Abstract
Salmonella spp. causes foodborne diseases related to the consumption of contaminated foods, especially poultry products. This study aimed to investigate the occurrence of Salmonella spp. serovars in raw eggs from supermarkets and street food markets in southern Brazil, to analyze virulence genes, resistance profiling to antimicrobials and sanitizers, and to determine the susceptibility of the isolates to Butia odorata extract. Among 160 samples analyzed, just two (1.25%) were positive for Salmonella spp.. One positive sample was from egg yolk (S. enterica serovar Gallinarum, isolate S28), and another one was from eggshell (S. enterica serovar Panama, isolate S37). Regarding the virulence genes, the isolate S37 harbored all the genes evaluated (hilA, invA, spvC, sefA, and pefA), while the isolate S28 did not harbor the pefA gene. The isolate S28 was resistant to tobramycin, azithromycin, and trimethoprim, while the isolate S37 showed resistance profile just to nalidixic acid. However, none of the resistance genes evaluated were identified. Both isolates showed resistance to benzalkonium chloride, chlorhexidine digluconate, sodium hypochlorite, and peracetic acid, presenting high MIC values for these sanitizers. In contrast, B. odorata extract showed antimicrobial activity against the isolates S28 and S37, however, more studies are needed to prove its potential as a natural antimicrobial compound.
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References
Anjum MF, Choudhary S, Morrison V, Snow LC, Mafura M, Slickers P, Ehricht R, Woodward MJ (2011) Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain. J Antimicrob Chem 66(3):550–559
Arshad MM, Wilkins MJ, Downes FP, Rahbar MH, Erskine RJ, Boulton ML, Younnus M, Saeed AM (1995) Epidemiologic attributes of invasive non-typhoidal Salmonella infections in Michigan, 1995–2001. Int J Infec Dis 12:176–182
Besser JM (2018) Salmonella epidemiology: a whirlwind of change. Food Microbiol 71:55–59
Brasil. Surtos de Doenças Transmitidas por Alimentos no Brasil (2018) Available at: http://www.saude.gov.br/images/pdf/2018/julho/02/Apresentacao-Surtos-DTA-Junho-2018.pdf. Accessed 26 August 2019.
Campioni F, Bergamini AMM, Falcão JP (2012) Genetic diversity, virulence genes and antimicrobial resistance of Salmonella Enteritidis isolated from food and humans over a 24-year period in Brazil. Food Microbiol 32:254–264
Cardona-Castro N, Restrepo-Pineda E, Correa-Ochoa M (2002) Detection of hilA Gene sequences in Serovars of Salmonella enterica subspecies Enterica. Mem Inst Osw Cruz 97(8):1153–1156
Clouthier SC, Müller K-H, Doran JL, Collinson SK, Kay WW (1993) Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis. J Bact 175(9):2523–2533
CLSI (Clinical and Laboratory Standards Institute), (2017) Performance standards for antimicrobial susceptibility testing; twenty-seven informational supplement, CLSI document M100–S25. PA, USA
Cortes VD, Rodriguez V, Verjan GN (2017) Phenotypic and Genotypic Antibiotic Resistance of Salmonella from Chicken Carcasses Marketed at Ibague. Colombia Braz J Poul Sci 19(2):347–354
EFSA (European Food Safety Authority) (2018) Salmonella, 2018. Available at: http://www.efsa.europa.eu/en/topics/topic/salmonella. Accessed 12 september 2018.
