Isolation and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli found in chilled chicken carcasses in the Federal District Region and surrounding areas

Patricia Renault Silva, Joana Marchesini Palma, Nara Rubia Souza, Helenira Melo de Moura, Simone Perecmanis, Angela Patricia Santana

Abstract


This study aimed to isolate Campylobacter jejuni and Campylobacter coli from chilled chicken carcasses marketed in the Federal District Region and surrounding areas, as well as to detect the occurrence of antimicrobial resistance and genes responsible for the same. A total of 105 chilled chicken carcasses were collected, of which 7 (6.67%) were positive for C. jejuni and 4 (3.81%) were positive for C. coli. These results were obtained using both the conventional microbiological isolation method and polymerase chain reaction assays. All of the positive strains were subjected to antimicrobial susceptibility testing for seven antimicrobials. The resistance incidences found in the C. jejuni strains were as follows: 71.43% for tetracycline and nalidixic acid, 42.86% for streptomycin and gentamicin, 57.14% for ciprofloxacin and erythromycin, and 28.57% for chloramphenicol. Among the C. coli strains, 100% were resistant to tetracycline and streptomycin, 75% were resistant to erythromycin, 50% were resistant to ciprofloxacin, gentamicin, and nalidixic acid, and no strains were resistant to chloramphenicol. While analyzing the presence of antimicrobial resistance genes in the isolated C. jejuni strains, the aph3-1 (resistance to aminoglycosides), aadE (resistance to streptomycin), and tet(O) (resistance to tetracycline) genes were identified, with occurrence rates of 57.14%, 28.57%, and 42.86%, respectively, whereas in the C. coli strains, there was a 25% occurrence rate for both the aph3-1 and tet(O) genes. The aadE gene was not found in the C. coli isolates. The results of this study demonstrated the presence of C. jejuni and C. coli in chilled chicken carcasses marketed in the Federal District Region and surrounding areas, as well as the antimicrobial resistance and the presence of resistance genes in these bacteria, which may pose threats to public health.

Keywords


Antimicrobial resistance; Campylobacter coli; Campylobacter jejuni; Chilled chicken carcass; Resistance gene.

Full Text:

PDF

References


AARESTRUP, F. M. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic & Clinical Pharmacology & Toxicology, Copenhagen, v. 96, n. 4, p. 271-281, 2005. DOI: 10.1111/j.1742-7843.2005.pto960401.x

AARESTRUP, F. M.; ENGBERG, J. Antimicrobial resistance of thermophilic campylobacter. Veterinary Research, Paris, v. 32, n. 3-4, p. 311-321, 2001. DOI: 10.1051/vetres:2001127.

BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa nº 9, de 27 de junho de 2003. Proíbe a fabricação, a manipulação, o fracionamento, a comercialização, a importação e o uso dos princípios ativos cloranfenicol, nitrofuranos e os produtos que contenham Estes princípios ativos, para uso veterinário e suscetível de emprego na alimentação de todos os animais e insetos. Diário Oficial [da] União, Brasília, 30. jun. 2003. 1, seção 1, p. 4.

CORTEZ, A. L. L.; CARVALHO, A. C. F. B.; SCARCELLI, E.; MIYASHIRO, S.; VIDAL-MARTINS, A. M. C.; BÜRGER, K. P. Survey of chicken abattoir for the presence of Campylobacter jejuni and Campylobacter coli. Revista do Instituto de Medicina Tropical de São Paulo, São Paulo, 48, n. 6, p. 307-310, 2006. DOI: 10.1590/S0036-46652006000600001

ENGBERG, J.; AARESTRUP, F. M.; TAYLOR, D. E.; GERNER-SMIDT, P.; NACHAMKIN, I. Quinolone and Macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerging Infectious Diseases, Atlanta, v. 7, n. 1, p. 24-34, 2001. DOI: 10.3201/eid0701.010104

ENGLEN, M. D.; HILL, A. E.; DARGATZ, D. A.; LADELY, S. R.; FEDORKA-CRAY, P. J. Prevalence and antimicrobial resistance of campylobacter in US dairy cattle. Journal of Applied Microbiology, Oxford, v. 102, n. 6, p. 1570-1577, 2007. DOI: 10.1111/j.1365-2672.2006.03189.x

EUROPEAN FOOD SAFETY AUTHORITY - EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. Parma: EFSA J., 2016. 4634 p.

FÀBREGA, A.; SÁNCHEZ-CÉSPEDES, J.; SOTO, S.; VILA, J. Quinolone resistance in the food chain. International Journal of Antimicrobial Agentes, Amsterdam, v. 31, n. 4, p. 307-315, 2008. DOI: 10.1016/j.ijantimicag.2007.12.010

FERNÁNDEZ, H.; PISÓN, V. Isolation of thermotolerant species of campylobacter from commercial chicken livers. International Journal of Antimicrobial Agentes, Amsterdam, v. 29, n. 1, p. 75-80, 1996. DOI: 10.1016/0168-1605(95)00023-2

FOOD STANDARDS AGENCY, UNITED KINGDOM - FSA. Foodborne disease strategy 2010-15. Londres 2011. Available at: www.food.gov.uk/multimedia/pdfs/fds2015.pdf. Accessed at: 20 apr. 2018.

