates from local poultry. In our previous report we speculated that the widespread use of fluoroquinolones in the poultry industry was a likely cause of the emergence of ciprofloxacin-resistant Campylobacter in human infections.2 Humphrey et al.5 recently reported the rapid emergence of almost 100% ciprofloxacin resistance among Campylobacter during treatment of commercial broiler flocks with difloxacin or enrofloxacin. High resistance rates persisted for up to 4 weeks post-treatment, which was noted as an important observation in relation to the entry of resistant strains into the food chain.

Multilocus sequence typing (MLST) data have demonstrated that Campylobacter jejuni undergoes frequent horizontal exchange of genetic material.6 Such recombination provides a mechanism, in addition to the de novo generation of point mutations, for the rapid horizontal spread of DNA conferring antimicrobial-resistant phenotypes. The selection pressures caused by widespread fluoroquinolone use in food animals and birds colonized by Campylobacter is a possible mechanism driving the continuing increase in ciprofloxacin resistance in Campylobacter causing human infections. MLST data allow the C. jejuni population structure to be defined in terms of clonal complexes,6 some of which appear to be associated with particular host species. Such data from isolates representing different potential sources of human infection (http://pubmlst.org/campylobacter/) may ultimately allow us to understand the routes by which antibiotic-resistant strains are entering the food chain, and explain regional differences such as those reported above.

References

1. Rao D, Rao JR, Crothers, E et al. Increased erythromycin resistance in clinical Campylobacter in Northern Ireland—an update. J Antimicrob Chemother 2005; 55: 395–6.[Free Full Text]

2. Bowler ICJW, Connor M, Lessing, MP et al. Quinolone resistance and Campylobacter species. J Antimicrob Chemother 1996; 38: 315.[ISI][Medline]

3. Health Protection Agency. http://www.hpa.org.uk/infections/topics_az/campy/data_ew.htm (15 February 2005, date last accessed).

4. The Campylobacter Sentinel Surveillance Scheme Collaborators. Ciprofloxacin resistance in Campylobacter jejuni: case–case analysis as a tool for elucidating risks at home and abroad. J Antimicrob Chemother 2002; 50: 561–8.[Abstract/Free Full Text]

5. Humphrey TJ, Jorgensen F, Frost JA 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: 690–8.[Abstract/Free Full Text]

6. Dingle KE, Colles FM, Wareing DR et al. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 2001; 39: 14–23.[Abstract/Free Full Text]





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