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Low-Level Fluoroquinolone Resistanceamong Campylobacter jejuni Isolates in Australia Leanne E. Unicomb,2,7 John Ferguson,3,4 Russell J. Stafford,1 Rosie Ashbolt,6 Martyn D. Kirk,8 Niels G. Becker,7
Mahomed S. Patel,7 Gwendolyn L. Gilbert,8 Mary Valcanis,9 and Lance Mickan,10 for the Australian Campylobacter
Subtyping Study Groupa
1OzFoodNet, Queensland Health, Archerfield, Queensland, 2OzFoodNet, Hunter New England Population Health, Wallsend, 3Hunter New EnglandHealth Service, Newcastle, 4University of Newcastle, Callaghan, and 5Centre for Infectious Diseases & Microbiology, Institute of ClinicalPathology and Medical Research, Wentworthville, New South Wales, 6OzFoodNet, Department of Health and Human Service, Hobart, Tasmania,7National Centre for Epidemiology and Population Health, Australia National University, and 8OzFoodNet, Department of Health and Ageing,Canberra, Australian Capital Territory, 9Microbiological Diagnostic Unit, Department of Microbiology and Immunology, University of Melbourne,Parkville, Victoria, and 10Institute of Medical and Veterinary Sciences, Rundle Mall, Adelaide, South Australia, Australia Background.
Ciprofloxacin-resistant Campylobacter jejuni isolates obtained from infected patients in Australia have not been detected in studies of isolates from specific geographic areas. The Australian government hasprohibited the use of fluoroquinolone in food-producing animals. To assess the impact of this policy, we haveexamined the antimicrobial susceptibility of isolates from 5 Australian states.
Methods.
We conducted a period-prevalence survey of the susceptibility of C. jejuni isolates to 10 antimicrobial agents. C. jejuni isolates obtained from 585 patients from 5 Australian states (Queensland, South Australia, Tasmania,Victoria, and Western Australia) were identified by means of notifiable disease databases and were systematicallyselected from September 2001 to August 2002.
Results.
Among locally acquired infections, only 2% of isolates (range, 0%–8% in different states) were resistant to ciprofloxacin. The locally acquired isolates also exhibited resistance to sulfisoxazole (55%), ampicillin (46%),roxithromycin (38%), tetracycline (7%), nalidixic acid (6%), chloramphenicol (3%), erythromycin (3%), genta-micin (2%), and kanamycin (0.2%). Treatment with antimicrobial agents in the 4 weeks before onset was notassociated with ciprofloxacin resistance.
Conclusions.
The very low level of ciprofloxacin resistance in C. jejuni isolates likely reflects the success of Australia’s policy of restricting use of fluoroquinolones in food-producing animals.
Campylobacter species are the most common bacterial particularly resistance to fluoroquinolones [2, 5]. An- cause of foodborne disease in Australia and other in- timicrobial resistance may add to the burden of disease; dustrialized countries [1–3] and constitute a substantial fluoroquinolone-resistant organisms have been re- health burden. The incidence of reported cases in Aus- ported to be associated with more-severe disease [6], tralia was 116.5 cases per 100,000 persons in 2003 [1], including diarrhea of a longer duration [7] and an in- and ∼277,000 cases of Campylobacter infection are es- creased likelihood of invasive disease and death [8].
The rising incidence of fluoroquinolone resistance has In Europe and the United States, increasing propor- been attributed to the use of fluoroquinolones in food- tions of patients are infected with strains of Campy- producing animals [5] and has been reflected in the lobacter species exhibiting antimicrobial resistance, high prevalence of ciprofloxacin-resistant animal Cam-pylobacter isolates in animals in those countries [9].
