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Prevalence and Antimicrobial Resistance of Campylobacter Jejuni and Campylobacter Coli Isolated from Raw Chicken Meat and Human Stools in Korea

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Prevalence and Antimicrobial Resistance of Campylobacter Jejuni and Campylobacter Coli Isolated from Raw Chicken Meat and Human Stools in Korea 2915 Journal of Food Protection, Vol. 69, No. 12, 2006, Pages 2915–2923 Copyright ᮊ, International Association for Food Protection Prevalence and Antimicrobial Resistance of Campylobacter jejuni and Campylobacter coli Isolated from Raw Chicken Meat and Human Stools in Korea YUN-SOOK KANG,1,2 YONG-SUN CHO,3 SUN-KYUNG YOON,1 MYEONG-AE YU,4 CHANG-MIN KIM,5 JONG-OK LEE,2 AND YU-RYANG PYUN1* 1Department of Biotechnology, Yonsei University, Seoul, 120-749, Korea; 2Korea Food and Drug Administration Seoul, 122-704, Korea; 3Food Analysis Research Team, Korea Food Research Institute, Gyunggi-do, 463-746, Korea; 4International Life Sciences Institute of Korea, Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/12/2915/2002244/0362-028x-69_12_2915.pdf by guest on 26 September 2021 Seoul, 150-889, Korea; and 5Dongwon F&B Food R&D Center, Gyunggi-do, 462-120, Korea MS 05-524: Received 17 October 2005/Accepted 9 May 2006 ABSTRACT Prevalence of Campylobacter in raw chicken meat and human stools and subsequent antibiotic resistance profiles of the pathogenic isolates obtained from 2000 through 2002 were investigated. Campylobacter jejuni and Campylobacter coli were isolated from 570 of the 923 raw chicken meat samples collected from traditional markets, large retail stores, or department stores in Korea, resulting in the isolation rate of 61.8%. A total of 579 Campylobacter isolates were obtained from raw chicken (36.3% for C. jejuni and 26.4% for C. coli) with the average population of 335.6 CFU/g. From 513 human stool samples, 15 isolates of Campylobacter were detected. Seasonal variation in the quantification of C. coli was not noticeable throughout the year, while the isolation rate of C. jejuni was the highest in September through October (840 CFU/g) followed by that of July through August and May through June in decreasing order, showing a significant seasonal effect (P Ͻ 0.05). Contamination of Campylobacter was more severe in raw chicken meat sold in traditional markets than in those sold in large retail stores and department stores. Prevalence of Campylobacter in raw chicken sold in traditional markets was significantly influenced by seasonal changes (P Ͻ 0.05), whereas the samples obtained from other places was less affected by the seasonal changes. Susceptibilities of the 594 chicken isolates to ciprofloxaxin, chloramphenicol, erythromycin, kanamycin, nalidixic acid, and tetracycline were determined by an E-test. Campylobacter isolates were the most resistant to nalidixic acid (91.4%) followed by ciprofloxaxin (87.9%), tetracycline (87.2%), kanamycin (30.6%), erythromycin (19.4%), and chloramphenicol (1.3%). Hu- man isolates showed a similar resistance to the six antibiotics tested. The proportion of Campylobacter isolates with multidrug resistance to four or more antimicrobials obtained from 2000 through 2002 ranged from 28 to 43.5%, indicating that it could be a serious health-threatening factor. This study suggests that it is prudent to establish an effective National Monitoring Program in Korea for the prevention and control of Campylobacter spp. Campylobacteriosis characterized by diarrhea, fever, Campylobacter and Salmonella, major human pathogens and abdominal cramps is the most common bacterial gas- worldwide, share common food vehicles in sporadic human troenteritidis in humans and animals worldwide. Over 2.4 infection (3). Poultry meat, especially undercooked and million human infections per year have been estimated in cross-contaminated with ready-to-eat foods, has been the the United States alone (1). Although campylobacteriosis is major cause of Campylobacter and Salmonella infections the most common infectious disease in the United States (3). In The Netherlands, 61% of raw chicken products were and other regions of the world, it has been rarely reported contaminated with C. jejuni, which was due to cross-con- in Korea, possibly because of fastidious culture conditions tamination during food preparation via cutting boards, of the pathogen, which made it overlooked in the past. plates, and food handlers (5). Approximately 71% of raw Since foodborne campylobacteriosis was first reported in retail chickens sold in the United Kingdom were contami- 2001, however, a few outbreaks have been continuously nated with Campylobacter spp. while only 8% of the chick- occurring in Korea (14), which implies that preventative en meat harbored Salmonella (20). It was reported that of and control measures for the illness are required. 