Accessibility / Report Error

Antimicrobial Resistance in Salmonella Serovars Isolated From an Egg-Producing Region in Brazil

VP Benevides MS Rubio LBR Alves FO Barbosa AIS Souza AM Almeida MRT Casas EAL Guastalli NM Soares A Berchieri JrAbout the authors

ABSTRACT

Fowl paratyphoid infections are caused by different Salmonella serovars that can affect a wide range of hosts. Due to its complex epidemiology, Salmonella serovar identification is crucial for the development and implementation of monitoring and control programs in poultry farms. Moreover, the characterization of the antimicrobial resistance profiles of Salmonella strains isolated from livestock is relevant to public health because they are a common causative agent of foodborne diseases. The objective of this study was to investigate the presence of Salmonella spp. and to identify the antimicrobial resistance profiles of strains isolated in the midwestern region of São Paulo state, which accounts for the highest production of table eggs in Brazil. For this purpose, 2008 fecal samples were collected on 151 commercial layer farms and submitted to microbiological analyses. Twenty-two serovars were isolated from 80 (52.9%) farms, among which S. Mbandaka and S. Braenderup were the most prevalent. All isolates expressed resistance to at least one of the 23 antimicrobials tested, and the highest resistance rates were determined against streptomycin (93.5%) and sulfonamide (84.6%). Moreover, multidrug resistance was observed in 41% of the isolates and the maximum drug resistance profile was against ten different antimicrobials. Therefore, the identification of Salmonella serovars in poultry production provides epidemiological knowledge to develop prevention and control measures in order to ensure poultry health and to prevent human infection by multiresistant strains.

Keywords:
Antimicrobial susceptibility; foodborne disease; salmonellosis; multi-drug resistance; public health

INTRODUCTION

Commercial table eggs are an important source of protein for Brazilian consumers. In 2018, Brazil produced 44.2 billion eggs, and had a per capita consumption of 212 eggs, representing a 10.4% increase relative to 2017 (APBA, 2019). This growth emphasizes the need to improve live production and egg processing management in order to achieve higher productivity, and to develop methods to allow layer farms and egg-processing companies to comply with the standards and guidelines of importing countries, in particular those relative to product quality and pathogen control (Donato et al., 2009Donato DCZ, Gandra ERS, Garcia PDSR, Reis CBM, Gameiro AH. A questão da qualidade no sistema agroindustrial do ovo. In. Anais do 47º Congresso da Sociedade Brasileira de Econonomia, Administração e Sociologia Rural; 2009. Porto Alegre, Rio Grande do Sul. Brasil; 2009. p.1-13.).

Bacteria of the genus Salmonella are widely distributed in nature and may infect both humans and animals, and more than 2659 Salmonella serovars have been identified (Issenhuth-Jeanjean et al., 2014Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, De Pinna E, et al. Supplement 2008-2010(n. 48) to the White-Kauffann-Le minor scheme. Research in Microbiology 2014;165:526-530.). Several of these serovars cause paratyphoid infection (Salles et al., 2008Salles RPR, Teixeira RSC, Siqueira AA, Silva EE, Castro SB, Cardoso WM. Monitoramento bacteriológico para Salmonella spp. em poedeira comercial na recria e produção de empresas avícolas da região metropolitana de fortaleza, CE, Brasil. Ciência Animal Brasileira 2008;9(2):427-432.; Kottwitz et al. 2008Kottwitz LBM, Back A, Leão JA, Alcocer I, Karan M, Oliveira TCRM. Contaminação por Salmonella spp. em uma cadeia de produção de ovos de uma integração de postura comercial. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2008;60:496-498.; Freitas Neto et al., 2014Freitas Neto OC, Galdino VMCA, Campello PL, Almeida AM, Fernandes SA, Berchieri Junior A. Salmonella serovars in laying hen flocks and commercial table eggs from a region of São Paulo State, Brazil. Revista Brasileira de Ciência Avícola 2014;16(2):57-62.; Perdoncini et al., 2014Perdoncini G, Ferreira JI, Lima LM, Rocha DT, Tejkowski TM, Pinto AT, et al. Salmonella spp. em ovos produzidos em sistema agroecológico. Revista Agrocientífica 2014;1(1):33-42.; Moraes et al., 2016Moraes DMC, Duarte SC, Bastos TSA, Rezende CLG, Leandro NSM, Café MB, et al. Detection of Salmonella spp. by conventional bacteriology and by quantitative polymerase-chain reaction in commercial egg structures. Brazilian Journal of Poultry Science 2016;18(1):117-124.). In addition, non-typhoidal Salmonella serovars may persist in the digestive tract of infected chickens without causing disease and are considered the main source of foodborne infections in humans, mainly due to the consumption of poultry products (Shah et al., 2017Shah DH, Paul NC, Sischo WC, Crespo R, Guard J. Population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes. Poultry Science 2017;96(3):687-702.).

Due to the wide variety of infection sources and its capacity to spread between hosts and vectors, it is very difficult, and often impossible, to eradicate Salmonella spp. in poultry farms, because poultry are susceptible hosts (Andino & Hanning, 2015Andino A, Hanning I. Salmonella enterica: survival, colonization, and virulence differences among serovars. Scientific World Journal 2015;2015:1-16.). Wild birds, rodents, and insects also play a central role in its dissemination among farms and persistence in poultry facilities (Ma et al., 2018Ma Z, Yang X, Fang Y, Tong Z, Lin H, Fan H. Detection of Salmonella infection in chickens by an indirect enzyme-linked immunosorbent assay based on presence of PagC antibodies in sera. Foodborne Pathogens and Disease 2018;15(2):109-113.). Therefore, the knowledge on Salmonella spp. prevalence in poultry flocks is required to design adequate biosecurity measures to reduce infection (Freitas Neto et al., 2014Freitas Neto OC, Galdino VMCA, Campello PL, Almeida AM, Fernandes SA, Berchieri Junior A. Salmonella serovars in laying hen flocks and commercial table eggs from a region of São Paulo State, Brazil. Revista Brasileira de Ciência Avícola 2014;16(2):57-62.).

Antimicrobials are used for the treatment of bacterial diseases in both human and veterinary medicine; however, their misuse (active principles, doses, or targets), have contributed to the emergence of resistant bacterial strains (Wright, 2010Wright GD. Q&A: antibiotic resistance:where does it come from and what can we do about it? BMC Biology 2010;8:123.). In Brazilian animal production, antibiotics are used not only for therapeutic purposes, but also for prophylaxis or as performance enhancers (Antunes et al., 2016Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis:the role of poultry meat. Clinical Microbiology and Infection 2016;22(2):110-121.). The most frequently used antimicrobial classes are β-lactams, tetracyclines, aminoglycosides, amphenicols, quinolones, fluoroquinolones, and sulfonamides (Moreno-Bondi et al., 2009Moreno-Bondi MC, Marazuela MD, Herranz S, Rodriguez E. An overview of sample preparation procedures for LC-MS multiclass antibiotic determination in environmental and food samples. Analytical and Bioanalytical Chemistry 2009;395(4):921-946.). However, Brazilian studies (Antunes et al., 2016; Celis-Estupiñan et al., 2017) have reported ineffective antimicrobial therapy against Salmonella spp. infection in poultry, which may contribute to the emergence of resistance. These results emphasize the need to determine the antimicrobial susceptibility profile of Salmonella spp. isolates for the design of programs to aid the rational use of antimicrobials in poultry production aiming at minimizing antimicrobial resistance in both poultry and humans (Allen et al., 2013Allen HK, Levine UY, Looft T, Bandrick M, Casey TA. Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends in Microbiology 2013;21(3):114-119.).

In this context, the objectives of this study were to identify Salmonella spp. isolate in layer farms in the largest egg producing region of Brazil, and to characterize their antimicrobial resistance profile.

MATERIAL AND METHODS

Ethics statement

All experimental procedures were approved by the Committee of Ethics on Animal Use of the School of Agriculture and Veterinarian Sciences, São Paulo State University (Unesp), Brazil, under protocol n. 07058/19.

