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Journal of Food Protection, Vol. 71, No. 3, 2008, Pages 602–607Copyright ᮊ, International Association for Food Protection Research Note
Comparison of Antimicrobial Resistance of
Campylobacter jejuni and Campylobacter coli Isolated from
Humans and Chicken Carcasses in Poland
˙ BIETA ROZ˙YNEK,1* KATARZYNA DZIERZ˙ANOWSKA-FANGRAT,1 DOROTA KORSAK,2,3 PIOTR KONIECZNY,4
SEBASTIAN WARDAK,5 JOLANTA SZYCH,5 MIROSŁAW JAROSZ,2 AND DANUTA DZIERZ
˙ ANOWSKA1
1Department of Clinical Microbiology & Immunology, The Children’s Memorial Health Institute, 04-730 Warsaw, Poland; 2National Food and Nutrition Institute, Warsaw, Poland; 3Department of General Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland; 4Infectious Diseases Hospital, Dziekanow Lesny, Warsaw, Poland; and 5National Institute of Hygiene, Warsaw, Poland MS 07-048: Received 29 January 2007/Accepted 11 September 2007 ABSTRACT
Campylobacter-associated gastroenteritis remains an important cause of morbidity worldwide, and some evidence suggests that poultry is an important source of this foodborne infection in humans. This study was conducted to analyze the prevalenceand genetic background of resistance of 149 Campylobacter jejuni and 54 Campylobacter coli strains isolated from broilerchicken carcasses and from stool samples of infected children in Poland from 2003 through 2005. Nearly all isolates weresusceptible to macrolides and aminoglycosides. The highest resistance in both human and chicken strains was observed forciprofloxacin (more than 40%), followed by ampicillin (13 to 21%), and tetracycline (8 to 29%). Resistance to ampicillin andtetracycline rose significantly between 2003 and 2005. Slight differences in resistance between human and chicken isolatesindicate that although chicken meat is not the only source of Campylobacter infection in our population, it can be involvedin the transmission of drug-resistant Campylobacter strains to humans.
Campylobacter jejuni and Campylobacter coli are im- and avilamycin have been used as growth promoters in portant causes of foodborne gastroenteritis in humans in poultry farming operations, but this procedure was banned many developed countries (2, 7, 24). Surveillance data on in 2006 according to the European Community 90/167/EEC human campylobacteriosis in Poland are limited. However, directive (11). However, antimicrobials such as tylosin, tia- the results of a 6-year study in Polish children with diarrhea mulin, lincomycin, amoxicillin, ampicillin, and tetracy- revealed that the incidence of Campylobacter infections ex- clines can be used in medicated feed (6, 13). ceeded that of salmonellosis (32). Campylobacteriosis is of- The most common mechanism of high-level quinolone ten associated with handling of raw poultry or eating of resistance in Campylobacter spp. is associated with a mu- undercooked poultry meat (4). Cross-contamination of raw tation in the quinolone resistance-determining region at po- poultry to other ready-to-eat foods via the cook’s hands or sition 86 in the gyrA gene (14). The most frequently ob- kitchen utensils also has been reported (27). Campylobac- served molecular mechanism of tetracycline resistance is teriosis is generally a self-limiting disease. However, in cas- the production of Tet(O), a ribosomal protection protein.
es of severe or extraintestinal infections and in immuno- The tet(O) gene is often associated with conjugative plas- compromised patients, antibiotics may be required. Eryth- mids. However, this gene also can be chromosomally lo- romycin is the usual drug of choice for the treatment of cated (12). The high-level resistance to erythromycin is me- Campylobacter infections (2). However, fluoroquinolones, diated by mutations in domain V of the 23S rRNA gene at gentamicin, and tetracycline also are clinically effective in treating Campylobacter infections when antimicrobial ther- The aim of this study was to compare the prevalence and genetic background of antimicrobial resistance in Pol- In many studies, a significant rise in resistance to fluo- ish strains of C. jejuni and C. coli isolated from chicken roquinolones, tetracycline, and erythromycin has been dem- carcasses and children to determine whether there was a onstrated in C. jejuni and C. coli isolates (1, 15, 21, 22, 31, 34, 35). Increasing resistance is probably partly due to MATERIALS AND METHODS
the wide use of these antimicrobials in veterinary medicine,especially in poultry (9, 10, 15, 40). In Poland, flavomycin Samples of 130 broiler chicken carcasses were obtained from selected supermarkets in Warsaw. Stool samples from 946 chil-dren with diarrhea were obtained from three large pediatric hos- * Author for correspondence. Tel: ϩ48 22 815 72 70; Fax: ϩ48 22 815 pitals in Warsaw. All samples were collected from 2003 through 72 75; E-mail: fangrat@supermedia.pl.