415 raw poultry meat samples sold in Switzerland, the path- The causative microorganism, Campylobacter, has ogens were detected from 91 samples with a contamination been the most common infectious agent transmitted to hu- rate of 21.9% (17). mans via raw meats and poultry (22). Campylobacter spe- Antibiotic susceptibility of Campylobacter spp. has cies of clinical importance include jejuni, coli, lari, fetus, been examined for effective clinical treatment of campy- and upsaliensis, among which C. jejuni and C. coli are lobacteriosis (1, 5, 6). Among the antibiotics, either a fluo- mainly implicated to foodborne disease of humans (21, 22). roquinolone, such as ciprofloxacin, or a macrolide is the drug of choice for the therapeutic treatment of Campylo- * Author for correspondence. Tel: ϩ82-2-2123-4098; Fax: ϩ82-2-362- bacter gastroenteritis (10). Fluoroquinolone antibiotics that 7265; E-mail: [email protected]. were first approved for the use in humans in 1986 in the 2916 KANG ET AL. J. Food Prot., Vol. 69, No. 12 United States were also approved for the use in poultry in posed of Bolton broth base (9.5 ml), 1 ml of fetal bovine serum 1995. Campylobacter isolates resistant to fluoroquinolones (filtered, 0.22 ␮M), and 1 ml of glycerol (10%). have been detected from both humans and poultry in most Samples. Raw chicken meat was purchased from small local regions of world and have been increasing in the regions markets, large retail stores, or department stores in Seoul, Daejon, where the antibiotics were abused (13). In recent years, ex- Busan, and Gwangju in Korea from March 2000 through Decem- tensive researches have been carried out to investigate the ber 2002. Human stool samples were obtained from patients with antibiotic resistance of Campylobacter, revealing informa- diarrhea who visited hospitals in Seoul and Jeolla Nam-do from tion that may be used to reduce the resistance of the path- January 2000 through December 2001. A total of 923 raw chicken ogen to therapeutic drugs (1, 2). meat and 513 human stool samples were collected and examined In this study, we investigated the prevalence of C. je- for the presence of Campylobacter species. Samples were stored Ͻ Њ juni and C. coli in raw chicken meat from 2000 through at refrigerated temperatures ( 5 C) until examination. Seasonal temperatures at the time of sample purchases were recorded for 2002, which can be used for estimating potential risk of calculating the average temperature for each 2-month period. The Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/12/2915/2002244/0362-028x-69_12_2915.pdf by guest on 26 September 2021 foodborne campylobacteriosis in Korea. Human stool sam- average temperatures measured and calculated throughout the year ples were also monitored for the presence of Campylobac- were then used as the temperature of seasonal bimonthly periods. ter spp. in order to determine whether there might be any relationship between the food contamination level and clin- Strain isolation and identification. From each raw chicken ical implications. Among the food supply chains, raw sample, 25 g cut from the surface was added to 100 ml of selective chickens sold through traditional markets were expected to broth (e.g., Bolton broth) containing Campylobacter selective sup- plement (5% lysed horse blood and four antibiotics mentioned be highly contaminated. Therefore, prevalence of Campylo- above) and homogenized using a stomacher (model 400, Norfolk, bacter in raw chickens sold in three different retail places, UK). The mixture was preincubated at 35ЊC for 4 h under mi- including traditional markets, large retail stores, and de- croaerobic conditions and subsequently at 42ЊC for 24 to 48 h partment stores, was examined throughout different seasons under the same conditions. Human stool samples were subjected when temperature changes were distinct among other en- without further enrichment to the isolation procedure. vironmental factors. The results would contribute to the de- Enriched cultures were streaked onto Abeyta-Hunt agar con- velopment and enforcement of preventative and control taining antibiotic supplement and incubated microaerobically for measures that can effectively reduce the contamination of 24 to 48 h. Translucent white, moist, and glistening colonies, typ- raw chickens during distribution, storage, and sales. Anti- ical of Campylobacter, were selected and streaked onto Abeyta- biotic susceptibility and multidrug resistance of both chick- Hunt agar with antibiotic supplement. Campylobacter colonies were selected and used for further identification using biochemical en and clinical isolates were examined using six antibiotics tests. Gram staining, catalase and oxidase reactions, and hippurate that have been applied for food animals as well as for the tests were carried out for the identification as previously described clinical treatment of human infection in Korea. Results on (19). API Campy Kit (bioMe´rieux, Inc., Marcy l’Etoile, France) the antibiotic resistance profiles of Campylobacter isolates was
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