Sample collection

Fecal samples were collected in 151 commercial layer farms located in 11 municipalities of the midwestern region of São Paulo state, between 2016 and 2017. Fecal samples (n=2008) of 300 grams each were collected in sterile flasks and refrigerated (4-8°C) until analyses (Brasil, 2017).

Identification of Salmonella serovars

The isolation and identification of Salmonella spp. were performed at the Avian Pathology Laboratory, Department of Veterinary Pathology, School of Agricultural and Veterinary Science (FCAV), São Paulo State University (Unesp), Jaboticabal, SP, Brazil.

Salmonella spp. microbiological assays followed the protocol (Figure 1) recommended by the Brazilian Ministry of Agriculture, Livestock and Food Supply (MAPA) (Brasil, 1995). Those isolates that had a suggestive biochemical profile for Salmonella were streaked on lysogen agar and then tested with somatic and flagellar antisera. All microbiological media inoculated with testing samples were incubated at 37 °C for 24 hours.

Figure 1
Flowchart of the microbiological assays used for the identification of Salmonella serotypes in fecal samples of commercial layers reared in the midwestern region of the state of São Paulo, SP, Brazil, between 2016 and 2017.

Presumed Salmonella colonies were submitted to the Polymerase Chain Reaction (PCR) targeting the invA gene to confirm the genus, as described by Fratamico & Strobaugh (1998Fratamico PM, Strobaugh TP. Simultaneous detection of Salmonella spp and Escherichia coli O157:H7 by multiplex PCR. Journal of Industrial Microbiology and Biotechnology 1998;21(3):92-98.). This virulence gene can only be found in Salmonella spp. and it is conserved among serovars (Oliveira et al., 2002Oliveira SD, Santos LR, Schuch DMT, Silva AB, Salle CTP, Canal CW. Detection and identification of salmonellas from poultry by PCR. Veterinary Microbiology 2002;87(1):25-35.). Positive samples in both microbiological and molecular assays were submitted to the Enterobacteria Section of Adolfo Lutz Institute, São Paulo, SP, Brazil, for serovar identification (Brasil, 1995).

Antimicrobial sensitivity test

The antimicrobial sensitivity of Salmonella strains was evaluated by Kirby-Bauer disk diffusion (Bauer et al., 1966Bauer AW, Kirby E, Sherris EM, Turk M. Antibiotic by standardized single disk method. American Journal of Clinical Pathology 1966;45:493-496.) and Minimal Inhibitory Concentration (MIC) (Thamlikitkul & Tiengrim, 2014Thamlikitkul V, Tiengrim S. In vitro activity of colistin plus sulbactam against extensive-drug-resistant Acinetobacter baumannii by checkerboard method. Journal of the Medical Association of Thailand 2014;97(Suppl.):S1-S3.) tests. Escherichia coli strain ATCC® 25922™ (CLSI, 2017) was used for quality control. Twenty-three antimicrobials belonging to 8 classes were evaluated (Table 1). The MIC test was performed only for polymyxin E, and strain resistance was assumed when antimicrobial concentration was higher than 2 µg/mL (CLSI, 2017). The results were compared with the standards of the Clinical and Laboratory Standards Institute reports (CLSI, 2013; CLSI, 2017). Intermediate profiles were assumed as resistant on disk diffusion test as an interpretation criterion (Firoozeh et al., 2011Firoozeh F, Shahcheraghi F, Salehi TZ, Karimi V, Aslani MM. Antimicrobial resistance profile and presence of class I integrongs among Salmonella enterica serovars isolated from human clinical specimens in Tehran, Iran. Iranian Journal Microbiology 2011;3(3):112-117.). Serovars resistant to three or more antimicrobials from different classes were considered multiresistant (Schwarz et al., 2010Schwarz S, Silley P, Simjee S, Woodford N, Duijkeren EV, Johnson AP, et al. Assessing the antimicrobial susceptibility of bacteria obtained from animals. Veterinary Microbiology 2010;141(1-2):1-4.).

Table 1
Antimicrobials used in sensitivity tests.

RESULTS AND DISCUSSION

The implementation of biosecurity measures directly influences the impact of foodborne salmonellosis from poultry products (Gama et al., 2003; Kottwitz et al., 2008Kottwitz LBM, Back A, Leão JA, Alcocer I, Karan M, Oliveira TCRM. Contaminação por Salmonella spp. em uma cadeia de produção de ovos de uma integração de postura comercial. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2008;60:496-498.). Human salmonellosis outbreaks in many countries have been associated with the consumption of table eggs (Nor Faiza et al., 2013Nor Faiza S, Saleha AA, Jalila A, Fauziah N. Occurrence of campylobacter and Salmonella in ducks and duck eggs in Selangor, Malaysia. Tropical Biomedicine 2013;30(1):155-158.; Long et al., 2017Long M, Yu H, Chen L, Wu G, Zhao S, Deng W, et al. Recovery of Salmonella isolated from eggs and the commercial layer farms. Gut Pathogens 2017;14:9-74.), which may be contaminated during their formation in the oviduct or their passage through the cloaca (contact with feces). Salmonella spp. survey on layers farms is essential for understanding the epidemiology of infection, which is influenced by farm, layer strain, production system, and technologies applied (Gama et al., 2003; Kottwitz et al., 2008). Although the Brazilian legislation on Salmonella control in poultry farms has become increasingly stringent, requiring structural changes of facilities, vaccination, and microbiological assays, Salmonella spp. serotyping is not mandatory, except for S. Gallinarum, S. Pullorum, S. Enteritidis, and S. Typhimurium (Brasil, 2003; Brasil, 2013; Brasil 2017).

In this study, fecal samples were collected in layer farms located in 11 municipalities in the midwestern region of the state of São Paulo, which is the largest table egg-producing region in Brazil, with 187 layer farms (ABPA, 2019). All strains suggestive of Salmonella in the microbiological assays were tested positive by PCR. Out of the 151 farms evaluated, 80 farms (52.9%) were positive for Salmonella spp. Previous reports detected Salmonella spp. in 3.98% cloacal swabs (Andrade et al., 1995Andrade MA, Mesquita AJ, Souza AM, Batista MAC. Frequência de Salmonella em granjas de postura comercial localizadas no município de Goiás e entorno. Pesquisa Agropecuária Tropical 1995;25(2):21-26.), 6.25% fecal samples (Salles et al., 2008Salles RPR, Teixeira RSC, Siqueira AA, Silva EE, Castro SB, Cardoso WM. Monitoramento bacteriológico para Salmonella spp. em poedeira comercial na recria e produção de empresas avícolas da região metropolitana de fortaleza, CE, Brasil. Ciência Animal Brasileira 2008;9(2):427-432.), and 25% mature flocks (Freitas Neto et al., 2014Freitas Neto OC, Galdino VMCA, Campello PL, Almeida AM, Fernandes SA, Berchieri Junior A. Salmonella serovars in laying hen flocks and commercial table eggs from a region of São Paulo State, Brazil. Revista Brasileira de Ciência Avícola 2014;16(2):57-62.) in Brazilian layer farms, suggesting that biosecurity failures may allow the dissemination of this pathogen among farms (Iwabuchi et al., 2010Iwabuchi E, Maruyama N, Hara A, Nishimura M, Muramatsu M, Ochiai T, et al. Nationwide survey of Salmonella prevalence in environmental dust from layer farms in Japan. Journal of Food Protection 2010;73(11):1993-2000.; Moraes et al., 2016Moraes DMC, Duarte SC, Bastos TSA, Rezende CLG, Leandro NSM, Café MB, et al. Detection of Salmonella spp. by conventional bacteriology and by quantitative polymerase-chain reaction in commercial egg structures. Brazilian Journal of Poultry Science 2016;18(1):117-124.).