Surveillance of antimicrobial resistance is important for monitoring trends. Data regarding antimicrobial re- Received 6 November 2005; accepted 23 January 2006; electronically published sistance among Campylobacter isolates in Australia are a Members of the study group are listed at the end of the text.
limited, and studies have been confined to specific geo- Reprints or correspondence: Ms. Leanne Unicomb, National Centre for Epidemiology and Population Health, Australia National University, Canberra, ACT graphic regions [10–12]. Resistant isolates are not com- 0200, Australia (leanne.unicomb@anu.edu.au).
mon, and fluoroquinolone resistance has not been de- Clinical Infectious Diseases
2006; 42:1368–74
tected previously among locally acquired isolates [12].
ᮊ 2006 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2006/4210-0004$15.00 The aim of this study was to estimate the prevalence 1368 • CID 2006:42 (15 May) • Unicomb et al.
of antimicrobial resistance among Australian isolates of Cam- [13], and only C. jejuni isolates (subspecies jejuni or doylei) pylobacter jejuni. Australia is in an almost unique position in that it is has prohibited fluoroquinolones from being used in Susceptibility testing was performed at each public health food-producing animals, although it has animal production and laboratory by the agar dilution method using Mueller-Hinton food production systems comparable to those of other devel- agar with 5% lysed sheep blood, in accordance with National oped nations. By measuring the prevalence of fluoroquinolone Committee for Clinical Laboratory Standards (now called resistance among C. jejuni isolates obtained from Australian Clinical and Laboratory Standards Institute [CLSI]), as de- patients, some insight might be gained into the benefit of scribed elsewhere [14]. MICs were defined as the lowest con- stricter control over the use of medically important antimicro- centration giving complete inhibition of visible growth. An- bials in food animals. Prevalence of resistance was examined timicrobial agents tested and breakpoints denoting resistance for Campylobacter isolates obtained from patients from 5 ju- were as follows: nalidixic acid, у32 mg/L; ciprofloxacin, у4 risdictions, representing ∼60% of the Australian population, mg/L; tetracycline, у16 mg/L; ampicillin, у32 mg/L; eryth- over a 1-year period and was compared by travel status and romycin, у8 mg/L; roxithromycin, у8 mg/L; gentamicin, у8 mg/L; kanamycin, у32 mg/L; chloramphenicol, у32 mg/L;and sulfisoxazole, у 350 mg/L. Because there are no rec- ommended breakpoints specifically for Campylobacter species,the CLSI breakpoints for Enterobacteriaceae were used, except Study population.
Campylobacter isolates were collected from for erythromycin, for which the breakpoint for Staphylococcus case-patients enrolled in a multicenter, prospective, case-con- trol study of sporadic infection (to be reported separately). Thecase-patients were identified from laboratory reports from 5 Before the study began, a set of 8 isolates that had been Australian states (Queensland, South Australia, Tasmania, Vic- previously tested for susceptibility to 7 of the 10 agents used toria, and Western Australia) between September 2001 and Au- in the study [10] were tested by each laboratory to ensure gust 2002. These jurisdictions represented all states that require reproducibility of results. During the testing of study isolates, doctors and laboratories to report patients infected with Cam- C. jejuni NCTC 11351 (same isolate as the CLSI-recom- pylobacter species. The 2 Australian territories were not in- mended ATCC 33560 [15]) was included as the control in cluded, and New South Wales, where Campylobacter is not notifiable, was not included. Each jurisdiction aimed to recruit Statistical analyses.
∼200 patients of all ages using a systematic method of selection.
tients infected with ciprofloxacin-resistant isolates and patients Patients were excluded if they could not be contacted, their infected with susceptible isolates; (2) the prevalence of resis- parents were not English speakers, they could not answer ques- tance among locally acquired isolates and the prevalence among tions (e.g., because of dementia or because they were deceased), isolates acquired overseas; and (3) the severity of disease among they could not recall the date of onset of their diarrhea, onset patients infected with ciprofloxacin-susceptible Campylobacter was у10 days before the specimen was collected, they could and the severity of disease among patients infected with cip- not be interviewed within 30 days after onset, another member rofloxacin-resistant Campylobacter. The following severity in- of the household had had diarrhea or had been diagnosed with dicators were examined: duration of diarrhea, presence of blood Campylobacter infection in the previous 4 weeks, they had a in the stool, fever and vomiting, hospitalization, and length of mixed infection (i.e., an additional diarrheal pathogen was si- hospital stay. The 95% CIs for prevalence and ORs were based multaneously detected), they were part of an outbreak, or they on standard large sample methods for estimates of proportions.
