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Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye

Year 2024, Volume: 19 Issue: 2, 72 - 77, 30.08.2024
https://doi.org/10.17094/vetsci.1539862

Abstract

Salmonella enterica serovar Enteritidis (S. Enteritidis) is the most predominant serovar in poultry and eggs, and it poses a significant threat to public health worldwide as it is a leading cause of salmonellosis in humans, which is transmitted through the consumption of contaminated poultry products like eggs. The objective of this study was to evaluate the presence of S. Enteritidis in household chicken eggs collected from Erzurum Province, Türkiye. A total of 168 household chicken eggs were collected from 168 small family poultry farms. Salmonella spp. was not isolated from any of the examined egg internal contents; however, successful isolation and identification of Salmonella spp. were achieved in 4 of the shell samples. Further characterization of the identified Salmonella spp. isolates was performed at the serovar level using 16S rDNA sequence analysis, and all 4 isolates were identified as S. Enteritidis. In conclusion, this study highlights the inherent risk of S. Enteritidis contamination in household chicken eggs and emphasizes the vital significance of implementing stringent food safety measures to safeguard consumer well-being and ensure the protection of public health.

References

  • 1. Popa GL, Papa MI. Salmonella spp. infection-a continuous threat worldwide. Germs. 2021;11(1):88-96.
  • 2. Pijnacker R, Dallman TJ, Tijsma AS et al. An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: a microbiological and epidemiological study. Lancet Infect Dis. 2019;19(7):778-786.
  • 3. Zhang G, Thau E, Brown EW, Hammack TS. Comparison of a novel strategy for the detection and isolation of Salmonella in shell eggs with the Food and Drug Administration Bacteriological Analytical Manual method. Poult Sci. 2013;92(12):3266-3274.
  • 4. Almeida C, Cerqueira L, Azevedo N, Vieira M. Detection of Salmonella enterica serovar Enteritidis using real time PCR, immunocapture assay, PNA FISH and standard culture methods in different types of food samples. Int J Food Microbiol. 2013;161(1):16-22.
  • 5. Pasquali F, De Cesare A, Valero A, Olsen JE, Manfreda G. Improvement of sampling plans for Salmonella detection in pooled table eggs by use of real-time PCR. Int J Food Microbiol. 2014;1(184):31-34.
  • 6. Wang X, Wang H, Li T, et al. Characterization of Salmonella spp. isolated from chickens in Central China. BMC Vet Res. 2020;16 (1):299.
  • 7. Church DL, Cerutti L, Gürtler A, Griener T, Zelazny A, Emler S. Performance and application of 16S rRNA gene cycle sequencing for routine identification of bacteria in the clinical microbiology laboratory. Clin Microbiol Rev. 2020;33(4):e00053-19.
  • 8. Cruz-Méndez JS, Ortiz-Muñoz JD, Rondon-Barragan IS. Genotyping of Salmonella enterica strains from animal and human origin using three molecular techniques. Iraqi J Vet Sci. 2022;36(2):531-538.
  • 9. Cufaoglu G, Ambarcioglu P, Derinöz AN, Ayaz ND. Prevalence, Serotype Diversity and Antibiotic Resistance of Salmonella Among Poultry Meat and Eggs in Turkiye: A Meta-analysis. J Agric Sci. 2023;29(2):519-533.
  • 10. Özdemir D. The structural characteristics, management, and challenges of backyard poultry farming in residential areas of Turkey. Animals. 2020;10(12):2336.
  • 11. Chousalkar KK, Flynn P, Sutherland M, Roberts JR, Cheetham BF. Recovery of Salmonella and Escherichia coli from commercial eggshells and effect of translucency on bacterial penetration in eggs. Int J Food Microbiol. 2010;142(1-2):207-213.
  • 12. Fredriksson NJ, Hermansson M, Wilén BM. The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PloS One. 2013;8(10):e76431.
  • 13. Gantois I, Ducatelle R, Pasmans F, et al. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev. 2009;33(4):718-738.
  • 14. Chemaly M, Huneau-Salaün A, Labbe A, Houdayer C, Petetin I, Fravalo P. Isolation of Salmonella enterica in laying-hen flocks and assessment of eggshell contamination in France. J Food Prot. 2009;72(10):2071-2077.
  • 15. Long M, Yu H, Chen L, et al. Recovery of Salmonella isolated from eggs and the commercial layer farms. Gut Pathog. 2017;9(1):74.
  • 16. Moosavy MH, Esmaeili S, Bagheri Amiri F, Mostafavi E, Zahraei Salehi T. Detection of Salmonella spp in commercial eggs in Iran. Iran J Microbiol. 2015;7(1):50-54.
  • 17. Radkowski M. Occurrence of Salmonella spp. in consumption eggs in Poland. Int J Food Microbiol. 2001;64(1-2):189-191.
  • 18. Suresh T, Hatha AA, Sreenivasan D, Sangeetha N, Lashmanaperumalsamy P. Prevalence and antimicrobial resistance of Salmonella enteritidis and other salmonellas in the eggs and egg-storing trays from retail markets of Coimbatore, South India. Food Microbiol. 2006;23(3):294-299.
  • 19. Gao D, Ji H, Wang L. Fitness Trade-Offs in Phage Cocktail-Resistant Salmonella enterica Serovar Enteritidis Results in Increased Antibiotic Susceptibility and Reduced Virulence. Microbiol Spectr. 2022,10(5):e0291422.
  • 20. Webb HE, Kim JY, Tagg KA. Fourteen mcr-1-Positive Salmonella enterica Isolates Recovered from Travelers Returning to the United States from the Dominican Republic. Microbiol Resour Announc. 2022;11(5):e0011822.
  • 21. Li C, Tyson GH, Hsu CH. Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica. Front Microbiol. 2021;12:777817.
  • 22. Rehman MA, Ziebell K, Nash JH, et al. Complete Genome Sequences of 16 Canadian Strains of Salmonella enterica subsp. enterica Serovar Enteritidis. Genome Announc. 2014; 2(2): e00330-14.

