Abstract
Genetic profiles of Salmonella Minnesota isolates were analyzed using pulsed-field gel electrophoresis (PFGE). In total, 13 isolates obtained from the broiler industry collected in the states of Minas Gerais (11) and São Paulo (2), as well as five recovered from cases of foodborne infections in humans in the states of Minas Gerais (2), Santa Catarina (1), and Rio Grande do Sul (2), were submitted to PFGE. These 18 S. Minnesota isolates together with other 12 of poultry origin were also subjected to antimicrobial susceptibility testing. The PFGE analysis of 18 strains of S. Minnesota generated a dendrogram that grouped the isolates with 83–90% similarity into four main clusters. Among them, cluster “A” grouped the majority of isolates (13), including two of human origin that showed 90% similarity with a broiler isolate, both recovered in Minas Gerais. The S. Minnesota isolates showed resistance to tetracycline (80%), cefoxitin (80%), ceftazidime (46.7%), nalidixic acid (23.3%), ciprofloxacin (13.3%), and streptomycin (10%). No resistance to gentamicin, chloramphenicol, meropenem, nitrofurantoin, and sulfamethoxazole-trimethoprim was found. Moreover, 23.3% of the evaluated isolates presented multi-resistance profile, all from Minas Gerais. The results highlight the importance of further studies involving S. Minnesota, which is prevalent in the Brazilian broiler flocks and could provoke foodborne infection in humans.
Data availability
Not applicable.
Code availability
Not applicable.
References
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. Poult Sci 94(3):433–441. https://doi.org/10.3382/ps/peu081
Ferrari RG, Rosario D, Cunha-Neto A, Mano SB, Figueiredo E, Conte-Junior CA (2019) Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis. Appl Environ Microbiol 85(14):e00591-e619. https://doi.org/10.1128/AEM.00591-19
Monte DF, Sellera FP (2020) Salmonella. Emerg Infect Dis 26(12):2955. https://doi.org/10.3201/eid2612.et2612
MAPA (2018) Nota Técnica: Salmonella em carne de frango. Ministério da Agricultura, Pecuária e Abastecimento. https://www.gov.br/agricultura/pt-br/assuntos/inspecao/produtos-animal/arquivos-publicacoes-dipoa/entenda-melhor-salmonela-em-carne-de-frango. Acessed 10 Jan 2021.
Gieraltowski L, Higa J, Peralta V, Green A, Schwensohn C, Rosen H, Libby T, Kissler B, Marsden-Haug N, Booth H, Kimura A, Grass J, Bicknese A, Tolar B, Defibaugh-Chávez S, Williams I, Wise M (2016) National outbreak of multidrug resistant Salmonella Heidelberg infections linked to a single poultry company. PLoS ONE 11(9):e0162369. https://doi.org/10.1371/journal.pone.0162369
Souza AIS, Saraiva MMS, Casas MRT, Oliveira GM, Cardozo MV, Benevides VP, Barbosa FO, Freitas Neto OC, Almeida AM, Junior BA (2020) High occurrence of β-lactamase-producing Salmonella Heidelberg from poultry origin. PLoS ONE 15(3):e0230676. https://doi.org/10.1371/journal.pone.0230676
Melo RT, Resende AR, Mendonça EP, Nalevaiko PC, Monteiro GP, Buiatte ABG, Rossi DA (2020) Salmonella Minnesota de origem avícola apresenta fatores de virulência e risco potencial aos humanos. Arq Bras Med Vet Zootec 72(4):1353–1362. https://doi.org/10.1590/1678-4162-10884
Okamoto AS, Andreatti Filho RL, Rocha TS, Menconi A, Marietto-Gonçalves GA (2009) Detection and transfer of antimicrobial resistance gene integron in Salmonella Enteritidis derived from avian material. Rev Bras Cienc Avic 11(3):195–201. https://doi.org/10.1590/S1516-635X2009000300009
CLSI (2019) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Clinical and Laboratory Standards Institute. https://clsi.org/standards/products/veterinary-medicine/documents/vet01/. Acessed 27 Jan 2021.
Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, Barrett TJ (2006) Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 3(1):59–67. https://doi.org/10.1089/fpd.2006.3.59
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18(3):268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Landers TF, Cohen B, Wittum TE, Larson EL (2012) A review of antibiotic use in food animals: perspective, policy and potential. Public Health Rep 127(1):4–22. https://doi.org/10.1177/003335491212700103
Mendonça EP, de Melo RT, Nalevaiko PC, Monteiro GP, Fonseca BB, Galvão NN, Giombelli A, Rossi DA (2019) Spread of the serotypes and antimicrobial resistance in strains of Salmonella spp. isolated from broiler. Braz J Microbiol 50(2):515–522. https://doi.org/10.1007/s42770-019-00054-w
Monte DF, Lincopan N, Berman H, Cerdeira L, Keelara S, Thakur S, Fedorka-Cray PJ, Landgraf M (2019) Genomic features of high-priority Salmonella enterica serovars circulating in the food production chain, Brazil, 2000–2016. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-45838-0
Perin AP, Martins BTF, Barreiros MAB, Yamatogi RS, Nero LA, Dos Santos Bersot L (2020) Occurrence, quantification, pulse types, and antimicrobial susceptibility of Salmonella sp. isolated from chicken meat in the state of Paraná. Brazil. Food Microbiol 51(1):335–345. https://doi.org/10.1007/s42770-019-00188-x
Voss-Rech D, Potter L, Vaz CS, Pereira DI, Sangioni LA, Vargas ÁC, de Avila BS (2017) Antimicrobial resistance in nontyphoidal Salmonella isolated from human and poultry-related samples in Brazil: 20-year meta-analysis. Foodborne Pathog Dis 14(2):116–124. https://doi.org/10.1089/fpd.2016.2228
CDC (2019) Antibiotic resistance threats in the United States. U.S. Department of Health and Human Services. https://www.cdc.gov/drugresistance/Biggest-Threats.html. Accessed 28 Jan 2021.
Jacoby GA (2009) AmpC beta-lactamases. Clin Microbiol Rev 22(1):161–182. https://doi.org/10.1128/CMR.00036-08
Edirmanasinghe R, Finley R, Parmley EJ, Avery BP, Carson C, Bekal S, Golding G, Mulvey MR (2017) A whole-genome sequencing approach to study cefoxitin-resistant Salmonella enterica serovar Heidelberg isolates from various sources. Antimicrob Agents Chemother 61(4):e01919-e2016. https://doi.org/10.1128/AAC.01919-16
Van den Berg RR, Dissel S, Rapallini MLBA, van der Weijden CC, Wit B, Heymans R (2019) Characterization and whole genome sequencing of closely related multidrug-resistant Salmonella enterica serovar Heidelberg isolates from imported poultry meat in the Netherlands. PLoS ONE 14(7):e0219795. https://doi.org/10.1371/journal.pone.0219795
Melo RT, Galvão NN, Guidotti-Takeuchi M, Peres PABM, Fonseca BB, Profeta R, Azevedo VAC, Monteiro GP, Brenig B, Rossi DA (2021) Molecular characterization and survive abilities of Salmonella Heidelberg strains of poultry origin in Brazil. Front Microbiol 12:674147. https://doi.org/10.3389/fmicb.2021.674147
Monte DFM, Andrigheto C, Ribeiro VB, Landgraf M, Destro MT (2020) Highly clonal relationship among Salmonella Enteritidis isolates in a commercial chicken production chain, Brazil. Braz J Microbiol 51:2049–2056. https://doi.org/10.1007/s42770-020-00372-4
Acknowledgements
We are grateful to TECSA Laboratory and to the staff of the Laboratory of Enterobacteria of the Oswaldo Cruz Foundation (FioCruz) for the strains and technical support.
Author information
Authors and Affiliations
Contributions
All authors whose names appear on the submission made substantial contributions to the conception of the work, interpretation of data, and critical review, agreeing to be accountable for all aspects of the work.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Waldir P. Elias
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Moreira, J.P.F.F., do Monte, D.F.M., Lima, C.d. et al. Molecular genotyping reveals inter-regional relatedness among antimicrobial resistant Salmonella Minnesota strains isolated from poultry farm and humans, Brazil. Braz J Microbiol 53, 503–508 (2022). https://doi.org/10.1007/s42770-021-00666-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-021-00666-1