Exact methods were used when counts were small. In particular, A telephone-administered questionnaire was used to docu- Fisher’s exact test was used to the compare prevalence of an- ment exposures for the 7 days before onset of illness. Questions timicrobial resistance in locally acquired isolates with the prev- included details of overseas travel (country visited and travel alence of resistance in travel-acquired isolates. Prevalences of dates), demographic characteristics (age and sex), severity of resistance among isolates from locally acquired infections were illness (duration of diarrhea, bloody stools, fever, and vomit- compared across jurisdictions and by antimicrobial exposure ing), care management (hospital admission and duration of status using likelihood ratio tests based on logistic regression, hospitalization), consumption of antimicrobial agents in the 4 with potential confounders included in the analyses.
weeks before onset, and underlying diseases.
Logistic regression was also used to compare dichotomous Laboratory methods.
measures of severity of illness, such as hospitalization and blood transported from the clinical laboratory to the state public in stool, whereas standard linear regression was used to com- health laboratory for storage and additional testing. C. jejuni pare continuous measures, such as duration of illness and isolates were distinguished from non-jejuni species at each pub- length of hospital stay. Statistical analyses were performed using lic health laboratory using PCR that targeted the HipO gene Australian Campylobacter Antimicrobial Resistance • CID 2006:42 (15 May) • 1369
95% CI, 0.2–10.2). No patient infected with a ciprofloxacin-resistant isolate had taken a fluoroquinolone in the 4 weeks The characteristics of the study population, including the num- before onset of illness. Nine (64%) of 14 patients with cipro- ber of cases of Campylobacter infection reported during the floxacin-resistant isolates were given antibiotic therapy for their study period, the number of case-patients recruited, and the Campylobacter infection, compared with 222 (40%) of 549 pa- proportion of isolates tested, are summarized by state in table tients with ciprofloxacin-susceptible isolates; however, this dif- 1. Of the 585 isolates tested, 279 (48%) were from female ference did not reach statistical significance (OR, 2.5; 95% CI, patients, and the median age was 32 years (range, 0–93 years).
The proportion of Campylobacter isolates tested for antimicro- Infection with a ciprofloxacin-resistant strain of C. jejuni bial susceptibility from reported case-patients from each state did not result in a more-severe illness, but the number of ranged from 3% in Victoria to 14% in South Australia. The patients that were infected with a ciprofloxacin-resistant strain population under surveillance in the 5 participating states com- of C. jejuni was small. There were no significant differences prised ∼64% of the Australian population in 2001.
in the distribution of symptoms; compared with patients in- Prevalences of resistance to the 10 antimicrobial agents fected ciprofloxacin-susceptible strains, patients infected with among locally acquired isolates is shown in table 2. Sulfisox- ciprofloxacin-resistant strains were no more likely to have azole resistance was the most common (55% of isolates), and fever (68% vs. 74%; OR, 1.6; 95% CI, 0.4–5.9), or vomiting only 2% of isolates were resistant to ciprofloxacin.
(38% vs. 35%; OR, 1.6; 95% CI, 0.6–4.5), or bloody stools Ciprofloxacin resistance was found among locally acquired (15% vs. 42%; OR, 0.4; 95% CI, 0.1–5.4). Duration of di- isolates from all states except Tasmania (table 2). All 14 locally arrhea was similar for patients infected with ciprofloxacin- acquired isolates were also resistant to nalidixic acid, and 10 resistant strains and patients infected with ciprofloxacin-sen- (71%) were resistant to 11 class of antimicrobial agent (table sitive strains (median duration for both groups, 7 days; 3). Temporal clusters of infection were detected in Victoria as were the percentage of patients requiring hos- (November–December 2001 and January–February 2002) and pitalization (14% vs. 13%; OR, 0.8; 95% CI, 0.2–3.6) and the in South Australia (May 2002), but a variety of resistance phe- length of hospital stay (median duration for both groups, 0 notypes were detected in these clusters, indicating that the iso- days; P p .13) in multivariate models controlling for age and lates were unlikely to be related (table 3). The prevalence of underlying disease, regardless of travel status.
