Abstract
Serotypes and antimicrobial susceptibility of Salmonella’s isolates from broiler production chain were determined. A total of 239 isolated strains from chicken, carcasses, breeding environments, and slaughter was analyzed by disk diffusion test, in the period of 2009 to 2010. For antibiotics with a high number of resistant strains, the minimal inhibitory concentration (MIC) was performed. We identified 24 serotypes, being the most frequent, Minnesota (31.4%) and Infantis (22.6%). The highest percentages of resistance were obtained for sulfonamide (42.7%), followed by tetracycline with 37.6% and amoxicillin with 27.6%. From the total, 32 resistance profiles were identified, being 60.7% of the strains were resistant to at least one antibiotic. Of these, 31.7% of the isolates showed multidrug resistance profiles belonging to serovar Minnesota, Saintpaul, and S. enterica. The highest resistance was found in isolates from slaughterhouse (66.9%) and aviary (58.7%). A large number of strains showed MIC above the maximum tested concentration for the antibiotics amoxicillin and sulfamethoxazole. The high number of Salmonella’s resistant strains indicates the need for prudent use of these drugs in poultry production in order to reduce the occurrence and spread of antibiotic resistance profiles, and the risk that multiresistant strains isolated from broilers may pose a risk to human health.
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References
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7–15
Shao D, Shi Z, Wei J, Ma Z (2011) A brief review of foodborne zoonosis in China. Epidemiol Infect 139:1497–1504
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra RM, International Collaboration on Enteric Disease ‘Burden of Illness’ Studies (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889
Brasil (2008) Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Manual integrado de vigilância e controle da febre tifoide. Brasília: Editora do Ministério da Saúde, 92 p. (Série A. Normas e Manuais Técnicos). Available at: http://bvsms.saude.gov.br/bvs/publicacoes/manual_vigilancia_controle_febre_tifoidel.pdf. Accessed 14.02.2017
CDC (2009) Centers for Disease Control and Prevention. National Salmonella Surveillance Annual Summary. p 1–96, Available at http://www.cdc.gov/ncezid/dfwed/PDFs/SalmonellaAnnualSummaryTables2009.pdf. Accessed 24.03.2016
WHO. World Health Organization. Food safety and foodborne illness. 2002. Available at: http://www.who.int/mediacentre/factsheets/fs237/en/print.html. Accessed 15.08.2015
EFSA. European Food Safety Authority (2008) Scientific opinion of the panel on biological hazards on a request from the European Food Safety Authority on foodborne antimicrobial resistance as a biological hazard. EFSA J 765:1–87
WHO. World Health Organization (2004) 1st Joint FAO/OIE/WHO Expert workshop on non-human antimicrobial usage and antimicrobial resistance: scientific assessment, Geneva, pp 1–5 December 2003. Available at: http://www.who.int/foodsafety/publications/micro/nov2003/en/. Accessed 21.02.2015
Jay JM, Loessner MJ, Golden DA (2005) Modern food microbiology, 7th edn. Springer, New York
Le Hello S, Hendriksen RS, Doublet B et al (2011) International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infect Dis 204(5):675–684
Ungemach FR, Müller-Bahrdt D, Abraham G (2006) Guidelines for prudent use of antimicrobials and their implications on antibiotic usage in veterinary medicine. Int J Med Microbiol 296:33–38
Thakur S, Brake J, Keelara S, Zou M, Susick E (2013) Farm and environmental distribution of Campylobacter and Salmonella in broiler flocks. Res Vet Sci 94:33–42
Brasil (2003) Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa n. 70, de 6 de outubro de 2003. Institui o Programa de Redução de Patógenos Monitoramento Microbiológico e Controle de Salmonella sp. em Carcaças de Frangos e Perus. Available at: http://extranet.agricultura.gov.br/sislegis-consulta/consultarLegislacao.do?operacao=visualizar&id=3136. Accessed 12.08.2015
Grimont PAD, Weill FX. Antigenic formulae of the Salmonella serovars. Paris: WHO Collaborating Centre for reference and research on Salmonella; 2007
CLSI (2013) Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing: twenty-third informational supplement. CLSI M100-S23, Wayne
Brasil (2008) Ministério da Saúde. Agência Nacional de Vigilância Sanitária - Anvisa. Relatório do Monitoramento da Prevalência e do Perfil de Suscetibilidade aos Antimicrobianos em Enterococos e Salmonelas Isolados de Carcaças de Frango Congeladas Comercializadas no Brasil. Programa Nacional de Monitoramento da Prevalência e da Resistência Bacteriana em Frango (PREBAF). Brasília,. 186 p