Twenty-two serovars and two rough strains were identified in 80 isolates (Table 2). The rough samples were not subjected to antimicrobial susceptibility test. The highest prevalence was observed for serovars S. Mbandaka (37.2%) and S. Braenderup (12.8%), followed by S. Senftenberg and S. Tennessee (6.4%), S. Saintpaul (5.1%), S. Rissen (3.8%), S. Sandiego, S. Javiana, S. Meleagridis, S. Panama, S. I.O7:eh:- and S. Cerro (2.6%) and, S. Oranienburg, S. Schwarzengrund, S. Ouakam, S. Muenster, S. Livingstone, S. Agona, S. Yoruba, S. Enteritidis, S. Minnesota and S. Derby, isolated in only one sample (1.3%). Previous studies have reported the simultaneous presence of several serovars on a same layer farms, such as S. Agona, S. O: 4,5, S. Schwarzengrund, S. Cerro, S. Anatum, S. Enteritidis, S. Johannesburg, S. Corvallis (Moraes et al., 2016Moraes DMC, Duarte SC, Bastos TSA, Rezende CLG, Leandro NSM, Café MB, et al. Detection of Salmonella spp. by conventional bacteriology and by quantitative polymerase-chain reaction in commercial egg structures. Brazilian Journal of Poultry Science 2016;18(1):117-124.; Du et al, 2017Du X, Jiang X, Ye Y, Guo B, Wang W, Ding J, et al. Next generation sequencing for the investigation of an outbreak of Salmonella Schwarzengrund in Nanjing, China. International Journal of Biological Macromolecules 2017;107(Pt A):393-396.), S. subesp. enterica 4,12: r: -, S. Mbandaka, S. subesp. enterica 6,7: z10: -, S. Havana, S. Braenderup (Freitas Neto et al., 2014Freitas Neto OC, Galdino VMCA, Campello PL, Almeida AM, Fernandes SA, Berchieri Junior A. Salmonella serovars in laying hen flocks and commercial table eggs from a region of São Paulo State, Brazil. Revista Brasileira de Ciência Avícola 2014;16(2):57-62.), S. Typhimurium, and S. subesp. enterica 4,12: d: - (Snow et al., 2007Snow LC, Davies RH, Christiansen KC, Carrique-Mas JJ, Wales AD, O’Connor JL, et al. Survey of Salmonella prevalence on commercial layer farms in the United Kingdom. Veterinary Record 2007;161(14):471-476.; Chemaly et al., 2009Chemaly M, Huneau-Salaun A, Labbe A, Houdayer C, Petetin I, Fravalo P. Isolation of Salmonella enterica in layer flocks and assessment of eggshell contamination in France. Journal of Food Protection 2009;72(10):2071-2077.).

Table 2
Salmonella serovars identified in fecal samples of commercial layers reared in the midwestern region of São Paulo state, SP, Brazil, between 2016 and 2017.

The most prevalent serovar isolated in the present study (S. Mbandaka) was also previously reported in layer farms in Argentina and Brazil, with prevalence rates of 11% and 7.5%, respectively (Kottwitz et al., 2008Kottwitz LBM, Back A, Leão JA, Alcocer I, Karan M, Oliveira TCRM. Contaminação por Salmonella spp. em uma cadeia de produção de ovos de uma integração de postura comercial. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2008;60:496-498.; Soria et al., 2017Soria MC, Soria MA, Bueno DJ, Godano EI, Gómez SC, ViaButron IA, et al. Salmonella spp. contamination in commercial layer hen farms using different types of samples and detection methods. Poultry Science 2017;96(8):2820-2830.). Iwabuchi et al. (2010Iwabuchi E, Maruyama N, Hara A, Nishimura M, Muramatsu M, Ochiai T, et al. Nationwide survey of Salmonella prevalence in environmental dust from layer farms in Japan. Journal of Food Protection 2010;73(11):1993-2000.) detected S. Mbandaka in the dust of the poultry house air circulation system, which suggests that usual poultry house disinfection procedures are not able to eliminate this serovar, contributing to its persistence on infected farms.

S. Braenderup, the second most prevalent serovar isolated in this study (12.8%), is also responsible for human infections (EFSA, 2017; CDC, 2019), and it is associated with the consumption of eggs (Nor Faiza et al., 2013Nor Faiza S, Saleha AA, Jalila A, Fauziah N. Occurrence of campylobacter and Salmonella in ducks and duck eggs in Selangor, Malaysia. Tropical Biomedicine 2013;30(1):155-158.; Long et al., 2017Long M, Yu H, Chen L, Wu G, Zhao S, Deng W, et al. Recovery of Salmonella isolated from eggs and the commercial layer farms. Gut Pathogens 2017;14:9-74.) and of vegetables, such as tomatoes (Micallef et al., 2012Micallef SA, Rosenberg Goldstein RE, George A, Kleinfelter L, Boyer MS, McLaughlin CR, et al. Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on mid-Atlantic tomato farms. Environmental Research 2012;114:31-39.) and lettuce (Gajraj et al., 2012Gajraj R, Pooransingh S, Hawker JI, Olowokure B. Multiple outbreaks of Salmonella braenderup associated with consumption of iceberg lettuce. International Journal of Environmental Health Research 2012;22(2):150-155.). The third most prevalent serovar isolated, S. Senftenberg (6.4%), has been the leading cause of foodborne disease during the last decade (Pezzoli et al., 2008Pezzoli L, Elson R, Little CL, Yip H, Fisher I, Yishai R, et al. Packed with Salmonella - investigation of an international outbreak of Salmonella Senftenberg infection linked to contamination of prepacked basil in 2007. Foodborne Pathogens and Disease 2008;5(5):661-668.). In Brazil, most cases of human salmonellosis are not reported, and therefore, we were not able to find epidemiological data on the serovars causing foodborne infections (SVS, 2019).

The low prevalence of some serovars determined in the present study may be attributed to their preference for other animal or plant infection targets. For instance, S. Enteritidis and S. Schwarzengrund serovars were the most prevalent in eggs samples (Moraes et al., 2016Moraes DMC, Duarte SC, Bastos TSA, Rezende CLG, Leandro NSM, Café MB, et al. Detection of Salmonella spp. by conventional bacteriology and by quantitative polymerase-chain reaction in commercial egg structures. Brazilian Journal of Poultry Science 2016;18(1):117-124.), and S. Agona was associated with the consumption of contaminated fishmeal by layers (Berchieri Junior et al., 1985Berchieri Junior A, Paulillo AC, Fernandes SA, Irino K, Pessoa GVA. Sensibilidade a antimicrobianos por Salmonella isolados de farinhas de origem animal utilizados no preparo de rações. Revista de Microbiologia 1985;16(1):56-60.; Clark et al., 1973Clark GM, Kaufmann AF, Gangarosa EJ, Thompson MA. Epidemiology of an international outbreak of Salmonella agona. Lancet 1973;1(7827):490-493.).

In Brazil, 58.8% of human foodborne disease agents are not identified; however, when diagnosed, Salmonella spp. is the most prevalent (SVS, 2015). The most prevalent serovars reported in foodborne outbreaks in the USA, European Union, and Brazil are S. Enteritidis and S. Typhimurium (EFSA, 2017; EU, 2018; CDC, 2019), and are typically associated with the consumption of poultry products (Jackson et al., 2013Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ. Outbreak associated Salmonella enterica serotypes and food commodities, United States, 1998-2008. Emerging Infectious Diseases 2013;19(8):1239-1244.; SVS, 2019). In the present study, S. Typhimurium was not found, and S. Enteritidis was isolated only in one farm. This result was expected, as the Brazilian government established a national plan for the control of Salmonella in breeder flocks in 1994 (Brasil, 2003). This plan requires the mandatory destruction of breeder flocks infected by S. Gallinarum biovars Gallinarum and Pullorum, and eggs from flocks infected with S. Enteritidis and S. Typhimurium serovars cannot be incubated.