ciprofloxacin resistance in Victoria was higher than in all otherstates combined (9% vs. 2%; OR, 6.2; 95% CI, 2.1–18.5), but DISCUSSION
this significant difference should be interpreted with care, be- This is the first Australian study to report locally acquired cause it is a post hoc comparison. When controlling for juris- Campylobacter isolates resistant to fluoroquinolones. However, diction, patients infected with ciprofloxacin-resistant isolates the prevalence of ciprofloxacin resistance among locally ac- were more likely to have an underlying disease than those in- quired isolates in Australia was low at 2% and ranged from fected with ciprofloxacin-susceptible isolates (OR 5.1; 95% CI, 0% to 8% across 5 states. The absence of ciprofloxacin-resistant isolates in locally acquired infections in Australia has been at- People who acquired Campylobacter infections overseas were tributed previously to restricting the use of fluoroquinolones more likely to be infected with resistant strains; 9 (82%) of 11 in food-producing animals. Data regarding antimicrobial sus- overseas-acquired isolates were resistant to 11 class of anti- ceptibility among Campylobacter isolates infecting Australian microbial agent, compared with 291 (51%) of 574 locally ac- food-producing animals is limited; however, Campylobacter iso- quired isolates (OR, 4.4; 95% CI, 0.9–41.9). Resistances to cip- lates (all species) from pigs have been shown to be uniformly rofloxacin and tetracycline were significantly more prevalent susceptible to ciprofloxacin [17], likely reflecting the low prev- among overseas-acquired isolates than they were among locally alence of resistance in isolates obtained from Australian ani- acquired isolates: ciprofloxacin, 64% vs. 2% (OR, 67.5; 95% mals. The prevalence is similar to that described for humans CI, 15.2–351.6); and tetracyline, 55% vs. 7% (OR, 16.7; 95% from Sweden (between 0% and 9%), where the use of anti- CI, 4.0–72.6). Nine of 11 patients had travelled to Asia (In- biotics as growth promoters was banned in 1986 [18]. A low donesia, Malaysia, Singapore, Thailand, and Vietnam) during prevalence of ciprofloxacin resistance was also found among the week before onset of illness; the remaining 2 patients had isolates obtained from Swedish animals [9]. Among studies that travelled to Africa and North and South America (data not have separated locally acquired from travel-acquired isolates, in countries that have allowed the use of fluoroquinolones for Patients infected with locally acquired ciprofloxacin-resistant animals, the prevalence of locally acquired ciprofloxacin resis- strains were no more likely to have taken an antimicrobial agent tance ranges from 7% to 29% [3, 19]. The overall prevalence in the 4 weeks before onset, compared with patients infected of ciprofloxacin resistance is much higher in some countries, with ciprofloxacin-susceptible isolates (6% vs. 7%; OR, 1.3; probably reflecting widespread use of ciprofloxacin in humans 1370 • CID 2006:42 (15 May) • Unicomb et al.
Summary of patients with Campylobacter infection and the Campylobacter jejuni isolates included in the study.
a All states that reported Campylobacter infections to the National Notifiable Diseases Database have been included in the study. Neither of the 2 territories were included.
b Population estimated from the 2001 census (Australia Bureau of Statistics).
c All Campylobacter-infected patients reported to National Notifiable Diseases Database [16].
d Species determined using PCR [13].
Percentage of locally acquired Campylobacter jejuni isolates resistant to 10 antimicrobial agents by state, September 2001–August 2002.
a Percentage of all isolates tested for resistance from the respective state that were resistant to the specified antimicrobial agent.