Brasil (2009) Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa N° 26, de 09 de julho de 2009. Aprova o regulamento técnico para a fabricação, o controle de qualidade, a comercialização e o emprego de produtos antimicrobianos de uso veterinário. Diário Oficial da União, seção 1, p. 14
Berchieri A Jr, Freitas Neto OC (2009) Salmoneloses. In: Berchieri A Jr et al (eds) Doenças das aves, 2nd edn. FACTA, Campinas, pp 435–454
Brasil (2003) Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa n. 78, de 3 de novembro de 2003. Aprova as Normas Técnicas para Controle e Certificação de Núcleos e Estabelecimentos Avícolas como livres de Salmonella Gallinarum e de Salmonella Pullorum e Livres ou Controlados para Salmonella Enteritidis e para Salmonella Typhimurium. Available at: http://extranet.agricultura.gov.br/sislegis-consulta/consultarLegislacao.do?operacao=visualizar&id=3864. Accessed 10.08.2015
EFSA. European Food Safety Authority (2007) Report of the Task Force on Zoonosis Data Collection on the Analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus, in the EU, 2005-2006, Part A: Salmonella prevalence estimates. EFSA J 98:1–85
EFSA. European Food Safety Authority (2010) Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008, Part A: Campylobacter and Salmonella prevalence estimates. EFSA J 8(3):1–99
Loureiro ECB, Marques NDB, Ramos FLP, Reis EMF, Prazeres D (2010) Salmonella serovars of human origin identified in Pará State, Brazil from 1991 to 2008. Rev Pan-Amaz Saude 1(1):93–100
IDSC (2009) Infectious Disease Surveillance Center. Salmonellosis in Japan as of June 2009. Infectious Agents Surveillance Report. 30:203–204
Noda T, Murakami K, Ishiguro Y, Asai T (2010) Chicken meat is an infection source of Salmonella serovar Infantis for humans in Japan. Foodborne Pathog Dis 7:727–735
Oliveira SD, Flores FS, Santos LR, Brandelli A (2005) Antimicrobial resistance in Salmonella Enteritidis strains isolated from broiler carcasses, food, human and poultry-related samples. Int J Food Microbiol 97:297–305
Trongjit S, Angkititrakul S, Tuttle RE, Poungseree J, Padungtod P, Chuanchuen R (2017) Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand–Cambodia border provinces. Microbiol Immunol 61:23–33
Brasil (2003) Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa N° 9, de 27 de Junho de 2003. Proibe 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, seção 1, p. 4
OIE (2007) World Organization for Animal Health. List of antimicrobials of veterinary importance. Report of the 75th general session (Resolution n° XXVIII). Paris, France, 25 p
WHO (2007) World Health Organization. Critically important antimicrobials for human medicine. Categorization for the development of risk management strategies to contain antimicrobial resistance due to non-human antimicrobial use. Report of the 2nd WHO Expert Meeting held in Copenhagen. Geneva, Switzerland, 34 p
Saraíva-Gomes J, Focaccia R, Lima VP (2006) Febres tifoide e paratifoide. In: Veronesi R (ed) Tratado de Infectologia, 3rd edn. Atheneu, São Paulo, pp 919–932
Singer R, Finch R, Wegener HC, Bywater R, Walters J, Lipsitch M (2003) Antibiotic resistance - the interplay between antibiotic use in animals and human beings. Lancet Infect Dis 3:47–51
WHO (2005) World Health Organization. Drug-resistant Salmonella. Fact Sheet No 139, revised, April. Avaiable at: http://www.who.int/mediacentre/factsheets/fs139/en/. Accessed 07.09.2016
Palermo Neto J (2011) Mecanismos de resistência aos antibióticos em saúde pública. In: Conferência Facta 2011 de Ciência e Tecnologia Avícolas, 2011, Santos. Anais... Santos: FACTA, p 39–50
Capita R, Alonso-Calleja C, Prieto M (2007) Prevalence of Salmonella enterica serovars and genovars from chicken carcasses in slaughterhouses in Spain. J Appl Microbiol 103:1366–1375
Mangen MJ, Batz M, Kassbohrer A et al (2010) Integrated approaches for the public health prioritization of foodborne and zoonotic pathogens. Risk Anal 30:782–797
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This study was financially supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Ministério da Agricultura Pecuária e Abastecimento (MAPA), and the Secretaria de Defesa Agropecuária (SDA), approved with the grant number 578372/2008-8, according to the Notice CNPq/MAPA/SDA no. 064/2008.
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Mendonça, E.P., de Melo, R.T., Nalevaiko, P.C. et al. Spread of the serotypes and antimicrobial resistance in strains of Salmonella spp. isolated from broiler. Braz J Microbiol 50, 515–522 (2019). https://doi.org/10.1007/s42770-019-00054-w
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DOI: https://doi.org/10.1007/s42770-019-00054-w