Aile Tipi Tavuk Yumurtalarında Salmonella Enterica Serovar Enteritidis’in Tespiti ve Moleküler Karakterizasyonu: Erzurum İli, Türkiye’den Bir Vaka Çalışması

Year 2024, Volume: 19 Issue: 2, 72 - 77, 30.08.2024
https://doi.org/10.17094/vetsci.1539862

Abstract

Salmonella enterica serovar Enteritidis (S. Enteritidis), kümes hayvanları ve yumurtalarda en yaygın serovardır. Dünya genelinde halk sağlığı için önemli bir tehdit oluşturmaktadır çünkü insanlarda salmonellozun önde gelen nedenidir. Kontamine tavuk ürünleri, özellikle yumurtaların tüketimi yoluyla insanlara bulaşır. Bu çalışmanın amacı, Türkiye'nin Erzurum ilinden toplanan evcil tavuk yumurtalarında S. Enteritidis'in varlığını değerlendirmektir. Toplam 168 evcil tavuk yumurtası, 168 adet küçük aile tipi tavuk çiftliğinden toplandı. Salmonella spp., incelenen hiçbir yumurta içeriğinden izole edilmedi. Ancak Salmonella spp.'nin başarılı izolasyonu ve tanısı 4 kabuk örneğinde elde edildi. Tanımlanan Salmonella spp. izolatlarının serovar düzeyinde daha fazla karakterizasyonu için 16S rDNA sekans analizi kullanıldı. Tüm izolatlar S. Enteritidis olarak tanımlandı. Sonuç olarak, bu çalışma ev tipi tavuk yumurtalarında S. Enteritidis kontaminasyon riskini ortaya koymakta, tüketicinin sağlığını korumak ve halk sağlığını güvence altına almak için sıkı gıda güvenliği önlemlerinin uygulanmasının hayati önemini vurgulamaktadır.

