Amoxicillin / Clavulanic Acid and Cefotaxime Resistance in Salmonella Minnesota and Salmonella Heidelberg from Broiler Chickens

Document Type: Original Paper

Authors

1 Department of Veterinary Collective Health and Public Health, Faculty of Veterinary, Fluminense Federal University, Niterói, RJ, Brazil

2 Department of Bacteriology, Oswaldo Cruz Institute, Rio de Janeiro, RJ, Brazil

Abstract

This study investigated the resistance of various Salmonella strains to beta-lactam antibiotics. Salmonella Minnesota (36 strains) and Salmonella Heidelberg (24 strains) were isolated from broiler chickens and carcasses by the Disk Diffusion Test and resistance genes blaCTX-M-8, blaACC-1 and blaCMY-2 were detected by PCR. Of the 60 strains tested, 80% were resistant to at least one antibiotic. Specifically, 66.7% were resistant to amoxicillin/clavulanic acid and 75% were resistant to cefotaxime. Among the amoxicillin/clavulanic acid resistant strains, the blaCMY-2 gene was detected in 40%, blaACC-1 in 37.5% and blaCTX-M-8 in 7.5%. Among the cefotaxime resistant strains, we detected the genes blaCTX-M-8 in 13.3%, blaACC-1 in 33.3%, and blaCMY-2 in 31.1%. The presence of cefotaxime- and amoxicillin/clavulanic acid-resistant Salmonella in poultry, and the prevalence of extended spectrum betalactamases and AmpC-betalactamases in these strains are of huge concern to public health and economy.

