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Tracking Campylobacter contamination along a broiler chicken production chain from the farm level to retail in China

https://doi.org/10.1016/j.ijfoodmicro.2014.04.023Get rights and content

Highlights

  • First tracking Campylobacter contamination in broiler production chain in China.

  • Provided evidence suggesting C. coli has become the predominant species in China.

  • Most (83.4%) of Campylobacter strains exhibited multi-drug resistance.

  • Campylobacter in retail meat was originated from fecal contamination in abattoir.

Abstract

This study was conducted to determine the prevalence and distribution of Campylobacter species along a broiler production chain from farm to retail, and to evaluate the antimicrobial resistance profile of Campylobacter isolates. A total of 259 Campylobacter isolates (C. jejuni n = 106, C. coli n = 153) were isolated from broiler ceca samples (72.5%, 103/142), broiler carcasses (34.1%, 46/135), and retail broiler meat (31.3%, 40/128) samples collected in Shanghai, China. Minimal inhibitory concentrations of six antimicrobials were determined using the agar dilution method. High prevalence of resistance to ciprofloxacin (C. jejuni: 99.1%;C. coli: 100%) and tetracycline (C. jejuni: 100%;C. coli: 98.7%) was detected among the C. jejuni and C. coli isolates. The vast majority of C. coli were resistant to clindamycin (92.2%), gentamicin (95.4%), and erythromycin (94.1%), but only 25.5%, 53.8%, and 16.0% of C. jejuni exhibited resistance to these three antimicrobials, respectively. In contrast, the prevalence of florfenicol resistance in C. jejuni (37.7%) was significantly higher than that in C. coli (7.8%) (P < 0.05). It is noteworthy that all Campylobacter isolates were resistant to one or more antimicrobials, and 71.7% of C. jejuni and 98.0% of C. coli isolates exhibited multi-drug resistance (resistant to three or more antimicrobials). Fifty-five C. jejuni and sixty C. coli isolates, selected from different production stages, species, and antimicrobial resistance patterns, were analyzed by pulsed field gel electrophoresis (PFGE), among which 15 unique PFGE patterns (PFGE patterns represented by a single strain) and 31 clusters (PFGE patterns represented by multiple strains) were detected. Furthermore, nearly all of the PFGE patterns of the Campylobacter strains isolated from retail broiler meats overlapped with those of the strains from ceca and slaughterhouse carcasses. Together, these findings revealed the high prevalence of Campylobacter species in a broiler chicken production chain, and the concerning situation of antimicrobial resistance in Campylobacter species. The findings also indicated that Campylobacter isolates from retail broiler meats were associated with fecal contamination in the slaughterhouse, underlying the need for improved measures for reducing carcass contamination in slaughter plants.

Introduction

Campylobacter species, especially C. jejuni and C. coli, are the most frequently identified foodborne bacteria causing gastroenteritis throughout the world (Coker et al., 2002). Although most campylobacteriosis occurs as self-limiting enteritis, more severe and long-lasting cases, particularly in immune-comprised patients, may require antibiotic treatment (Gibreel et al., 2004). The macrolides erythromycin and azithromycin are the antimicrobials of choice when therapeutic intervention is warranted. Other antibiotic options include fluoroquinolones (ciprofloxacin), aminoglycosides (gentamicin), and tetracyclines (Wardak et al., 2007). Campylobacter species are increasingly resistant to these clinically important antibiotics, which compromises clinical therapy and presents a major threat to public health (Anderson et al., 2001, Cox and Popken, 2006). Use of antimicrobials in animal husbandry contributes to the selection of antibiotic resistant Campylobacter strains that are transmitted to humans through the food chain (Radostits and Rubinstein, 2002).

Epidemiological studies have demonstrated that handling and consumption of contaminated poultry meat, particularly chicken products, are a major source of human Campylobacter species infections (Samuel et al., 2004, Wingstrand et al., 2006). Broiler chickens have been regarded as one of the main reservoirs of Campylobacter species, and the colonization level of Campylobacter species in broiler ceca can reach as high as 109 CFU/g (Stern et al., 2008). Carcass contamination usually occurs directly via leakage of intestinal contents during the slaughtering process (Elvers et al., 2011). Studies have been conducted to investigate the prevalence and antimicrobial susceptibility of poultry-associated Campylobacter species, and most of them have reported the emergence of resistant strains (Andersen et al., 2006, Osaili et al., 2011). In China, an active surveillance system to monitor the prevalence and antimicrobial resistance of Campylobacter species from farm to retail is not yet available, and little information has been reported on Campylobacter species in chicken (Chen et al., 2010). The prevalence and distribution of Campylobacter species along the broiler production chain are unknown in China, which hamper the implementation of interventions.

To collect information concerning Campylobacter in poultry production in China, this study tracked Campylobacter contamination in ceca, carcasses, and retail meats of a broiler production chain in Shanghai, China. The isolates were profiled for antimicrobial susceptibility, and PFGE was employed to explore the diversity and linkage of Campylobacter species isolates from different production stages.

Section snippets

Sample collection

The investigation was conducted during October and November of 2012 in a vertically-integrated commercial poultry production continuum in Shanghai, China, in which more than 1,000,000 broiler chickens were reared, slaughtered, and sold per year. A total of 142 broiler cecal samples (one from each broiler), representing samples of broiler at the farm level, were collected at a slaughterhouse after evisceration. One hundred and thirty-five whole broiler carcasses were also sampled at the end of

Incidence of Campylobacter species

Overall, 103 of the 142 (72.5%) cecal samples tested positive (Table 2) for Campylobacter species, and 17 of the 142 (12.0%) positive samples were positive for both C. jejuni and C. coli, indicating the high prevalence of Campylobacter in broiler ceca. Considering that only three colonies were picked from each positive plate, the real positive rate for both species might be even higher. A total of 157 Campylobacter isolates were obtained from ceca, including 69 C. jejuni and 88 C. coli. Among

Acknowledgements

This work was supported by Key Projects in the National Science & Technology Pillar Program during the Twelfth Five-year Plan Period (2012BAK01B02), the National Natural Science Foundation of China (U1031004), the Special Fund for Agro-scientific Research in the Public Interest (201203040), and the Research Fund for the Doctoral Program of Higher Education of China (20100008120001).

References (34)

  • O.M. Radostits et al.

    The therapeutic use of fluoroquinolones in poultry: The effect on Campylobacter and the potential human health consequences

    Int. J. Infect. Dis.

    (2002)
  • Clinical and Laboratory Standards Institute

    Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; informational supplement

    CLSI document M31-A3

    (2008)
  • A.O. Coker et al.

    Human campylobacteriosis in developing countries

    Emerg. Infect. Dis.

    (2002)
  • L.A.T. Cox et al.

    Quantifying potential human health impacts of animal antibiotic use: Enrofloxacin and macrolides in chickens

    Risk Anal.

    (2006)
  • K.T. Elvers et al.

    Molecular tracking, through processing, of Campylobacter strains colonizing broiler flocks

    Appl. Environ. Microbiol.

    (2011)
  • H.P. Endtz et al.

    Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine

    J. Antimicrob. Chemother.

    (1991)
  • D. Ewnetu et al.

    Prevalence and antimicrobial resistance of Campylobacter isolates from humans and chickens in Bahir Dar, Ethiopia

    Foodborne Pathog. Dis.

    (2010)
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