Characteristics of patients infected with locally-acquired ciprofloxacin-resistant Campylobacter jejuni.
Nalidixic acid, roxithromycin, sulfisoxazole Nalidixic acid, tetracyline, ampicillin, gentamicin, Nalidixic acid, ampicillin, roxithromycin Nalidixic acid, ampicillin, erythromycin, roxithromycin, gentamicin a Names of antimicrobial agents were not recorded.
b Patient was admitted to a hospital.
in those regions. These regions include countries in which Aus- of illness, but there was no association between this and cip- tralian travellers are likely to acquire infection; for example, 180% of clinical isolates in Thailand have been reported to be In our study, infection with a ciprofloxacin-resistant isolate ciprofloxacin resistant [5], and 35% of clinical isolates in In- was not associated with increased severity of illness; this con- donesia were ciprofloxacin resistant [20].
trasts with a study from the United States, in which a similar The source of resistant isolates from locally acquired infec- number of patients infected with ciprofloxacin-resistant organ- tions is unclear. It is possible that the case-patient had been isms was more likely to be hospitalized and have bloody di- overseas 17 days before the onset of illness or had direct contact arrhea [25] than were patients infected with susceptible isolates.
with a recently returned traveller; however, person-to-person A study [7] that described patients infected with ciprofloxacin- transmission is uncommon [21]. Other possible sources include resistant isolates who had prolonged diarrhea included 63 pa- consumption of contaminated, imported food or acquisition tients; it is possible that the larger sample size raised the sta- of resistance during a hospital stay. However, only 2 of the 14 tistical power of the study to detect a difference.
patients infected with ciprofloxacin-resistant isolates had been There are some limitations in generalizing the results of admitted to a hospital for treatment. Furthermore, only cooked this study to the Australian population. First, patients in-cluded in this study were identified through notifications and chicken is permitted for importation into Australia [12], and were, therefore, more likely to have had relatively severe in- viable Campylobacter organisms are unlikely to be present.
fections, leading to presentation and a stool test. Second, we Previous studies have shown that treatment of patients with relied on self-reported information regarding overseas travel, quinolones after onset of illness but before collection of the antimicrobial therapy, and clinical symptoms, and this infor- stool specimen is associated with detection of quinolone-resis- mation was not validated. However, the potential measure- tant isolates [22]. We did not collect information on the timing ment bias resulting from this method was likely to be non- of antimicrobial treatment or the agent used. However, patients differential (i.e., occurring equally among patients infected with ciprofloxacin-resistant isolates were significantly more with resistant and susceptible strains).
likely to have been given antibiotic therapy for their infection In summary, antimicrobial resistance among Australian than were patients infected with susceptible isolates, and cip- strains of C. jejuni is uncommon, excepting resistance to am- rofloxacin is commonly used in Australia for the treatment of picillin, roxithromycin, and sulfisoxazole. Of particular im- enteric infections. Therefore, this explanation is plausible.
portance is that resistance to fluoroquinolone is very low and Three previous Australian studies that reported travel his- probably reflects Australia’s policy of prohibiting fluoroquin- tories of patients examined 153, 140, and 50 isolates, respec- olones for animal use. Sensible use of fluoroquinolones in clin- tively [12]; the sample sizes in these studies may have been ical treatment remains a high priority if a low prevalence of insufficient to detect a low prevalence of resistant isolates. The resistance in C. jejuni and other organisms is to be maintained.
reasons for variation in the apparent prevalence of locally ac- The United States withdrew approval for the use of fluoro- quired ciprofloxacin-resistant isolates by state of residence are quinolones in animals following reports between 1994 and 1996 of the increasing levels of fluoroquinolone resistance. Such a Resistance to sulfisoxazole, ampicillin, and roxithromycin policy should be considered for wider adoption. The detection was detected commonly among isolates obtained from patients of ciprofloxacin resistance among locally acquired infections that acquired their infections locally. The prevalence of am- warrants additional investigations and ongoing surveillance.
