Characteristics and antimicrobial resistance of Campylobacter isolated from pig and cattle carcasses in Poland

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Abstract

A total of 70 Campylobacter isolates recovered from 114 cattle and 177 pig carcasses at the slaughterhouse level were characterized by the presence of 7 putative virulence genes and antimicrobial susceptibility using the microbroth dilution method and minimal inhibitory concentration (MIC). The prevalence of Campylobacter was 14.9% and 29.9% in cattle and pig samples, respectively. The majority of cattle carcasses were contaminated with C. jejuni (64.7%), whereas pig carcasses were mainly positive for C. coli (77.4%). Most of the strain, irrespective of origin, possessed at least one pathogenic gene marker tested, mainly flaA and cadF genes responsible for motility and adherence to host epithelial cells, respectively. Several isolates also possessed the cdtA and cdtB genes responsible for the production of cytolethal distending toxin. Antibiotic profiling showed that campylobacters were most frequently resistant to quinolones (nalidixic acid and ciprofloxacin, total 57.1% of isolates) followed by streptomycin (52.9%, only C. coli strains) and tetracycline (51.4%). Resistance to erythromycin was demonstrated only in 4 C. coli strains of pig origin. None of the isolates, irrespective of origin, was resistant to gentamycin. Multi-resistance patterns, defined as resistance to antimicrobials of at least two different classes, were observed among 65.4% of the isolates, mainly C. coli recovered from pig carcasses.

Aarestrup FM, Engberg J (2001) Antimicrobial resistance of thermophilic Campylobacter. Vet Res 32: 311-321.

Anon (2012) European Food Safety Authority, European Centre for Disease Prevention and Control; the European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA Journal 10: 2597 (pp 442).

Bae W, Hancock DD, Call DR, Park YH, Berge AC, Finger RM, Sischo WM, Besser TE (2007) Dissemination of antimicrobial resistant strains of Campylobacter coli and Campylobacter jejuni among cattle in Washington State and California. Vet Microbiol 122: 306-315.

Bae W, Kaya KN, Hancock DD, Call DR, Park YH, Besser TE (2005) Prevalence and antimicrobial resistance of thermophilic Campylobacter spp. from cattle farms in Washington State. Appl Environ Microbiol 71: 169-174.

Bang DD, Nielsen EM, Scheutz F, Pedersen K, Handberg K, Madsen M (2003) PCR detection of seven virulence and toxin genes of Campylobacter jejuni and Campylobacter coli isolates from Danish pigs and cattle and cytolethal distending toxin production of the isolates. J Appl Microbiol 94: 1003-1014.

Beach JC, Murano EA, Acuff GR (2002) Prevalence of Salmonella and Campylobacter in beef cattle from transport to slaughter. J Food Prot 65: 1687-1693.

Bohaychuk VM, Gensler GE, Barrios PR (2011) Microbiological baseline study of beef and pork carcasses from provincially inspected abattoirs in Alberta, Canada. Can Vet J 52: 1095-1100.

Chaˆtre P, Haenni M, Meunier D, Botrel MA, Calavas D, Madec JY (2010) Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from cattle between 2002 and 2006 in France. J Food Prot 73: 825-831.

Datta S, Niwa H, Itoh K (2003) Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains isolated from humans, poultry meat and broiler and bovine faeces. J Med Microbiol 52: 345-348.

Egger R, Korczak BM, Niederer L, Overesch G, Kuhnert P (2012) Genotypes and antibiotic resistance of Campylobacter coli in fattening pigs. Vet Microbiol 155: 272-278.

Endtz HP, Ruijs G J, van Klingeren B, Jansen WH, van der Reyden T, Mouton RP (1991) Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother 27: 199-208.

Englen MD, Hill AE, Dargatz DA, Ladely SR, Fedorka-Cray PJ (2007) Prevalence and antimicrobial resistance of Campylobacter in US dairy cattle. J Appl Microbiol 102: 1570-1577.

Fernandes M, Mena C, Silva I, Teixeira P (2010) Study of cytolethal distending toxin (cdt) in Campylobacter coli using a multiplex polymerase chain reaction assay and its distribution among clinical and food strains. Foodborne Path Dis 7: 103-106.

Garcia MM, Lior H, Stewart RB, Ruckerbauer GM, Trudel JR, Skljarevski A (1985) Isolation, characterization, and serotyping of Campylobacter jejuni and Campylobacter coli from slaughter cattle. Appl Environ Microbiol 49: 667-672.

Ghafir Y, China B, Dierick K., De Zutter L, Daube G (2007) A seven-year survey of Campylobacter contamination in meat at different production stages in Belgium. Int J Food Microbiol 116: 111-120.

Gillespie IA, O’Brien SJ, Frost JA, Adak GK, Horby P, Swan AV, Painter MJ, Neal KR (2002) A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg Infect Dis 8: 937-942.

Hakkinen M, Heiska H, Ha¨nninen ML (2007) Prevalence of Campylobacter spp. in cattle in Finland and antimicrobial susceptibilities of bovine Campylobacter jejuni strains. Appl Environ Microbiol 73: 3232-3238.

Inglis GD, Kalischuk LD, Busz HW (2004) Chronic shedding of Campylobacter species in beef cattle. J Appl Microbiol 97: 410-420.

Keener KM, Bashor MP, Curtis PA, Sheldon BW, Kathariou S (2004) Comprehensive review of Campylobacter and poultry processing. Comp Rev Food Sci Food Safety 3: 105-116.

Krutkiewicz A, Klimuszko D (2010) Genotyping and PCR detection of potential virulence genes in Campylobacter jejuni and Campylobacter coli isolates from different sources in Poland. Folia Microbiol (Praha) 55: 167-175.