FREDIANI-WOLF, V.; STEPHAN, R. Resistance patterns of Campylobacter spp. strains isolated from poultry carcasses in a big Swiss poultry slaughterhouse. International Journal of Food Microbiology, Amsterdam, v. 89, n. 2-3, p. 233-240, 2003. DOI: 10.1016/S0168-1605(03)00152-1

FRYE, J. G.; LINDSEY, R. L.; MEINERSMANN, R. J.; BERRANG, M. E.; JACKSON, C. R.; ENGLEN, M. D.; TURPIN, J. B.; FEDORKA-CRAY, P. J. Related antimicrobial resistance genes detected in different bacterial species co-isolated from swine fecal samples. Foodborne Pathogens and Disease, New Rochelle, v. 8, n. 6, p. 663-679, 2011. DOI: 10.1089/fpd.2010.0695

GIACOMELLI, M.; SALATA, C.; MARTINI, M.; MONTESISSA, C.; PICCIRILLO, A. Antimicrobial resistance of Campylobacter jejuni and Campylobacter coli from poultry in Italy. Microbial Drug Resistance, Larchmont, v. 20, n. 2, p. 181-188, 2014. DOI:10.1089/mdr.2013.0110.

GIBREEL, A. D.; TAYLOR, E. Macrolide resistance in Campylobacter jejuni and Campylobacter coli. Journal of Antimicrobial Chemotherapy, Londres, v. 58, n. 2, p. 243-255, 2006. DOI: 10.1093/jac/dkl210

HAN, K.; JANG, S. S.; CHOO, E.; HEU, S.; RYU, S. Prevalence, genetic diversity, and antibiotic resistance patterns of Campylobacter jejuni from retail raw chickens in Korea. International Journal of Food Microbiology, Amsterdam, v. 114, n. 1, p. 50-59, 2007. DOI: 10.1016/j.ijfoodmicro.2006.10.042

HÄNNINEN, M. L.; HANNULA, M. Spontaneous mutation frequency and emergence of ciprofloxacin resistance in Campylobacter jejuni and Campylobacter coli. Journal of Antimicrobial Chemotherapy, Londres v. 60, n. 6, p. 1251-1257, 2007. DOI: 10.1093/jac/dkm345

HARVEY, R. B.; YOUNG, C. R.; ZIPRIN, R. I.; HUME, M. E.; GENOVESE, K. J.; ANDERSON, R. C.; DROLESKEY, R. E.; STANKER, L. H.; NISBET, D. J. Prevalence of campylobacter spp. isolated from the intestinal tract of pigs raised in an integrated swine production system. Journal of the American Veterinary Medical Association, Schaumburg, v. 215, n. 11 p. 1601-1604, 1999.

IOVINE, N. M. Resistance mechanisms in Campylobacter jejuni. Virulence, v. 4, n. 3, p. 230-240, 2013. DOI: 10.4161/viru.23753

ISHIHARA, K.; KIRA, T.; OGIKUBO, K.; MORIOKA, A.; KOJIMA, A.; KIJIMA-TANAKA, M.; TAKAHASHI, T.; TAMURA, Y. Antimicrobial susceptibilities of Campylobacter isolated from food-producing animals on farms (1999-2001): results from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. International Journal of Antimicrobial Agents, v.24, n. 3, p. 63-69, 2004. DOI: 10.1016/j.ijantimicag.2004.03.017

JAMALI, H.; GHADERPOUR, A.; RADMEHR, B.; CHUAN, W. K. S.; CHAI, L. C.; ISMAIL, S. Prevalence and antimicrobial resistance of campylobacter species isolates in ducks and geese. Food Control, Vurrey, v. 50, p. 328-330, 2015. DOI: 10.1016/j.foodcont.2014.09.016

KANG, Y. S.; CHO, Y. S.; YOON, S. K.; YU, M. A.; KIM, C. M.; O LEE, J.; PYUN, Y. R. Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from raw chicken meat and human stools in Korea. Journal of Food Protection, v. 69, n. 12, p. 2915-2923, 2006.

KASHOMA, I. P.; KASSEM, I. I.; JOHN, J.; KESSY, B. M.; GEBREYES, W.; KAZWALA, R. R.; RAJASHEKARA, G. Prevalence and antimicrobial resistance of campylobacter isolated from dressed beef carcasses and raw milk in Tanzania. Microbial Drug Resistance, Larchmont, v. 22, n. 1, p. 40-52, 2015. DOI: 10.1089/mdr.2015.0079

KUDIRKIENÈ, E.; BUNEVICIENE, J.; BRONDSTED, L.; INGMER, H.; OLSEN, J. E.; MALAKAUSKAS, M. Evidence of broiler meat contamination with post-desinfection strains of Campylobacter jejuni from slaughterhouse. International Journal of Food Microbiology, Amsterdam, v. 45, n. 1, p. 116-120, 2011. DOI: 10.1016/j.ijfoodmicro.2010.06.024




DOI: http://dx.doi.org/10.5433/1679-0359.2019v40n5Supl1p2247

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433 / 1679-0359
E-mail:  semina.agrarias@uel.br
Este obra está licenciado com uma Licença  Creative Commons Atribuição-NãoComercial 4.0 Internacional .