ANTIBIOTIC RESISTANCE OF CAMPYLOBACTER ISOLATES FROM POLAND Isolation of Campylobacter spp. from chicken meat was per- resistance to ampicillin rose from 8 to 35.5% (P ϭ 0.04) formed according to the International Organization for Standard- in human isolates and from 5.8 to 30.4% (P ϭ 0.01) in ization guideline 10272 (20). After initial bacterial characteriza- chicken isolates. High rates of ciprofloxacin resistance tion by phase-contrast microscopy, Gram staining, catalase and (Ͼ40%) were noted in both human and chicken isolates oxidase production, and growth at 25 and 42ЊC, suspected colo- and did not change significantly during the study period.
nies were confirmed as C. jejuni or C. coli using the PCR method Cross-resistance to nalidixic acid and ciprofloxacin was with specific primers (33). Isolation and identification of human found in all quinolone-resistant strains.
Campylobacter strains were performed according to World HealthOrganization recommendations (17) and confirmed by the PCR Resistance phenotypes are shown in Table 3. Resis- assay (33). All Campylobacter isolates were maintained in 20% tance to quinolones was the predominant phenotype ob- glycerol in Brucella broth at Ϫ70ЊC for subsequent analysis.
served both in human (50%) and chicken (63.3%) isolates.
C. jejuni and C. coli susceptibility to seven antimicrobials The frequency of double resistance was significantly higher was determined by the Etest (AB Biodisk, Solna, Sweden) on (P Ͻ 0.001) in human isolates (27 of 68 isolates, 39.7%) Mueller-Hinton agar containing 5% sheep blood. Etests were used than in chicken isolates (7 of 60 isolates, 11.6%). Only two in accordance with the manufacturer’s instructions. The plates human C. jejuni isolates were simultaneously resistant to were incubated at 37ЊC for 48 h under microaerophilic conditions.
The following CLSI interpretative criteria for the Enterobacteri- All 149 C. jejuni and 54 C. coli strains were screened aceae family were used as breakpoints for Campylobacter resis- for molecular mechanisms of resistance to tetracycline, tance: 16 mg/liter gentamicin and tetracycline, 32 mg/liter nali- erythromycin, and ciprofloxacin. The results of phenotypic dixic acid, 4 mg/liter ciprofloxacin, and 32 mg/liter ampicillin.
For erythromycin and azithromycin, an interpretative breakpoint and genetic analyses of resistance to tetracycline were fully for Staphylococcus spp. of 8 mg/liter was used (26). C. jejuni concordant. All tetracycline-resistant isolates possessed the ATCC 33560 and C. coli ATCC 33559 were used as reference tet(O) gene. The results of macrolide susceptibility testing by Etests and 23S rRNA gene analysis were in agreement The tet(O) gene was detected by PCR assay (12). Thr-86-Ile for all but one isolate. The only C. jejuni isolate resistant mutations in the gyrA gene were identified by the mismatch am- to erythromycin by the Etest method (MIC of 24 mg/liter) plification mutation assay PCR (MAMA PCR) as described else- had no detectable A2074C or A2075G mutations in the 23S where (41, 42); however, different reaction conditions were used: rRNA gene by either PCR-RFLP assay or direct sequenc- 94ЊC for 5 min for predenaturation followed by 35 cycles of 94ЊC ing. All Campylobacter isolates resistant to quinolones by for 30 s, 54ЊC for 1 min, and 72ЊC for 1 min and a final extension the Etest had Thr-86-Ile mutations in the gyrA gene de- at 72ЊC for 7 min. The presence of Thr-86-Ile substitutions was tected by MAMA PCR and PCR-RFLP assays. However, additionally confirmed by the PCR–restriction fragment lengthpolymorphism (RFLP) method (3). The PCR-RFLP method also these mutations were also found by both molecular methods was used for the detection of A2074C and A2075G mutations in in two isolates phenotypically susceptible to ciprofloxacin the 23S rRNA gene (39). Isolates with discrepant phenotypic and (both MICs of 2 mg/liter) and nalidixic acid (MICs of 1 genetic susceptibility results were subjected to direct sequencing and 8 mg/liter). Both isolates were further confirmed by of respective genes using DYEnamic ET Terminator Cycle Se- direct sequencing to contain Thr-86-Ile mutations.