In order to minimize the occurrence of bacterial diseases, antimicrobials have been routinely used as therapeutics both in human and veterinary medicine. However, in animal production, antimicrobials have also been applied for prophylaxis and performance enhancement for many years (Rodríguez et al., 2012Rodríguez I, Rodicio MR, Guerra B, Hopkins KL. Potential international spread of multidrug-resistant invasive Salmonella enterica serovar Enteritidis. Emerging Infectious Diseases 2012;18(7):1173-1176.; Chen et al., 2013Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatrics and Neonatology 2013;54(3):147-152.; Burke et al., 2014Burke L, Hopkins KL, Meunier D, Pinna E, Fitzgerald-Hughes D, Humphreys Woodford N. Resistance to third-generation cephalosporins in human non-typhoidal Salmonella enterica isolates from England and Wales, 2010-12. Journal of Antimicrobial Chemotherapy 2014;69(4):977-981.; Sapkota et al., 2014Sapkota AR, Kinney EL, George A, Hulet RM, Cruz-Cano R, Schwab KJ, et al. Lower prevalence of antibiotic-resistant Salmonella on large-scale U.S. conventional poultry farms that transitioned to organic practices. Science of the Total Environment 2014;476-477:387-392.; Cosby et al., 2015Cosby DE, Cox NA, Harrison MA, Wilson JL, Jeff Buhr R, Fedorka-Cray PJ. Salmonella and antimicrobial resistance in broilers:a review. Journal of Applied Poultry Research 2015;24(3):408-426.; Pande et al., 2015Pande VV, Gole VC, McWhorter AR, Abraham S, Chousalkar KK. Antimicrobial resistance of non-typhoidal Salmonella isolates from egg layer flocks and egg shells. International Journal of Food Microbiology 2015;203:23-26.; Antunes et al., 2016Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis:the role of poultry meat. Clinical Microbiology and Infection 2016;22(2):110-121.; Grant et al., 2016Grant A, Hashem F, Parveen S. Salmonella and Campylobacter:antimicrobial resistance and bacteriophage control in poultry. Food Microbiology 2016;53:104-109.; Du et al., 2017Du X, Jiang X, Ye Y, Guo B, Wang W, Ding J, et al. Next generation sequencing for the investigation of an outbreak of Salmonella Schwarzengrund in Nanjing, China. International Journal of Biological Macromolecules 2017;107(Pt A):393-396.), particularly β-lactams, aminoglycosides, amphenicols, quinolones, fluoroquinolones, tetracyclines and sulfonamides (Moreno-Bondi et al., 2009Moreno-Bondi MC, Marazuela MD, Herranz S, Rodriguez E. An overview of sample preparation procedures for LC-MS multiclass antibiotic determination in environmental and food samples. Analytical and Bioanalytical Chemistry 2009;395(4):921-946.).

The antimicrobial sensitivity test result of the present study showed that 100% of the isolates were resistant to at least one of the antimicrobials tested, and resistance to streptomycin was the most frequent, found in 93.5% of the isolates tested (Table 3). The resistance of Salmonella spp. to critically important antimicrobials, such as fluoroquinolones and extended-spectrum cephalosporins, is a significant public health concern, threatening the efficiency of antimicrobial agents (Campos et al., 2018Campos J, Mourão J, Silveira L, Saraiva M, Correia CB, Maçãs AP, et al. Imported poultry meat as a source of extended-spectrum cephalosporin-resistant CMY-2-producing Salmonella Heidelberg and Salmonella Minnesota in the European Union, 2014-2015. International Journal of Antimicrobial Agents 2018;51(1):151-154.; Hassena et al., 2019Hassena AB, Siala M, Guermazi S, Zormati S, Gdoura R, Sellami H. Occurrence and phenotypic and molecular characterization of antimicrobial resistance of Salmonella isolates from food in Tunisia. Journal of Food Protection 2019, 82(7):1166-1175.). High rates of Salmonella spp. non-susceptible to fluoroquinolones and cephalosporins were observed in humans (Andoh et al., 2017Andoh LA, Ahmed S, Olsen JE, Obiri-Danso K, Newman MJ, Opintan JA, et al. Prevalence and characterization of Salmonella among humans in Ghana. Tropical Medicine and Health 2017;45:3.). In the present study, Salmonella spp. isolates showed resistance to streptomycin (93.5%), sulfonamide (84.6%) and ciprofloxacin (41%), followed by nalidixic acid and enrofloxacin (20.5%), tetracycline and oxytetracycline (17.9%), sulfamethoxazole/trimethoprim (14.1%) and amoxicillin and amoxicillin/clavulanic acid (9%). Isolates were sensitive to norfloxacin, amikacin, gentamicin, aztreonam, cefotaxime, ceftiofur, cefepime, imipenem, chloramphenicol, and phosphomycin, which should be used with caution in order to prevent the emergence of resistance, where their use is allowed (Wright, 2010Wright GD. Q&A: antibiotic resistance:where does it come from and what can we do about it? BMC Biology 2010;8:123.).

Table 3
Antimicrobial susceptibility of the Salmonella strains isolated in commercial layer farms located in different municipalities of the Midwestern region of São Paulo state, SP, Brazil, between 2016 and 2017, expressed in number of resistant strains.

Considering that norfloxacin and ciprofloxacin belong to the same drug class, equal resistance profiles against both antimicrobials were expected. However, in the present study, isolates were shown to be sensitive to norfloxacin and presented intermediate resistance to ciprofloxacin. This may be explained by the fact that isolates with intermediate-resistance profile were classified as resistant due to the interpretation criterion adopted. Nevertheless, this discrepancy between sensitive and intermediate profiles remains unclear and further studies are needed to elucidate it. It should be emphasized that the emergence and dissemination of strains resistant to fluoroquinolones (ciprofloxacin) may lead to treatment failure of serious infections in humans (Chen et al., 2013Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatrics and Neonatology 2013;54(3):147-152.). The resistance profile of the isolates in the present study may be attributed to the presence of PMQR (plasmid-mediated quinolone resistance) genes, such as qcnr, aac (6′)-Ib-cr, qepA, and oqxAB. According to Campbell et al. (2018Campbell D, Tagg K, Bicknese A, McCullough A, Chen J, Karp BE, et al. Identification and Characterization of Salmonella enterica serotype newport isolates with decreased susceptibility to ciprofloxacin in the United States. Antimicrobial Agents and Chemotherapy 2018;62(7):e00653-18.), isolates harboring PMQR genes may show reduced susceptibility against ciprofloxacin and may not be resistant to nalidixic acid. In the study of Hopkins et al. (2007Hopkins KL, Wootton L, Day MR, Threlfall E. Plasmid-mediated quinolone resistance determinant qnrS1 found in Salmonella enterica strains isolated in the UK. Journal of Antimicrobial Chemotherapy 2007;59(6):1071-1075.), all Salmonella serovars expressing both reduced susceptibility against ciprofloxacin and higher susceptibility to nalidixic acid harbored qnr genes. Resistance may also be affected by the number of qnr genes copies and by their transcription levels (Rodríguez-Martínez et al., 2006; Xu et al., 2007Xu X, Wu S, Ye X, Liu Y, Shi W, Zhang Y,et al. Prevalence and expression of the plasmid-mediated quinolone resistance determinant qnrA1. Antimicrobial Agents and Chemotherapy 2007;51:4105-4110.).

Polymyxin-E MIC results ranged between 0.5 and 4 µg/mL, and only two isolates were considered resistant, using 2 µg/mL as a cutoff point, according to CLSI (2017). Although most strains were characterized as sensitive to this antimicrobial, it should be emphasized that it must be cautiously used. Although the use of polymyxin A was discontinued in the 1970s due to its toxicity, it was reintroduced in the 1990s due to the emergence of multiresistant bacteria (Storm et al., 1977Storm DR, Rosenthal KS, Swanson PE. Polymyxin and related peptide antibiotics. Annual Review of Biochemistry 1977;46:723-763.; Poirel et al., 2017Poirel L, Jayol A, Nordamann P. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clinical Microbiology Reviews 2017;30(2):557-596.). In 2016, the use of colistin sulfate as a performance enhancer was banned in Brazil (Brasil, 2016) in order to prevent cross-resistance of pathogens of public health concern (Hu et al., 2017Hu YY, Wang YL, Sun QL, Huang ZX, Wang HY, Zhang R, et al. Colistin resistance gene mcr-1 in gut flora of children. International Journal of Antimicrobial Agents 2017;50(4):593-597.). Therefore, the identification of polymyxin E-resistant zoonotic Salmonella strains in layer farms in the present study is a matter of concern, as this drug is one of the last treatment choices for human salmonellosis, and resistance against broad-spectrum drugs may result in high mortality rates (Costa et al., 2013Costa RG, Festivo ML, Araujo MS, Reis EM, Lázaro NS, Rodrigues DP. Antimicrobial susceptibility and serovars of Salmonella circulating in commercial poultry carcasses and poultry products in Brazil. Journal of Food Protection 2013;76(12):2011-2017.; Shang et al., 2018Shang K, Wei B, Kang M. Distribution and dissemination of antimicrobial-resistant Salmonella in broiler farms with or without enrofloxacin use. BMC Veterinary Research 2018;14(257).).