picillin resistance in this study (46%) was similar to that re-ported in previous Australian studies [10, 11] and studies from AUSTRALIAN CAMPYLOBACTER SUBTYPING
the United Kingdom [23]. Low levels of resistance were detected STUDY GROUP
for erythromycin, chloramphenicol, gentamicin, and kana- Penny Adamson (Flinders Medical Centre, South Australia), mycin, as reported in Australia [10, 24] and elsewhere [18, 19, Kellie Cheung (Institute of Clinical Pathology and Medical Re- 23, 25]. Tetracycline resistance was low, which contrasts with search, Westmead, New South Wales), Barry Combs (Depart- findings from the United States [25] but is similar to findings ment of Human Services, Adelaide, South Australia), Craig from Europe [18, 19, 26]. Isolates from travel-associated cases Dalton (Hunter New England Population Health, Newcastle, were more commonly resistant to nalidixic acid, ciprofloxacin, New South Wales), Steve Djordjevic (Elizabeth Macarthur Ag- and tetracycline than were isolates from locally acquired cases, ricultural Institute, Camden, New South Wales), Robyn Doyle as found previously in Australia [10] and Denmark [19]. Iso- (Institute of Medical and Veterinary Science, Adelaide, South lates resistant to nalidixic acid and susceptible to ciprofloxacin Australia), John Ferguson (Hunter New England Health Ser- were found among travel-acquired and locally acquired isolates, vice, Newcastle, New South Wales), Lyn Gilbert (Institute of as found in other studies [10, 23]. Six percent of case-patients Clinical Pathology and Medical Research, Westmead, New had taken an antimicrobial agent in the 4 weeks before onset South Wales), Rod Givney (Department of Human Services, Australian Campylobacter Antimicrobial Resistance • CID 2006:42 (15 May) • 1373
Adelaide, South Australia), David Gordon (Flinders Medical 8. Helms M, Simonsen J, Olsen KEP, Molbak K. Adverse health events associated with antimicrobial drug resistance in Campylobacter spe- Centre, Bedford Park, South Australia), Joy Gregory (Depart- cies: a registry-based cohort study. J Infect Dis 2005; 191:1050–5.
ment of Human Services, Melbourne, Victoria), Geoff Hogg 9. Bywater R, Deluyker H, Deroover E, et al. A European survey of (Microbiological Diagnostic Unit, University of Melbourne, antimicrobial susceptibility among zoonotic and commensal bacteriaisolated from food-producing animals. J Antimicrob Chemother Parkville, Victoria), Tim Inglis (Division of Microbiology & 2004; 54:744–54.
Infectious Diseases, PathWest, Nedlands, Western Australia), 10. Sharma H, Unicomb L, Forbes W, Djordjevic S, Valcanis M, Dalton Peter Jelfs (Institute of Clinical Pathology and Medical Re- C, Ferguson J. Antibiotic resistance in Campylobacter jejuni isolated search, Westmead, New South Wales), Martyn Kirk (Oz- from humans in the Hunter Region, New South Wales. Commun
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FoodNet, Canberra, Australian Capital Territory), Karin Lalor 11. Alfredson DA, Akhurst RJ, Korolik V. Antimicrobial resistance and (Department of Human Services, Melbourne, Victoria), Jan genomic screening of clinical isolates of thermophilic Campylobacter Lanser (Institute of Clinical Pathology and Medical Research, spp. from south-east Queensland, Australia. J Appl Microbiol
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18. Osterlund A, Hermann M, Kahlmeter G. Antibiotic resistance among Financial support.
The OzFoodNet program of work (an initiative of Campylobacter jejuni/coli strains acquired in Sweden and abroad: a the Australian Government Department of Health and Ageing) and New longitudinal study. Scand J Infect Dis 2003; 35:478–81.
South Wales Health (through the Hunter Medical Research Institute).
19. Danish Integrated Antimicrobial Resistance Monitoring and Re- Potential conflicts of interest.
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