quencing Kit (GE Healthcare, Chalfont St. Giles, UK) on an Ap-plied Biosystems 3730 automated sequencer (Applied Biosystems, DISCUSSION
In several studies, handling and consumption of poul- Statistical analysis. The resistance rates were compared us-
try has been identified as important risk factors for Cam- pylobacter infections in humans (4, 16, 18, 36, 37). Thefrequency of contamination of retail chicken meat with Campylobacter spp. has exceeded 80% in some countries During a 3-year study, 100 Campylobacter strains were (4, 36, 37). In a recent survey undertaken in Poland by the isolated from 130 chickens, and 103 strains were obtained National Food and Nutrition Institute, 75% of chicken car- from 946 children. C. jejuni comprised 86.4% of human casses were contaminated with Campylobacter species (un- isolates (n ϭ 89) and 60% of chicken isolates (n ϭ 60).
published data). Microorganisms that colonize food animals The remaining isolates were C. coli. or contaminate food products and are transmitted to humans The results of antimicrobial susceptibility testing are via the food chain also can serve as a source of antimicro- summarized in Tables 1 and 2. All chicken Campylobacter bial resistance genes for bacteria residing in the human gas- strains and all but one human strain were susceptible to trointestinal tract. Increasing Campylobacter resistance to macrolides. Resistance to gentamicin was detected in three antimicrobials is likely the result of the wide use of these C. jejuni strains isolated from children and in one chicken agents in veterinary medicine and as growth promoters in strain. All gentamicin-resistant strains were obtained in animal farming operations. An estimated 50% of all anti- 2005. The overall resistance to tetracycline in chicken C. biotic usage worldwide is in veterinary medicine (24). Use jejuni and C. coli strains was 8.3 and 10%, respectively.
of quinolones, mainly enrofloxacin in veterinary applica- The respective rates in human isolates were 15.7 and tions, has been associated with the emergence of ciproflox- 28.5%. Tetracycline resistance in chicken isolates increased acin resistance in poultry and human strains of Campylo- from 0% in 2003 to 17.3% in 2005 (P ϭ 0.01). Ampicillin bacter (9, 10, 15). In contrast, in countries where quino- and ciprofloxacin had low activity against C. jejuni and C. lones have not been used in food-producing animals, very coli strains regardless of their origin. From 2003 to 2005, low incidences (2%) of ciprofloxacin-resistant Campylo- TABLE 1. MIC distributions of seven antimicrobial agents for 149 C. jejuni and 54 C. coli isolatesa a AM, ampicillin; Cj, C. jejuni; H, human; Ch, chicken; Cc, C. coli; EM, erythromycin; AZ, azithromycin; TC, tetracycline; CI, ciprofloxacin; NA, nalidixic acid; GM, gentamicin.
bacter have been observed (24). In Poland, quinolones are 86-Ile substitutions also were found in isolates resistant to allowed for therapeutic use in veterinary medicine by the ciprofloxacin but fully susceptible to nalidixic acid (5). Ministry of Agriculture and Rural Development, which A high prevalence of macrolide resistance in Campylo- may explain the high resistance rates in Campylobacter bacter has been reported mainly in those European coun- strains analyzed in this study and in Salmonella and Esch- tries where tylosin has been used as an animal growth pro- erichia coli strains of poultry origin (19). The high preva- moter (9). Among 203 Campylobacter isolates examined in lence of ciprofloxacin resistance in Campylobacter isolates this study, only 1 clinical C. jejuni strain had low resistance obtained from children may result from transmission of to erythromycin and azithromycin by the Etest, and this poultry strains, because quinolones are used only occasion- strain was simultaneously resistant to tetracycline, cipro- ally in children, mainly in the treatment of cystic fibrosis.