As described in Table 4, 18 resistance profiles were observed: two isolates were resistant to only one antimicrobial, while 16 showed multiple resistance (ranging from two to 10 antimicrobials). Out of the 78 isolates evaluated, 10 showed single resistance profile to sulfonamide (3/78) or to streptomycin (7/78). Multiresistant profile (resistant to three or more antimicrobials of different classes) were observed in 32 isolates, which were grouped in 11 different profiles. S. Schwarzengrund serovar presented the maximum resistance profile, being resistant to 10 of the antimicrobials tested.

Table 4
Antimicrobial resistance profiles of Salmonella strains isolated in commercial layer farms located in different municipalities of the Midwestern region of São Paulo state, SP, Brazil, between 2016 and 2017.

The incidence of antimicrobial resistance has increased over the years due to their frequent use in human and veterinary medicine, as well as to the adaptation and genetic reorganization of bacteria, including Salmonella spp. (Chen et al., 2013Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatrics and Neonatology 2013;54(3):147-152.; Burke et al., 2014Burke L, Hopkins KL, Meunier D, Pinna E, Fitzgerald-Hughes D, Humphreys Woodford N. Resistance to third-generation cephalosporins in human non-typhoidal Salmonella enterica isolates from England and Wales, 2010-12. Journal of Antimicrobial Chemotherapy 2014;69(4):977-981.; Sapkota et al., 2014Sapkota AR, Kinney EL, George A, Hulet RM, Cruz-Cano R, Schwab KJ, et al. Lower prevalence of antibiotic-resistant Salmonella on large-scale U.S. conventional poultry farms that transitioned to organic practices. Science of the Total Environment 2014;476-477:387-392.; Cosby et al., 2015Cosby DE, Cox NA, Harrison MA, Wilson JL, Jeff Buhr R, Fedorka-Cray PJ. Salmonella and antimicrobial resistance in broilers:a review. Journal of Applied Poultry Research 2015;24(3):408-426.; Pande et al., 2015Pande VV, Gole VC, McWhorter AR, Abraham S, Chousalkar KK. Antimicrobial resistance of non-typhoidal Salmonella isolates from egg layer flocks and egg shells. International Journal of Food Microbiology 2015;203:23-26.; Antunes et al., 2016Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis:the role of poultry meat. Clinical Microbiology and Infection 2016;22(2):110-121.; Grant et al., 2016Grant A, Hashem F, Parveen S. Salmonella and Campylobacter:antimicrobial resistance and bacteriophage control in poultry. Food Microbiology 2016;53:104-109.). The association of these factors favors the emergence of multiresistant bacteria, which is often related to human mortality rates in hospitals or intensive care units (Rodríguez et al., 2012Rodríguez I, Rodicio MR, Guerra B, Hopkins KL. Potential international spread of multidrug-resistant invasive Salmonella enterica serovar Enteritidis. Emerging Infectious Diseases 2012;18(7):1173-1176.; Du et al., 2017Du X, Jiang X, Ye Y, Guo B, Wang W, Ding J, et al. Next generation sequencing for the investigation of an outbreak of Salmonella Schwarzengrund in Nanjing, China. International Journal of Biological Macromolecules 2017;107(Pt A):393-396.). For instance, the use of ampicillin in livestock may lead to the emergence of bacterial strains resistant to this drug, and which may also be co-resistant to third-generation cephalosporins used to treat animal infections (Jensen et al., 2018Jensen LB, Birk T, Borck HB, Stehr L, Aabo S, Korsgaard H. Cross and co resistance among Danish porcine E. coli isolates. Research in Veterinary Science 2018;119:247-249.).

The antimicrobial incidence rate found in the present study is higher than those previously reported for Salmonella in broilers, of maximum phenotype resistance profile against eight antimicrobials in Brazil (Mion et al., 2014Mion L, Colla FL, Cisco IC, Webber B, Diedrich LN, Pilotto F, et al. Perfil de resistência a antimicrobianos por Salmonella Heidelberg isoladas de abatedouro avícola em 2005 e 2009. Acta Scientiae Veterinariae 2014;42:1197.) and seven in Mexico (Arslan & Eyi, 2010Arslan S, Eyi A. Occurrence and antimicrobial resistance profiles of salmonella species in retail meat products. Journal of Food Protection 2010;73(9):1613-1617.). However, it is lower compared with the findings of Yan et al. (2010Yan H, Li L, Alam MJ, Shinoda S, Miyoshi S, Shi L. Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. International Journal of Food Microbiology 2010;143(3):230-234.), who reported Salmonella spp. isolates resistant to up to 20 antimicrobials in China. Although studies evaluated different antimicrobials, they demonstrate the emergence of multiresistant bacterial strains.

Antunes et al. (2003Antunes P, Réu C, Sousa JC, Peixe L, Pestana N. Incidence of Salmonella from poultry products and their susceptibility to antimicrobial agents. International Journal of Food Microbiology 2003;82(2):97-103.) reported the 39% Salmonella serovars isolated from poultry products were resistant to streptomycin, while 93.5% streptomycin-resistant strains were characterized in the present study. This result may be attributed to the use of subtherapeutic doses of this antimicrobial in poultry production, which annually reduces its therapeutic effectiveness (Manie et al., 1998Manie T, Khan S, Brözel VS, Veith WJ, Gouws PA. Antimicrobial resistance of bacteria isolatedfrom slaughtered and retail chickens in South Africa. Letters in Applied Microbiology 1998;26(4):253-258.; Liljebjelke et al., 2017Liljebjelke KA, Hofacre CL, White DG, Ayers S, Lee MD, Maurer JJ. Diversity of antimicrobial resistance phenotypes in Salmonella isolated from commercial poultry farms. Frontiers in Veterinary Science 2017;4:96.). Sulfonamides were the second antimicrobial class showing the second highest resistant prevalence (84.6% of the isolates); however, when associated with trimethoprim, significantly lower resistance prevalence was determined, of only 14.1% of the isolates. Castagna et al. (2001) and Galdino et al. (2013Galdino VMC, Melo RT, Oliveira RP, Mendonça EP, Nalevaiko PC, Rossi DA. Virulence of Salmonella spp. of poultry products origin and antimicrobial resistance. Bioscience Journal 2013;29:932-939.) reported higher efficacy of that association when evaluating Salmonella spp. sensitivity in animal isolates. Due to its effectiveness, sulfonamide-trimethoprim association is widely used for the treatment of human infections; however, a 30% annual increase in Salmonella strains resistant to this association has been observed (Barlow et al., 2014Barlow RS, Debess EE, Winthrop KL, Lapidus JA, Vega R, Cieslak PR. Travel-associated antimicrobial drug-resistant nontyphoidal Salmonella, 2004-2009. Emerging Infectious Disease 2014;20(4):603-611.; Tagg et al., 2019Tagg KA, Francois Watkins L, Moore MD, Bennett C, Joung YJ, Chen JC, et al. Novel trimethoprim resistance gene dfrA34 identified in Salmonella Heidelberg in the USA. Journal of Antimicrobial Chemotherapy 2019;74(1):38-41.).