Keywords


Alvarez M, Tran JH, Chow N & Jacoby GA. 2004. Epidemiology of conjugative plasmid-mediated AmpC β-lactamases in the United States. Antimicrobial Agents and Chemotherapy, 48: 533-537. DOI: 10.1128/AAC.48.2.533-537.2004
Andrysiak AK, Olson AB, Tracz DM, Dore K, Irwin R, Ng LK & Gilmour MW. 2008. Genetic characterization of clinical and agri-food isolates of multi drug resistant Salmonella enterica serovar Heidelberg from Canada. BMC Microbiology, 8: 89. DOI: 10.1186/1471-2180-8-89
ANVISA 2012. Relatório de pesquisa em vigilância sanitária de alimentos. Programa nacional de monitoramento da prevalência e da resistência bacteriana em frango. Agência Nacional de Vigilância Sanitária, Brasília, Brasil.
Ayres M, Ayres Júnior M, Ayres DL & Santos ADA. 2007. 5th Ed. Aplicações estatísticas nas áreas das ciências bio-médicas. Instituto Mamirauá. Belém. 364 Pages.
Bauer AW, Kirby WM, Sherris JC & Turck M. 1966. Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45: 493-496.
Brasil 2009. Instrução Normativa SDA nº 26, de 09 de julho de 2009. Regulamento Técnico para a fabricação, o controle de qualidade, a comercialização e o emprego de produtos antimicrobianos de uso veterinário. Ministério da Agricultura, Pecuária e Abastecimento.
Cantón R, González-Alba JM & Galán JC. 2012. CTX-M enzymes: origin and diffusion. Frontiers in Microbiology, 3:110. DOI: 10.3389/fmicb.2012.00110
Cardoso A, Kanashiro A, Stoppa G, Castro A, Luciano R & Tessari E. 2015. Ocorrência de Salmonella spp. em carcaças de frango provenientes de abatedouros do estado de São Paulo, Brasil, no período de 2000 a 2010. Revista Científica Eletrônica de Medicina Veterinária, 24: 1-12.
CDC. 2008. Salmonella surveillance: annual summary, 2006. Centers for Disease Control and Prevention. Department of Health and Human Services, Atlanta.
CDC. 2014. National Antimicrobial Resistance Monitoring System: enteric bacteria. 2012 Human isolates final report. Centers for Disease Control and Prevention. Department of Health and Human Services, Atlanta.
CLSI. 2013. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From animals; Approved Standard. 4th. VET01-A4. 33(7), 94 Pages.
Cortez ALL, Carvalho ACFB, Ikuno AA, Bürger KP & Vidal-Martins AMC. 2006. Resistência antimicrobiana de cepas de Salmonella spp. isoladas de abatedouros de aves. Arquivos do Instituto Biológico, 73: 157-163.
Decré D, Verdet C, Raskine L, Blanchard H, Burghoffer B, Philippon A, Sanson-Le-Pors MJ, Petit JC & Arlet G. 2002. Characterization of CMY-type β-lactamases in clinical strains of Proteus mirabilis and Klebsiella pneumoniae isolated in four hospitals in the Paris area. Journal of Antimicrobial Chemotherapy, 50: 681-688. DOI: 10.1093/jac/dkf193
Drieux L, Brossier F, Sougakoff W & Jarlier V. 2008. Phenotypic detection of extended-spectrum β-lactamase production in Enterobacteriaceae: review and bench guide. Clinical Microbiology and Infection, 14: 90-103. DOI: 10.1111/j.1469-0691.2007.01846.x
FDA. 2010. National Antimicrobial Resistance Monitoring System-enteric bacteria (NARMS): 2007 executive report. U.S. Food and Drug Administration. Department of Health and Human Services, Rockville.
Fernandes SA, Paterson DL, Ghilardi-Rodrigues ÂC, Adams-Haduch JM, Tavechio AT & Doi Y. 2009. CTX-M-2–producing Salmonella Typhimurium isolated from pediatric patients and poultry in Brazil. Microbial Drug Resistance, 15: 317-321. DOI: 10.1089/mdr.2009.0050
Folster JP, Pecic G, McCullough A, Rickert R, Whichard JM. 2011. Characterization of blaCMY-encoding plasmids among Salmonella isolated in the United States in 2007. Foodborne Pathogens and Disease, 8: 1289-1294. DOI: 10.1089/fpd.2011.0944
Freitas J. 2011. Evolução de sorovares Modelo de Banco de Cepas. Seminário Internacional de Salmonellose Aviária. Rio de Janeiro.
Gokul BN, Menezes GA & Harish BN. 2010. ACC-1 β-lactamase–producing Salmonella enterica serovar Typhi, India. Emerging Infectious Diseases, 16: 1170-1171. DOI: 10.3201/eid1607.091643
Grimm V, Ezaki S, Susa M, Knabbe C, Schmid RD & Bachmann TT. 2004. Use of DNA microarrays for rapid genotyping of TEM beta-lactamases that confer resistance. Journal of Clinical Microbiology, 42: 3766-3774. DOI: 10.1128/JCM.42.8.3766-3774.2004
Hammack T, Andrews WH & Jacobson A. 2014. USFDA bacteriological analytical manual. http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149.htm#Prep Accessed on January 29. 2017.
Hanson ND. 2003. AmpC β-lactamases: what do we need to know for the future? Journal of Antimicrobial Chemotherapy, 52: 2-4. DOI: 10.1093/jac/dkg284
Hoffmann M, Zhao S, Pettengill J, Luo Y, Monday SR, Abbott J, Ayers SL, Cinar HN, Muruvanda T, Li C, Allard MW, Whichard J, Meng J, Brown EW & McDermott PF. 2014. Comparative genomic analysis and virulence differences in closely related Salmonella enterica serotype Heidelberg isolates from humans, retail meats, and animals. Genome Biology and Evolution, 6: 1046–1068. DOI: 10.1093/gbe/evu079
Jouini A, Vinué L, Slama KB, Sáenz Y, Klibi N, Hammami S, Boudabous A & Torres C. 2007. Characterization of CTX-M and SHV extended-spectrum β-lactamases and associated resistance genes in Escherichia coli strains of food samples in Tunisia. Journal of Antimicrobial Chemotherapy 60: 1137-1141. DOI: 10.1093/jac/dkm316
Ktari S, Arlet G, Verdet C, Jaoua S, Kachrid A, Redjeb SB, Mahjoubi-Rhimi F & Hammami A. 2009. Molecular epidemiology and genetic environment of acquired blaACC-1 in Salmonella enterica serotype Livingstone causing a large nosocomial outbreak in Tunisia. Microbial Drug Resistance, 15: 279-286. DOI: 10.1089/mdr.2009.0035
Liakopoulos A, Geurts Y, Dierikx CM, Brouwer MSM, Kant A, Wit B, Heymans R, Pelt W & Mevius DJ. 2016. Extended-spectrum cephalosporin-resistant Salmonella enterica serovar heidelberg strains, the netherlands. Emerging Infectious Diseases, 22: 1257-1261. DOI: 10.3201/eid2207.151377
Mendonça N, Manageiro V, Robin F, Salgado MJ, Ferreira E, Caniça M & Bonnet R. 2008. The Lys234Arg substitution in the enzyme SHV-72 is a determinant for resistance to clavulanic acid inhibition. Antimicrobial Agents  and Chemotherapy, 52: 1806-1811. DOI: 10.1128/AAC.01381-07
Minharro S, Nascimento CA, Galletti JP, Merisse TJ, Feitosa ACF, Santos HD, Dias FEF, Santana ES, Baldani CD & Andrade MA. 2015. Antimicrobial susceptibility of Salmonella serovars isolated from edible offal and carcasses of slaughtered poultry in the state of Tocantins, Brazil. Semina: Ciências Agrárias, 36: 2661-2670.
Nadjar D, Rouveau M, Verdet C, Donay JL, Herrmann JL, Lagrange PH, Philippon A & Arlet G. 2000. Outbreak of Klebsiella pneumoniae producing transferable AmpC-type β-lactamase (ACC-1) originating from Hafnia alvei. FEMS Microbiology Letters, 187: 35-40. DOI:  10.1111/j.1574-6968.2000.tb09133.x
Pérez-Pérez FJ & Hanson ND. 2002. Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. Journal of Clinical Microbiology, 40: 2153-2162. DOI: 10.1128/JCM.40.6.2153-2162.2002
PHAC. 2014. Annual summary 2012. National Enteric Surveillance Program. Public Health Agency of Canada.
RASFF. 2014. The Rapid Alert System for Food and Feed. 2013 annual report. European Commission-Health and Food Safety. https://ec.europa.eu/food/sites/food/files/safety/docs/rasff_annual_report_2013.pdf Accessed on January 31. 2017.
RASFF. 2015. The Rapid Alert System for Food and Feed. 2014 annual report. European Commission-Health and Food Safety.   https://ec.europa.eu/food/sites/food/files/safety/docs/rasff_annual_report_2014.pdf Accessed on January 31. 2017.
Silva KC, Fontes LC, Moreno AM, Astolfi-Ferreira CS, Ferreira AJP & Lincopan N. 2013. Emergence of extended-spectrum-β-lactamase CTX-M-2-producing Salmonella enterica serovars Schwarzengrund and Agona in poultry farms. Antimicrobial Agents and Chemotherapy, 57: 3458-3459. DOI: 10.1128/AAC.05992-11
Voss-Rech D, Vaz CS, Alves L, Coldebella A, Leão JA, Rodrigues DP & Back A. 2015. A temporal study of Salmonella enterica serotypes from broiler farms in Brazil. Poultry Science, 94: 433-441. DOI: 10.3382/ps/peu081
WHO. 2016. Salmonella (non-typhoidal). Fact sheet Nº 139. http://www.who.int/mediacentre/factsheets/fs139/en/ Accessed on January 31. 2017.