References

  • 1. Popa GL, Papa MI. Salmonella spp. infection-a continuous threat worldwide. Germs. 2021;11(1):88-96.
  • 2. Pijnacker R, Dallman TJ, Tijsma AS et al. An international outbreak of Salmonella enterica serotype Enteritidis linked to eggs from Poland: a microbiological and epidemiological study. Lancet Infect Dis. 2019;19(7):778-786.
  • 3. Zhang G, Thau E, Brown EW, Hammack TS. Comparison of a novel strategy for the detection and isolation of Salmonella in shell eggs with the Food and Drug Administration Bacteriological Analytical Manual method. Poult Sci. 2013;92(12):3266-3274.
  • 4. Almeida C, Cerqueira L, Azevedo N, Vieira M. Detection of Salmonella enterica serovar Enteritidis using real time PCR, immunocapture assay, PNA FISH and standard culture methods in different types of food samples. Int J Food Microbiol. 2013;161(1):16-22.
  • 5. Pasquali F, De Cesare A, Valero A, Olsen JE, Manfreda G. Improvement of sampling plans for Salmonella detection in pooled table eggs by use of real-time PCR. Int J Food Microbiol. 2014;1(184):31-34.
  • 6. Wang X, Wang H, Li T, et al. Characterization of Salmonella spp. isolated from chickens in Central China. BMC Vet Res. 2020;16 (1):299.
  • 7. Church DL, Cerutti L, Gürtler A, Griener T, Zelazny A, Emler S. Performance and application of 16S rRNA gene cycle sequencing for routine identification of bacteria in the clinical microbiology laboratory. Clin Microbiol Rev. 2020;33(4):e00053-19.
  • 8. Cruz-Méndez JS, Ortiz-Muñoz JD, Rondon-Barragan IS. Genotyping of Salmonella enterica strains from animal and human origin using three molecular techniques. Iraqi J Vet Sci. 2022;36(2):531-538.
  • 9. Cufaoglu G, Ambarcioglu P, Derinöz AN, Ayaz ND. Prevalence, Serotype Diversity and Antibiotic Resistance of Salmonella Among Poultry Meat and Eggs in Turkiye: A Meta-analysis. J Agric Sci. 2023;29(2):519-533.
  • 10. Özdemir D. The structural characteristics, management, and challenges of backyard poultry farming in residential areas of Turkey. Animals. 2020;10(12):2336.
  • 11. Chousalkar KK, Flynn P, Sutherland M, Roberts JR, Cheetham BF. Recovery of Salmonella and Escherichia coli from commercial eggshells and effect of translucency on bacterial penetration in eggs. Int J Food Microbiol. 2010;142(1-2):207-213.
  • 12. Fredriksson NJ, Hermansson M, Wilén BM. The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PloS One. 2013;8(10):e76431.
  • 13. Gantois I, Ducatelle R, Pasmans F, et al. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev. 2009;33(4):718-738.
  • 14. Chemaly M, Huneau-Salaün A, Labbe A, Houdayer C, Petetin I, Fravalo P. Isolation of Salmonella enterica in laying-hen flocks and assessment of eggshell contamination in France. J Food Prot. 2009;72(10):2071-2077.
  • 15. Long M, Yu H, Chen L, et al. Recovery of Salmonella isolated from eggs and the commercial layer farms. Gut Pathog. 2017;9(1):74.
  • 16. Moosavy MH, Esmaeili S, Bagheri Amiri F, Mostafavi E, Zahraei Salehi T. Detection of Salmonella spp in commercial eggs in Iran. Iran J Microbiol. 2015;7(1):50-54.
  • 17. Radkowski M. Occurrence of Salmonella spp. in consumption eggs in Poland. Int J Food Microbiol. 2001;64(1-2):189-191.
  • 18. Suresh T, Hatha AA, Sreenivasan D, Sangeetha N, Lashmanaperumalsamy P. Prevalence and antimicrobial resistance of Salmonella enteritidis and other salmonellas in the eggs and egg-storing trays from retail markets of Coimbatore, South India. Food Microbiol. 2006;23(3):294-299.
  • 19. Gao D, Ji H, Wang L. Fitness Trade-Offs in Phage Cocktail-Resistant Salmonella enterica Serovar Enteritidis Results in Increased Antibiotic Susceptibility and Reduced Virulence. Microbiol Spectr. 2022,10(5):e0291422.
  • 20. Webb HE, Kim JY, Tagg KA. Fourteen mcr-1-Positive Salmonella enterica Isolates Recovered from Travelers Returning to the United States from the Dominican Republic. Microbiol Resour Announc. 2022;11(5):e0011822.
  • 21. Li C, Tyson GH, Hsu CH. Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica. Front Microbiol. 2021;12:777817.
  • 22. Rehman MA, Ziebell K, Nash JH, et al. Complete Genome Sequences of 16 Canadian Strains of Salmonella enterica subsp. enterica Serovar Enteritidis. Genome Announc. 2014; 2(2): e00330-14.
There are 22 citations in total.

Details

Primary Language English
Subjects Veterinary Microbiology
Journal Section Research Articles
Authors

Berna Yanmaz

Ediz Kağan Özgen

Publication Date August 30, 2024
Published in Issue Year 2024 Volume: 19 Issue: 2

Cite

APA Yanmaz, B., & Özgen, E. K. (2024). Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye. Veterinary Sciences and Practices, 19(2), 72-77. https://doi.org/10.17094/vetsci.1539862
AMA Yanmaz B, Özgen EK. Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye. Veterinary Sciences and Practices. August 2024;19(2):72-77. doi:10.17094/vetsci.1539862
Chicago Yanmaz, Berna, and Ediz Kağan Özgen. “Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye”. Veterinary Sciences and Practices 19, no. 2 (August 2024): 72-77. https://doi.org/10.17094/vetsci.1539862.
EndNote Yanmaz B, Özgen EK (August 1, 2024) Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye. Veterinary Sciences and Practices 19 2 72–77.
IEEE B. Yanmaz and E. K. Özgen, “Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye”, Veterinary Sciences and Practices, vol. 19, no. 2, pp. 72–77, 2024, doi: 10.17094/vetsci.1539862.
ISNAD Yanmaz, Berna - Özgen, Ediz Kağan. “Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye”. Veterinary Sciences and Practices 19/2 (August 2024), 72-77. https://doi.org/10.17094/vetsci.1539862.
JAMA Yanmaz B, Özgen EK. Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye. Veterinary Sciences and Practices. 2024;19:72–77.
MLA Yanmaz, Berna and Ediz Kağan Özgen. “Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye”. Veterinary Sciences and Practices, vol. 19, no. 2, 2024, pp. 72-77, doi:10.17094/vetsci.1539862.
Vancouver Yanmaz B, Özgen EK. Detection and Molecular Characterization of Salmonella Enterica Serovar Enteritidis in Household Chicken Eggs: A Case Study From Erzurum, Türkiye. Veterinary Sciences and Practices. 2024;19(2):72-7.

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