As the emergence of Salmonella isolates resistant to ampicillin and sulfonamide/trimethoprim has increased over the years, broad-spectrum antimicrobials, such as ciprofloxacin and cephalosporins, have been applied for the treatment of human salmonellosis (Chen et al., 2013Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatrics and Neonatology 2013;54(3):147-152.; Antunes et al., 2016Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis:the role of poultry meat. Clinical Microbiology and Infection 2016;22(2):110-121.). Moreover, since the use of fluoroquinolones was allowed in animal production, Salmonella spp. strains resistant to ciprofloxacin have been isolated in both animal products and humans (Cosby et al., 2015Cosby DE, Cox NA, Harrison MA, Wilson JL, Jeff Buhr R, Fedorka-Cray PJ. Salmonella and antimicrobial resistance in broilers:a review. Journal of Applied Poultry Research 2015;24(3):408-426.). The 41% rate of ciprofloxacin-resistant strains determined in the present study is in agreement with previous studies, which also found high incidence rates of resistant Salmonella spp., of 25.0% in Ghana (Andoh et al., 2017Andoh LA, Ahmed S, Olsen JE, Obiri-Danso K, Newman MJ, Opintan JA, et al. Prevalence and characterization of Salmonella among humans in Ghana. Tropical Medicine and Health 2017;45:3.) and of 35.1% in Shanghai (Wei et al., 2019Wei Z, Xu X, Yan M, Chang H, Li Y, Kan B, et al. Salmonella typhimurium and Salmonella enteritidis infections in sporadic diarrhea in children: source tracing and resistance to third-generation cephalosporins and ciprofloxacin. Foodborne Pathogens and Diseases 2019;16(4):244-255.). These results are a matter of concern, as the emergence of such strains may lead to failure of the treatment of severe bacterial infections in human medicine (Costa et al., 2013Costa RG, Festivo ML, Araujo MS, Reis EM, Lázaro NS, Rodrigues DP. Antimicrobial susceptibility and serovars of Salmonella circulating in commercial poultry carcasses and poultry products in Brazil. Journal of Food Protection 2013;76(12):2011-2017.; Shang et al., 2018).

The occurrence of multi-drug resistant strains in humans may also be related to antimicrobial residues in food sources. The 2017 annual report published by the Brazilian Ministry of Agriculture on non-conformities in animal products showed that drug residues were found in 1.21% (12/3,894) of poultry products samples, with 1.03% (6/584) in eggs and 0.18% (6/3,310) in broiler products, respectively. The main drugs detected were enrofloxacin (1.81%), sulfaquinoxaline (0.17%), sulfamethazine (0.36%), doxycycline (0.08%), nicarbazin (0.85%), and arsenic (0.51%) (Brasil, 2018). This report emphasizes the public health concerns with the consumption of antibiotics in foods of animal origin, as only one of the drugs found was not derived from animal products, and resistance to two of the antibiotics reported were found in the present study, which may contribute to increase the populations of resistant and multiresistant bacteria.

The intense selective pressure imposed by the indiscriminate administration of antimicrobials has led to the emergence of bacterial strains resistant to these compounds (Wright, 2010Wright GD. Q&A: antibiotic resistance:where does it come from and what can we do about it? BMC Biology 2010;8:123.). The emergence and dissemination of resistant Salmonella spp. isolated from food of animal origin has important consequences for public health, as it limits treatment efficiency and increases mortality rates in humans (Costa et al., 2013Costa RG, Festivo ML, Araujo MS, Reis EM, Lázaro NS, Rodrigues DP. Antimicrobial susceptibility and serovars of Salmonella circulating in commercial poultry carcasses and poultry products in Brazil. Journal of Food Protection 2013;76(12):2011-2017.; Shang et al., 2018Shang K, Wei B, Kang M. Distribution and dissemination of antimicrobial-resistant Salmonella in broiler farms with or without enrofloxacin use. BMC Veterinary Research 2018;14(257).).

The present study showed that 52.9% (80/151) of the evaluated farms were positive for Salmonella spp., with 22 serovars isolated, and that 100% of the isolates were resistant to at least one of the tested antimicrobials, with 41% presenting multiple-drug resistance. The results emphasize the need to promote policies for the rational use of antimicrobials and for the effective implementation of biosecurity measures. In addition, the serotyping of Salmonella spp. isolated from poultry farms is required to provide epidemiological knowledge for the development of prevention and control measures of this pathogen aiming at ensuring animal health and product quality certification.

ACKNOWLEDGMENTS

This study was supported by São Paulo Research Foundation (FAPESP) and Coordination for the Improvement of Higher Education Personnel (CAPES) [grant numbers 2017/25743-7 (V.P. Benevides) and 2016/10369-0 (A. Berchieri Junior)] and the National Council of Technological and Scientific Development (CNPq). We also thank Adolfo Lutz Institute and Biological Institute for their sampling and laboratory analysis assistance.

