Skip to main content

Advertisement

SpringerLink
Log in

Virulence genes and sanitizers resistance in Salmonella isolates from eggs in southern Brazil

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Besser JM (2018) Salmonella epidemiology: a whirlwind of change. Food Microbiol 71:55–59

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Green MR, Sambrook J (2012) Molecular Cloning: A Laboratory Manual, 4th edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Maia DSV, Aranha BC, Chaves FC, Silva WP (2017) Antibacterial activity of Butia odorata Barb. Rodr extracts Trends Phyto Res 1(3):169–174

    CAS  Google Scholar 

  • Martelli F, Davies RH (2012) Salmonella serovars isolated from table eggs: an overview. Food Res Int 45:745–754

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Poppe C, Duncan CL, Mazzocco A (1998) Salmonella Contamination of Hatching and Table Eggs: a Comparison. Can J Vet Res 62:91–198

    Google Scholar 

  • Rychlik I, Gregorova D, Hradecka H (2006) Distribution and function of plasmids in Salmonella enterica. Vet Microbiol 112:1–10

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Departamento de Ciência E Tecnologia Agroindustrial, Faculdade de Agronomia Eliseu Maciel, Universidade Federal de Pelotas (UFPel), Pelotas, RS, Brazil

    Louise Haubert, Darla Silveira Volcan Maia, Cristiane Vaniel & Wladimir Padilha da Silva

  2. Faculdade de Veterinária, Universidade Federal de Pelotas (UFPel), Pelotas, RS, Brazil

    Simone de Fátima Rauber Würfel

  3. Núcleo de Biotecnologia, Centro de Desenvolvimento Tecnológico, Universidade Federal de Pelotas (UFPel), Pelotas, RS, Brazil

    Wladimir Padilha da Silva

Authors
  1. Louise Haubert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Darla Silveira Volcan Maia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simone de Fátima Rauber Würfel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristiane Vaniel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wladimir Padilha da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wladimir Padilha da Silva.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-021-05113-5

Keywords

Search

Navigation