Ethelberg S, Mølbak K, Josefsen MH (2014) Bacteria: Salmonella Non-Typhi. Encyc Food Saf 1:501–514
Fardsanei F, Soltan Dallal MM, Douraghi M, Salehi TZ, Mahmoodi M, Memariani H, Nikkhahi F (2017) Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype Enteritidis isolated from meats and eggs. Microb Pathog 107:451–456
Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Immerseel FV (2009) Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev 33:718–738
Grape M, Sundström L, Kronvall G (2003) Sulphonamide resistance gene sul3 found in Escherichia coli isolates from human sources. J Antimicrob Chemot 52(6):1022–1024
Green MR, Sambrook J (2012) Molecular Cloning: A Laboratory Manual, 4th edn. Cold Spring Harbor Laboratory Press, New York
Haubert L, Zehetmeyr ML, Pereira YMN, Kroning IS, Maia DSV, Sehn CP, Lopes GV, Lima AS, Silva WP (2019) Tolerance to benzalkonium chloride and antimicrobial activity of Butia odorata Barb. Rodr. extract in Salmonella spp. isolates from food and food environments. Food Res Int 116:652–659
Kalupahana RS, Rajapaksa DIG, Fernando PS, Thilakarathne DS, Abeynayake P (2017) Occurrence and characterization of nontyphoidal Salmonella in retail table eggs in Kandy district of Sri Lanka. Food Cont 72:244–248
Kehrenberg C, Schwarz S (2001) Occurrence and linkage of genes coding for resistance to sulfonamides, streptomycin and chloramphenicol in bacteria of the genera Pasteurella and Mannheimia. FEMS Microbiol Lett 205(2):283–290
Kerrn MB, Klemmensen T, Frimodt-Moller N, Espersen F (2002) Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J Antimicr Chemot 50:513–516
Kikuvi GM, Schwarz S, Ombui JN, Mitema ES, Kehrenberg C (2007) Streptomycin and chloramphenicol resistance genes in Escherichia coli isolates from cattle, pigs, and chicken in Kenya. Microb Drug Resist 13(1):62–68
Long M, Lai H, Deng W, Zhou K, Li B, Liu S, Fan L, Wang H, Zou L (2016) Disinfectant susceptibility of different Salmonella serotypes isolated from chicken and egg production chains. J App Microbiol 121(3):672–681
Maia DSV, Aranha BC, Chaves FC, Silva WP (2017) Antibacterial activity of Butia odorata Barb. Rodr extracts Trends Phyto Res 1(3):169–174
Martelli F, Davies RH (2012) Salmonella serovars isolated from table eggs: an overview. Food Res Int 45:745–754
Martineau F, Picard FJ, Grenier L, Roy PH, Ouellette M, Trial E, Bergeron MG (2000) Multiplex PCR assays for the detection of clinically relevant antibiotic resistance genes in staphylococci isolated from patients infected after cardiac surgery. J Antimicr Chemot 46:527–533
Matsui H, Bacot CM, Garlington WA, Doyle TJ, Roberts S, Gulig PA (2001) Virulence Plasmid-Borne spvB and spvC Genes Can Replace the 90-Kilobase Plasmid in Conferring Virulence to Salmonella enterica Serovar Typhimurium in Subcutaneously Inoculated Mice. J Bac 183(15):4652–4658
Poppe C, Duncan CL, Mazzocco A (1998) Salmonella Contamination of Hatching and Table Eggs: a Comparison. Can J Vet Res 62:91–198
Rychlik I, Gregorova D, Hradecka H (2006) Distribution and function of plasmids in Salmonella enterica. Vet Microbiol 112:1–10
Singh S, Yadav AS, Singh SM, Bharti P (2010) Prevalence of Salmonella in chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res Int 43:2027–2030
Rowlands REG, Ristori CA, Ikuno AA, Barbosa ML, Jakabi M, Franco BDGM (2014) Prevalence of drug resistance and virulence features in Salmonella spp. isolated from foods associated or not with salmonellosis in Brazil. Rev Inst Med Trop São Paulo 56(6):461–467
Shen X, Sun X, Xie Q, Liu H, Zhao Y, Pan Y, Hwang C, Wu VCH (2014) Antimicrobial effect of blueberry (Vaccinium corymbosum L.) extracts against the growth of Listeria monocytogenes and Salmonella Enteritidis. Food Cont 35(1):159–165
Sjolund-Karlsson M, Joyce K, Blickenstaff K, Ball T, Haro J, Medalla FM, Fedorka-Cray P, Zhao S, Crump JA, Whichard JM (2011) Antimicrobial susceptibility to azithromycin among Salmonella enterica Isolates from the United States. Antimicrob Agents Chemot 55(9):3985–3989
Thames CH, Pruden A, James RE, Ray PP, Knowlton KF (2012) Excretion of antibiotic resistance genes by dairy calves fed milk replacers with varying doses of antibiotics. Front Microbiol 3:1–12
Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesus J, Platt DJ, Olsen JE (2000) Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125:229–255
Weerakkody NS, Caffin N, Turner MS, Dykes GA (2010) In vitro antimicrobial activity of less-utilized spice and herb extracts against selected food-borne bacteria. Food Control 21(10):1408–1414
Zhu Y, Lai H, Zou L, Yin S, Wang C, Han X, Xia X, Hu K, He L, Zhou K, Chen S, Ao X, Liu S (2017) Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. Int J Food Microbiol 259:43–51
Acknowledgements
The authors thanks to the Laboratório de Enterobactérias—Fundação Instituto Oswaldo Cruz (FIOCRUZ) for serotyping Salmonella spp. isolates.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, Programa Nacional de Pós-Doutorado (PNPD), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (306367/2019-0).
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Haubert, L., Maia, D.S.V., Rauber Würfel, S.F. et al. Virulence genes and sanitizers resistance in Salmonella isolates from eggs in southern Brazil. J Food Sci Technol 59, 1097–1103 (2022). https://doi.org/10.1007/s13197-021-05113-5
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DOI: https://doi.org/10.1007/s13197-021-05113-5