REFERENCES

  • ABPA - Associação Brasileira de Proteína Animal. Relatório anual 2019. São Paulo; 2019. Disponível em: http://abpa-br.com.br/storage/files/relatorio-anual-2018.pdf
    » http://abpa-br.com.br/storage/files/relatorio-anual-2018.pdf
  • Allen HK, Levine UY, Looft T, Bandrick M, Casey TA. Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends in Microbiology 2013;21(3):114-119.
  • Andino A, Hanning I. Salmonella enterica: survival, colonization, and virulence differences among serovars. Scientific World Journal 2015;2015:1-16.
  • Andoh LA, Ahmed S, Olsen JE, Obiri-Danso K, Newman MJ, Opintan JA, et al. Prevalence and characterization of Salmonella among humans in Ghana. Tropical Medicine and Health 2017;45:3.
  • Andrade MA, Mesquita AJ, Souza AM, Batista MAC. Frequência de Salmonella em granjas de postura comercial localizadas no município de Goiás e entorno. Pesquisa Agropecuária Tropical 1995;25(2):21-26.
  • Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis:the role of poultry meat. Clinical Microbiology and Infection 2016;22(2):110-121.
  • Antunes P, Réu C, Sousa JC, Peixe L, Pestana N. Incidence of Salmonella from poultry products and their susceptibility to antimicrobial agents. International Journal of Food Microbiology 2003;82(2):97-103.
  • Arslan S, Eyi A. Occurrence and antimicrobial resistance profiles of salmonella species in retail meat products. Journal of Food Protection 2010;73(9):1613-1617.
  • Bauer AW, Kirby E, Sherris EM, Turk M. Antibiotic by standardized single disk method. American Journal of Clinical Pathology 1966;45:493-496.
  • Barlow RS, Debess EE, Winthrop KL, Lapidus JA, Vega R, Cieslak PR. Travel-associated antimicrobial drug-resistant nontyphoidal Salmonella, 2004-2009. Emerging Infectious Disease 2014;20(4):603-611.
  • Berchieri Junior A, Paulillo AC, Fernandes SA, Irino K, Pessoa GVA. Sensibilidade a antimicrobianos por Salmonella isolados de farinhas de origem animal utilizados no preparo de rações. Revista de Microbiologia 1985;16(1):56-60.
  • Brasil. Portaria n° 126, de 3 de novembro de 1995. Diário Oficial da República Federativa do Brasil, Brasília, DF, 6 nov. 1995, seção 1:17694-17698. Available from: http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=consultarLegislacaoFederal
    » http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=consultarLegislacaoFederal
  • Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Instrução normativa nº 78, de 3 novembro de 2003. Available from: http://extranet.agricultura.gov.br/sislegisconsulta/consultarLegislacao.do?operacao=visualizar&id=3864
    » http://extranet.agricultura.gov.br/sislegisconsulta/consultarLegislacao.do?operacao=visualizar&id=3864
  • Brasil. Instrução Normativa nº 10, de 11 de abril de 2013. Diário Oficial da República Federativa do Brasil, Brasília, DF, 12 abr. 2013, seção 1, p.2-4. Available from: http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?jornal=1&pagina=2&data=12/04/2013
    » http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?jornal=1&pagina=2&data=12/04/2013
  • Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Instrução normativa nº 45, de 22 de novembro de 2016. Seção 1, p.6. Available from: http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=consultarLegislacaoFederal
    » http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=consultarLegislacaoFederal
  • Brasil. Instrução Normativa nº 8, de 17 de fevereiro de 2017. Diário Oficial da República Federativa do Brasil, Brasília, DF, 3 de março 2017, seção 1, p.32-33. Available from: http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=03/03/2017&jornal=1&pagina=32&totalArq
    » http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=03/03/2017&jornal=1&pagina=32&totalArq
  • Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Anuário dos programas de controle de alimentos de origem animal do DIPOA. Brasília (DF): Secretaria de Defesa Agropecuária, Departamento de Inspeção de Produtos de Origem Animal, Coordenação Geral de Programas Especiais 4; 2018. Available from: http://www.agricultura.gov.br/assuntos/inspecao/produtos-animal/arquivos-publicacoes-dipoa/anuario-dipoa-v4
    » http://www.agricultura.gov.br/assuntos/inspecao/produtos-animal/arquivos-publicacoes-dipoa/anuario-dipoa-v4
  • Burke L, Hopkins KL, Meunier D, Pinna E, Fitzgerald-Hughes D, Humphreys Woodford N. Resistance to third-generation cephalosporins in human non-typhoidal Salmonella enterica isolates from England and Wales, 2010-12. Journal of Antimicrobial Chemotherapy 2014;69(4):977-981.
  • Campbell D, Tagg K, Bicknese A, McCullough A, Chen J, Karp BE, et al. Identification and Characterization of Salmonella enterica serotype newport isolates with decreased susceptibility to ciprofloxacin in the United States. Antimicrobial Agents and Chemotherapy 2018;62(7):e00653-18.
  • Campos J, Mourão J, Silveira L, Saraiva M, Correia CB, Maçãs AP, et al. Imported poultry meat as a source of extended-spectrum cephalosporin-resistant CMY-2-producing Salmonella Heidelberg and Salmonella Minnesota in the European Union, 2014-2015. International Journal of Antimicrobial Agents 2018;51(1):151-154.
  • Castagna SMF, Bessa MC, Carvalho DA, Cardoso M, Costa, M. Resistência a antimicrobianos de amostras de Salmonella spp. Isoladas de suínos abatidos no Estado do Rio Grande do Sul. Arquivos da Faculdade de Veterinária UFRGS 2001;29(1):44-49.
  • CDC - Centers for Disease Control and Prevention. Reports of Salmonella outbreak investigations from 2019. Georgia: Departament of Health and Human Services; 2019. Available from: https://www.cdc.gov/Salmonella/outbreaks-2019.html
    » https://www.cdc.gov/Salmonella/outbreaks-2019.html
  • Celis-Estupiñan ALDP, Batista DFA, Cardozo MV, Souza AIS, Rodrigues Alves LB, Almeida AM, et al. Further investigations on the epidemiology of fowl typhoid in Brazil. Avian Diseases 2016;46(4):416-425.
  • Chemaly M, Huneau-Salaun A, Labbe A, Houdayer C, Petetin I, Fravalo P. Isolation of Salmonella enterica in layer flocks and assessment of eggshell contamination in France. Journal of Food Protection 2009;72(10):2071-2077.
  • Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatrics and Neonatology 2013;54(3):147-152.
  • Clark GM, Kaufmann AF, Gangarosa EJ, Thompson MA. Epidemiology of an international outbreak of Salmonella agona. Lancet 1973;1(7827):490-493.
  • CLSI - Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard [Supplement VET01-A4]. 4th ed. Wayne: CLSI; 2013.
  • CLSI - Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing [supplement M100]. Wayne: CLSI; 2017.
  • Cosby DE, Cox NA, Harrison MA, Wilson JL, Jeff Buhr R, Fedorka-Cray PJ. Salmonella and antimicrobial resistance in broilers:a review. Journal of Applied Poultry Research 2015;24(3):408-426.
  • Costa RG, Festivo ML, Araujo MS, Reis EM, Lázaro NS, Rodrigues DP. Antimicrobial susceptibility and serovars of Salmonella circulating in commercial poultry carcasses and poultry products in Brazil. Journal of Food Protection 2013;76(12):2011-2017.
  • Donato DCZ, Gandra ERS, Garcia PDSR, Reis CBM, Gameiro AH. A questão da qualidade no sistema agroindustrial do ovo. In. Anais do 47º Congresso da Sociedade Brasileira de Econonomia, Administração e Sociologia Rural; 2009. Porto Alegre, Rio Grande do Sul. Brasil; 2009. p.1-13.
  • Du X, Jiang X, Ye Y, Guo B, Wang W, Ding J, et al. Next generation sequencing for the investigation of an outbreak of Salmonella Schwarzengrund in Nanjing, China. International Journal of Biological Macromolecules 2017;107(Pt A):393-396.
  • EFSA - European Food Safety Authority and 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 2016. EFSA Journal 2017;15(12):5077.
  • EU - European Commission. The rapid alert system for food and feed: 2017 annual report. Geneva: Health and Food Safety, RASFF; 2018.
  • Firoozeh F, Shahcheraghi F, Salehi TZ, Karimi V, Aslani MM. Antimicrobial resistance profile and presence of class I integrongs among Salmonella enterica serovars isolated from human clinical specimens in Tehran, Iran. Iranian Journal Microbiology 2011;3(3):112-117.
  • Fratamico PM, Strobaugh TP. Simultaneous detection of Salmonella spp and Escherichia coli O157:H7 by multiplex PCR. Journal of Industrial Microbiology and Biotechnology 1998;21(3):92-98.
  • Freitas Neto OC, Galdino VMCA, Campello PL, Almeida AM, Fernandes SA, Berchieri Junior A. Salmonella serovars in laying hen flocks and commercial table eggs from a region of São Paulo State, Brazil. Revista Brasileira de Ciência Avícola 2014;16(2):57-62.
  • Gajraj R, Pooransingh S, Hawker JI, Olowokure B. Multiple outbreaks of Salmonella braenderup associated with consumption of iceberg lettuce. International Journal of Environmental Health Research 2012;22(2):150-155.
  • Galdino VMC, Melo RT, Oliveira RP, Mendonça EP, Nalevaiko PC, Rossi DA. Virulence of Salmonella spp. of poultry products origin and antimicrobial resistance. Bioscience Journal 2013;29:932-939.
  • Gama NMSQ, Berchieri Junior A, Fernandes SA. Occurrence of Salmonella spp in laying hens. Revista Brasileira de Ciência Avícola 2013;5(1):15-21.
