Antibiotic resistance in Campylobacter spp. isolated from human faeces (1980–2000) and foods (1997–2000) in Northern Ireland: an update

John E. Moore1,*, Mary Crowe, Neville Heaney and Elizabeth Crothers

Northern Ireland Public Health Laboratory, Department of Bacteriology, Belfast City Hospital, Belfast BT9 7AD, UK

Sir,

Thermophilic Campylobacter spp., particularly Campylobacter jejuni and Campylobacter coli, continue to be the faecal pathogens most frequently isolated in Northern Ireland, with approximately 1000 laboratory reports per year.1 Although oral antibiotics are not normally prescribed in the majority of cases, antimicrobial therapeutic intervention may be required owing to the immunocompromised state of the patient or any other predisposing complication. Presently, there are very limited data in the literature on fluoroquinolone resistance in food and human faecal sources from Northern Ireland. Furthermore, as there is growing concern regarding rates of fluoroquinolone resistance in human isolates and the associated employment of similar agents within animal production, a study was initiated to examine the trends and rates of antibiotic resistance within human isolates submitted to the Northern Ireland Public Health Laboratory (NIPHL) over the last 20 years, 1980–2000, as well as to examine trends in resistance rates in campylobacters isolated from food sources in Northern Ireland over a more recent time period (1997–2000).

Human isolates were obtained from faecal specimens submitted to NIPHL for routine analysis from general practitioners, as well as from hospital wards, over the period 1980–2000 (n = 2066). Isolates were obtained by direct selective plating onto Preston's selective agar and incubated at 42°C for 48 h. Food samples were collected from retail premises by Environmental Health Officers from the 26 local council authorities within Northern Ireland and campylobacters (n = 729) were isolated in accordance with a method previously described by the Public Health Laboratory Service,2 modified to include 25 g chicken neck skin. Antibiotic susceptibility studies were performed at 37°C for both food and human isolates by a disc diffusion method employing the following antibiotic agents at the given disc concentrations: penicillin (2 µg), cefalexin (30 µg), erythromycin (5 µg), chloramphenicol (10 µg), gentamicin (10 µg), tetracycline (10 µg) and ciprofloxacin (1 µg). In addition, all human isolates for the period 1980–1995 were also tested against novobiocin (5 µg), kanamycin (30 µg) and neomycin (30 µg). Food isolates were also examined for trimethoprim susceptibility employing a 5 µg disc concentration.

Antibiotic resistance trends for erythromycin, ciprofloxacin, and tetracycline for foods (1997–2000) and human isolates (1996–2000) are shown in the TableGo. All food and human isolates examined were resistant to penicillin and cefalexin and susceptible to chloramphenicol and gentamicin. In addition, all food isolates were resistant to trimethoprim. For faecal isolates prior to 1996, chloramphenicol resistance was first noted in 1993 (1.4%) and also 1995 (0.8%); macrolide resistance in faecal isolates remained low with 2.0% and 2.6% of clinical isolates being resistant to erythromycin in 1987 and 1994, respectively; fluoroquinolone resistance in human isolates was 3.8% in 1992, increasing to 10% in 1993. Prior to 1992, over the 11 year period 1980–1991, no resistance to nalidixic acid was detected.


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Table. Comparison of antibiotic-resistant Campylobacter spp. isolated from recent foods and clinical isolates
 
The NIPHL has historically received between onequarter and one-third of all Northern Ireland Campylobacter faecal isolates and the majority of all isolates received generally originate from a mainly urban population. Like most other UK clinical diagnostic laboratories, confirmed human campylobacters are not characterized to the species level, as a generic identification accompanied by an antibiogram of suitable antimicrobial agents relating to the isolate is sufficient and cost-effective for the clinical management of most infected individuals. For the period 1989–1990 only 17% of human campylobacters reported to the CDSC were characterized to the species level,3 and hence it should be noted that failure to speciate these organism may mask shifts in rates of infection between the species.

In 2000, a slight rise to 4.2% in the frequency of erythromycin resistance was noted in the human population and concurrent to this, an approximately four-fold rise in macrolide resistance was noted in retail raw chicken. In comparison to overall UK resistance rates for erythromycin of 1.8%,4 Northern Ireland rates are slightly higher than the UK average. Human ciprofloxacin resistance rates have risen steadily in N. Ireland over the period, with a maximum three-fold rise from 9% to 23% in 1999, which dropped to 17.4% in 2000. However, there was no concurrent rise in fluoroquinolone resistance rates in poultry over a similar time period. There are several possible explanations for these data. First, the rise in the incidence of fluoroquinolone resistance in humans may be attributed to the increased consumption of poultry meat, following consumer concerns over the safety of British beef and BSE, as announced in a Government press release in March 1996. If cattle production statistics are compared between 1995, i.e. in the pre-consumer BSE awareness period and in 1997, approximately 8 months after the food safety announcement on BSE, a significant reduction of 304 000 tonnes (43.6%) in production is noted. Therefore, as consumers switched dietary habits from beef to poultry, a significant increase (15.8%) in the number of laboratory reports can be noted for the UK. For the same time period in Northern Ireland, there was a less marked increase in laboratory reports, although the percentage annual increase in laboratory report is notably higher in Northern Ireland than in the rest of the UK. In 1996, probably owing to a significant increase in demand for non-BSE-associated meats, there was a significant increase in the importation of poultry to the UK from the rest of the world, which has continued to increase at a steady rate, combined with a concurrent increase in poultry imports from the EU. Likewise, in 1996, the UK began to import significant amounts of pig meat from the rest of the world and this may have had an influence on antibiotic resistance in humans, particularly in pork-related cases of gastroenteritis, as the pig is the favoured host of C. coli and this species has historically been shown to have a high resistance to macrolides.

Previously, Gaunt & Piddock5 reported that consumption of imported chicken is a possible risk factor for the acquisition of a fluoroquinolone-resistant strain. Furthermore, these workers suggested that use of enrofloxacin was exerting a selective pressure on poultry campylobacters, as they were only able to demonstrate one fluoroquinolone-resistant isolate from UK poultry, relatively soon after the introduction of the licensing of enrofloxacin in the UK, in contrast to 14% of poultry carcasses imported from France and Denmark, where enrofloxacin had been licensed in each country since 1991.6 Further molecular epidemiological typing work is therefore required to correlate genotypes of fluoroquinolone-resistant isolates from British poultry, imported poultry, and humans to ascertain the relative significances to public health.

Notes

* Corresponding author. Tel: +44-28-9026-3554; Fax: +44-28-2589-2887; E-mail: jemoore{at}niphl.dnet.co.uk Back

References

1 . Campylobacter Communicable Disease Surveillance Centre (Northern Ireland). (1999). Review of Communicable Diseases, p. 58. CDSC, Colindale, UK.

2 . Anonymous. (1998). PHLS methods for food products: detection of Campylobacter species. Standard Method: F21. Public Health Laboratory Service, London, UK.

3 . Anonymous. (1992). Interim report on Campylobacter, p. 15. HMSO, London.

4 . Frost, J. A. & Thwaites, R. T. (1998). 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. World Health Organization, Geneva.

5 . Gaunt, P. N. & Piddock, L. J. V. (1996). Ciprofloxacin resistant Campylobacter spp. in humans: an epidemiological and laboratory study. Journal of Antimicrobial Chemotherapy 37, 747–57.[Abstract]

6 . Engberg, J., Aarestrup, F. M., Taylor, D. E., Gerner-Smidt, P. & Nachamkin, I. (2001). Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: Resistance mechanisms and trends in human isolates. Emerging Infectious Diseases 7, 24–34.[ISI][Medline]