floxacin, and ampicillin. However, this strain did not con- Campylobacter spp. resistance to quinolones most fre- tain either of the most frequent mutations in the 23S rRNA quently results from the Thr-86-Ile mutations in the gyrA gene responsible for macrolide resistance, which suggests gene (ACA→ATA in C. jejuni and ACT→ATT in C. coli) that resistance was associated with the efflux pump. Such (28, 29). In this study, all isolates resistant to quinolones a mechanism has been described in multidrug-resistant by the Etest possessed Thr-86-Ile substitutions. However, Campylobacter isolates with low-level macrolide resistance these mutations also were found in two isolates phenotyp- ically categorized as quinolone susceptible (ciprofloxacin An increase in the resistance of Campylobacter to tet- MIC of 2 mg/liter for both isolates and nalidixic acid MICs racyclines has been observed in many countries. The prev- of 1 and 8 mg/liter). A similar phenomenon has already alence of tetracycline resistance among Campylobacter iso- been observed. The gyrA Thr-86-Ile mutations were re- lates in the United States and Germany is close to 50% (23, ported in Campylobacter isolates with a ciprofloxacin MIC 25), and in Spain it exceeds 70% (34). In this study, overall of 2 mg/liter, which suggests that this concentration could tetracycline resistance did not exceed 30%, and there were be a more appropriate breakpoint for this agent (5, 29). Thr- no significant differences in tetracycline resistance between ANTIBIOTIC RESISTANCE OF CAMPYLOBACTER ISOLATES FROM POLAND human and chicken isolates. However, a significant increase tern in epidemiological investigations (31, 34, 35, 40). The in resistance was found during the last 3 years in chicken most frequent resistance pattern observed in this study was strains (but not in human isolates). This increase may be the lack of susceptibility to a single agent, which was char- associated with the use of chlortetracycline and doxycycline acteristic of 83.3 and 56% of chicken and human strains, in medicated feed for poultry and swine (6). The most im- respectively. Double resistance was detected three times portant mechanism of tetracycline resistance in Campylo- more frequently in human strains than in chicken strains.
bacter is the plasmid-mediated transfer of the tet(O) gene, Slight differences in resistance between human and chicken which codes for the ribosomal protection protein (12). All strains may indicate that chickens are not the only source our tetracycline-resistant isolates possessed the tet(O) gene.
of Campylobacter infection in our population. This finding Some authors have proposed the use of resistance pat- is concordant with our previous findings of a different dis- TABLE 2. Resistance of Campylobacter isolates of human and chicken origin to five antimicrobial agents in 2003, 2004, and 2005a a In 2003, 2004, and 2005, 25, 47, and 31 human isolates and 51, 26, and 23 chicken isolates, respectively, were obtained.
TABLE 3. Resistance phenotypes of chicken and human Campylobacter strains a CIR, resistance to ciprofloxacin; TCR, resistance to tetracycline; AMR, resistance to ampicillin; GMR, resistance to gentamicin; EMR, tribution of some virulence markers in human and chicken Denmark: risk factors and clinical consequences. Emerg. Infect. Dis. Campylobacter strains (33). European Community. 1990. Council directive 90/167/EEC laying This is the first Polish report of Campylobacter sus- down the conditions governing the preparation, placing on the mar- ceptibility in chicken meat strains. High resistance among ket and use of medicated feedingstuffs in the Community. Off. J. these isolates to some antimicrobials may lead to increasing numbers of difficult-to-treat campylobacteriosis cases in hu- Gibreel, A., D. M. Tracz, L. Nonaka, T. M. Ngo, S. R. Connell, and mans. Therefore, constant monitoring of resistance is re- D. E. Taylor. 2004. Incidence of antibiotic resistance in Campylo- quired in both human and poultry Campylobacter strains.
bacter jejuni isolated in Alberta, Canada, from 1999 to 2002, withspecial reference to tet(O)-mediated tetracycline resistance. Antimi- ACKNOWLEDGMENTS
crob. Agents Chemother. 48:3442–3450.
Gornowicz, E., and R. Kujawiak. 1999. Antybiotykowe stymulatory This work was supported by grant PB 0848/P05/2005/29 from the wzrostu w produkcji drobiu. Pol. Drob. 6:17–18.
Polish Committee for Scientific Research and grant 50/04 from the Chil- Gotz, T. D., and B. A. Martin. 1991. Characterization of high-level quinolone resistance in Campylobacter jejuni. Antimicrob. AgentsChemother. 35:840–845.
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