  • Grant A, Hashem F, Parveen S. Salmonella and Campylobacter:antimicrobial resistance and bacteriophage control in poultry. Food Microbiology 2016;53:104-109.
  • Hassena AB, Siala M, Guermazi S, Zormati S, Gdoura R, Sellami H. Occurrence and phenotypic and molecular characterization of antimicrobial resistance of Salmonella isolates from food in Tunisia. Journal of Food Protection 2019, 82(7):1166-1175.
  • Hopkins KL, Wootton L, Day MR, Threlfall E. Plasmid-mediated quinolone resistance determinant qnrS1 found in Salmonella enterica strains isolated in the UK. Journal of Antimicrobial Chemotherapy 2007;59(6):1071-1075.
  • Hu YY, Wang YL, Sun QL, Huang ZX, Wang HY, Zhang R, et al. Colistin resistance gene mcr-1 in gut flora of children. International Journal of Antimicrobial Agents 2017;50(4):593-597.
  • Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, De Pinna E, et al. Supplement 2008-2010(n. 48) to the White-Kauffann-Le minor scheme. Research in Microbiology 2014;165:526-530.
  • Iwabuchi E, Maruyama N, Hara A, Nishimura M, Muramatsu M, Ochiai T, et al. Nationwide survey of Salmonella prevalence in environmental dust from layer farms in Japan. Journal of Food Protection 2010;73(11):1993-2000.
  • Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ. Outbreak associated Salmonella enterica serotypes and food commodities, United States, 1998-2008. Emerging Infectious Diseases 2013;19(8):1239-1244.
  • Jensen LB, Birk T, Borck HB, Stehr L, Aabo S, Korsgaard H. Cross and co resistance among Danish porcine E. coli isolates. Research in Veterinary Science 2018;119:247-249.
  • Kottwitz LBM, Back A, Leão JA, Alcocer I, Karan M, Oliveira TCRM. Contaminação por Salmonella spp. em uma cadeia de produção de ovos de uma integração de postura comercial. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2008;60:496-498.
  • Liljebjelke KA, Hofacre CL, White DG, Ayers S, Lee MD, Maurer JJ. Diversity of antimicrobial resistance phenotypes in Salmonella isolated from commercial poultry farms. Frontiers in Veterinary Science 2017;4:96.
  • Long M, Yu H, Chen L, Wu G, Zhao S, Deng W, et al. Recovery of Salmonella isolated from eggs and the commercial layer farms. Gut Pathogens 2017;14:9-74.
  • Ma Z, Yang X, Fang Y, Tong Z, Lin H, Fan H. Detection of Salmonella infection in chickens by an indirect enzyme-linked immunosorbent assay based on presence of PagC antibodies in sera. Foodborne Pathogens and Disease 2018;15(2):109-113.
  • Manie T, Khan S, Brözel VS, Veith WJ, Gouws PA. Antimicrobial resistance of bacteria isolatedfrom slaughtered and retail chickens in South Africa. Letters in Applied Microbiology 1998;26(4):253-258.
  • Micallef SA, Rosenberg Goldstein RE, George A, Kleinfelter L, Boyer MS, McLaughlin CR, et al. Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on mid-Atlantic tomato farms. Environmental Research 2012;114:31-39.
  • Mion L, Colla FL, Cisco IC, Webber B, Diedrich LN, Pilotto F, et al. Perfil de resistência a antimicrobianos por Salmonella Heidelberg isoladas de abatedouro avícola em 2005 e 2009. Acta Scientiae Veterinariae 2014;42:1197.
  • Moraes DMC, Duarte SC, Bastos TSA, Rezende CLG, Leandro NSM, Café MB, et al. Detection of Salmonella spp. by conventional bacteriology and by quantitative polymerase-chain reaction in commercial egg structures. Brazilian Journal of Poultry Science 2016;18(1):117-124.
  • Moreno-Bondi MC, Marazuela MD, Herranz S, Rodriguez E. An overview of sample preparation procedures for LC-MS multiclass antibiotic determination in environmental and food samples. Analytical and Bioanalytical Chemistry 2009;395(4):921-946.
  • Nor Faiza S, Saleha AA, Jalila A, Fauziah N. Occurrence of campylobacter and Salmonella in ducks and duck eggs in Selangor, Malaysia. Tropical Biomedicine 2013;30(1):155-158.
  • Oliveira SD, Santos LR, Schuch DMT, Silva AB, Salle CTP, Canal CW. Detection and identification of salmonellas from poultry by PCR. Veterinary Microbiology 2002;87(1):25-35.
  • Pande VV, Gole VC, McWhorter AR, Abraham S, Chousalkar KK. Antimicrobial resistance of non-typhoidal Salmonella isolates from egg layer flocks and egg shells. International Journal of Food Microbiology 2015;203:23-26.
  • Perdoncini G, Ferreira JI, Lima LM, Rocha DT, Tejkowski TM, Pinto AT, et al. Salmonella spp. em ovos produzidos em sistema agroecológico. Revista Agrocientífica 2014;1(1):33-42.
  • Pezzoli L, Elson R, Little CL, Yip H, Fisher I, Yishai R, et al. Packed with Salmonella - investigation of an international outbreak of Salmonella Senftenberg infection linked to contamination of prepacked basil in 2007. Foodborne Pathogens and Disease 2008;5(5):661-668.
  • Poirel L, Jayol A, Nordamann P. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clinical Microbiology Reviews 2017;30(2):557-596.
  • Rodríguez I, Rodicio MR, Guerra B, Hopkins KL. Potential international spread of multidrug-resistant invasive Salmonella enterica serovar Enteritidis. Emerging Infectious Diseases 2012;18(7):1173-1176.
  • Rodríguez-Martinez JM, Velasco C, Pascual A, Garcia I, Martinez-Martinez L. Correlation of quinolone resistance levels and differences in basal and quinolone-induced expression from three qnrA-containing plasmids. Clinical Microbiology and Infection 2006;12:440-445.
  • Salles RPR, Teixeira RSC, Siqueira AA, Silva EE, Castro SB, Cardoso WM. Monitoramento bacteriológico para Salmonella spp. em poedeira comercial na recria e produção de empresas avícolas da região metropolitana de fortaleza, CE, Brasil. Ciência Animal Brasileira 2008;9(2):427-432.
  • Sapkota AR, Kinney EL, George A, Hulet RM, Cruz-Cano R, Schwab KJ, et al. Lower prevalence of antibiotic-resistant Salmonella on large-scale U.S. conventional poultry farms that transitioned to organic practices. Science of the Total Environment 2014;476-477:387-392.
  • Schwarz S, Silley P, Simjee S, Woodford N, Duijkeren EV, Johnson AP, et al. Assessing the antimicrobial susceptibility of bacteria obtained from animals. Veterinary Microbiology 2010;141(1-2):1-4.
  • Shah DH, Paul NC, Sischo WC, Crespo R, Guard J. Population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes. Poultry Science 2017;96(3):687-702.
  • Shang K, Wei B, Kang M. Distribution and dissemination of antimicrobial-resistant Salmonella in broiler farms with or without enrofloxacin use. BMC Veterinary Research 2018;14(257).
  • Snow LC, Davies RH, Christiansen KC, Carrique-Mas JJ, Wales AD, O’Connor JL, et al. Survey of Salmonella prevalence on commercial layer farms in the United Kingdom. Veterinary Record 2007;161(14):471-476.
  • Soria MC, Soria MA, Bueno DJ, Godano EI, Gómez SC, ViaButron IA, et al. Salmonella spp. contamination in commercial layer hen farms using different types of samples and detection methods. Poultry Science 2017;96(8):2820-2830.
  • Storm DR, Rosenthal KS, Swanson PE. Polymyxin and related peptide antibiotics. Annual Review of Biochemistry 1977;46:723-763.
  • SVS - Secretaria de Vigilância em Saúde. Doenças transmitidas por alimentos. Brasília: Ministério da Saúde, Secretaria de Vigilância em Saúde; 2015. Available from: http://u.saude.gov.br/images/pdf/2015/novembro/09/Apresenta----o-dados-geraisDTA-2015.pdf
    » http://u.saude.gov.br/images/pdf/2015/novembro/09/Apresenta----o-dados-geraisDTA-2015.pdf
  • SVS - Secretaria de Vigilância em Saúde. Doenças transmitidas por alimentos. Brasília: Ministério da Saúde. Secretaria de Vigilância em Saúde; 2019. Available from: http://saude.gov.br/saude-de-a-z/doencas-transmitidas-por-alimentos
    » http://saude.gov.br/saude-de-a-z/doencas-transmitidas-por-alimentos
  • Tagg KA, Francois Watkins L, Moore MD, Bennett C, Joung YJ, Chen JC, et al. Novel trimethoprim resistance gene dfrA34 identified in Salmonella Heidelberg in the USA. Journal of Antimicrobial Chemotherapy 2019;74(1):38-41.
  • Thamlikitkul V, Tiengrim S. In vitro activity of colistin plus sulbactam against extensive-drug-resistant Acinetobacter baumannii by checkerboard method. Journal of the Medical Association of Thailand 2014;97(Suppl.):S1-S3.
  • Wei Z, Xu X, Yan M, Chang H, Li Y, Kan B, et al. Salmonella typhimurium and Salmonella enteritidis infections in sporadic diarrhea in children: source tracing and resistance to third-generation cephalosporins and ciprofloxacin. Foodborne Pathogens and Diseases 2019;16(4):244-255.
  • Wright GD. Q&A: antibiotic resistance:where does it come from and what can we do about it? BMC Biology 2010;8:123.
  • Xu X, Wu S, Ye X, Liu Y, Shi W, Zhang Y,et al. Prevalence and expression of the plasmid-mediated quinolone resistance determinant qnrA1. Antimicrobial Agents and Chemotherapy 2007;51:4105-4110.
  • Yan H, Li L, Alam MJ, Shinoda S, Miyoshi S, Shi L. Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. International Journal of Food Microbiology 2010;143(3):230-234.

Publication Dates

  • Publication in this collection
    07 Oct 2020
  • Date of issue
    2020

History

  • Received
    19 Jan 2020
  • Accepted
    08 May 2020
Fundacao de Apoio a Ciência e Tecnologia Avicolas Rua Barão de Paranapanema, 146 - Sala 72, Bloco A, Bosque, Campinas, SP - 13026-010. Tel.: 19 3255-8500 - Campinas - SP - Brazil
E-mail: revista@facta.org.br