Krutkiewicz A, Sałamaszyńska-Guz A, Rzewuska M, Klimuszko D, Binek M (2009) Resistance to antimicrobial agents of Campylobacter spp. strains isolated from animals in Poland. Pol J Vet Sci 12: 465-472.

Leatherbarrow AJ, Hart CA, Kemp R, Williams NJ, Ridley A, Sharma M, Diggle PJ, Wright EJ, Sutherst J, French NP (2004) Genotypic and antibiotic susceptibility characteristics of a Campylobacter coli population isolated from dairy farmland in the United Kingdom. Appl Environl Microbiol 70: 822-830.

Lindblad M, Lindmark H, Lambertz ST, Lindqvist R (2007) Microbiological baseline study of swine carcasses at Swedish slaughterhouses. J Food Prot 70: 1790-1797.

Little CL, Richardson JF, Owen RJ, de Pinna E, Threlfall EJ (2008) Campylobacter and Salmonella in raw red meat in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003-2005. Food Microbiol 25: 538-543.

Mayrhofer S, Paulsen P, Smulders FJ, Hilbert F (2004) Antimicrobial resistance profile of five major food-borne pathogens isolated from beef, pork and poultry. Int J Food Microbiol 97: 23-29.

Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV (1999) Food-related illness and death in the United States. Emerg Infect Dis 5: 607-625.

Mu¨ller J, Schulze F, Mu¨ller W, Ha¨nel I (2006) PCR detection of virulence-associated genes in Campylobacter jejuni strains with differential ability to invade Caco-2 cells and to colonize the chick gut. Vet Microbiol 113: 123-129.

Ono K, Yamamoto K (2009) Contamination of meat with Campylobacter jejuni in Saitama, Japan. Int J Food Microbiol 47: 211-219.

Qin SS, Wu CM, Wang Y, Jeon B, Shen ZQ, Wang Y, Zhang Q, Shen JZ (2011) Antimicrobial resistance in Campylobacter coli isolated from pigs in two provinces in China. Int J Food Microbiol 146: 94-98.

Quintana-Hayashi MP, Thakur S (2012) Longitudinal study of the persistence of antimicrobial-resistant Campylobacter strains in distinct swine production systems on farms, at slaughter, and in the environment. Appl Environ Microbiol 78: 2698-2705.

Rozynek E, Dzierzanowska-Fangrat K, Jozwiak P, Popowski J, Korsak D, Dzierzanowska D (2005) Prevalence of potential virulence markers in Polish Campylobacter jejuni and Campylobacter coli isolates obtained from hospitalized children and from chicken carcasses. J Med Microbiol 54: 615-619.

Rozynek E, Dzierzanowska-Fangrat K, Korsak D, Konieczny P, Wardak S, Szych J, Jarosz M, Dzierzanowska D (2008) Comparison of antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from humans and chicken carcasses in Poland. J Food Prot 71: 602-607.

Sheppard SK, Dallas JF, MacRae M, McCarthy ND, Sproston EL, Gormley FJ, Strachan NJ, Ogden ID, Maiden MC, Forbes KJ (2009) Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. Int J Food Microbiol 134: 96-103.

Shin E, Lee Y (2007) Antimicrobial resistance of 114 porcine isolates of Campylobacter coli. Int J Food Microbiol 118: 223-227.

Smole Mozˇina S, Kurincˇicˇ M, Klancˇnik A, Mavri A (2011) Campylobacter and its multi-resistance in the food chain. Trends Food Sci Technol 22: 91-98.

Stanley KN, Wallace JS, Currie JE, Diggle PJ, Jones K (1998) The seasonal variation of thermophilic campylobacters in beef cattle, dairy cattle and calves. J Appl Microbiol 85: 472-480.

Szygalski Biasi R, Ernlund Freitas de Macedo R, Scaranello Malaquias MA, Franchin PR (2011) Prevalence, strain identification and antimicrobial resistance of Campylobacter spp. isolated from slaughtered pig carcasses in Brazil. Food Control 22: 702-707.

Tam CC, O’Brien SJ, Adak GK, Meakins SM, Frost JA (2003) Campylobacter coli - an important foodborne pathogen. J Infect 47: 28-32.

Thakur S, Gebreyes WA (2005) Campylobacter coli in swine production: antimicrobial resistance mechanisms and molecular epidemiology. J Clin Microbiol 43: 5705-5714.

Wang G, Clark CG, Taylor TM, Pucknell C, Barton C, Price L, Woodward DL, Rodgers FG (2002) Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol 40: 4744-4747.

Wieczorek K (2010) Antimicrobial resistance and virulence markers of Campylobacter jejuni and Campylobacter coli isolated from retail poultry meat in Poland. Bull Vet Inst Pulawy 54: 563-569.

Wieczorek K, Denis E, Lynch O, Osek J (2013) Molecular characterization and antibiotic resistance profiling of Campylobacter isolated from cattle in Polish slaughterhouses. Food Microbiol 34: 130-136

Wieczorek K, Osek J (2005) Multiplex PCR assays for simultaneous identification of Campylobacter jejuni and Campylobacter coli. Med Weter 61: 797-799.

Wieczorek K, Osek J (2010) Simultaneous occurrence of selected food-borne bacterial pathogens on bovine hides, carcasses and beef meat. Pol J Vet Sci 13: 645-651.

Yeh KS, Chen SP, Lin JH (2003) One-year (2003) nationwide pork carcass microbiological baseline data survey in Taiwan. J Food Prot 68: 458-461.

Polish Journal of Veterinary Sciences

The Journal of Committee of Veterinary Sciences of Polish Academy of Sciences and University of Warmia and Mazury in Olsztyn

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