Investigation of Genetic-molecular Sources of Multidrug Resistance of Salmonella Isolated from Eggs
Social Determinants of Health,
Vol. 8 (2022),
1 January 2022
,
Page 1-11
https://doi.org/10.22037/sdh.v8i1.39325
Abstract
Background: Bacteria can be transmitted to consumers around the world due to the movement of animals, and food products. One of the most important sources of Salmonella transmission to humans is through eggs.
Methods: 500 egg samples from 37 Iranian brands were extracted from Salmonella yolk and shell source and after confirmation by differential phenotypic methods and resistance test for tetracycline, cellophanamide and nitrofurantoin-furazolidone antibiotics were performed. DNA of strains was extracted and using PCR with specific primers, the presence of tetA, tetB, tetC, tetD, tetG, tetE, tetE, tetH, sul (I), sul (II), sul (III), nfsA, nfsB were examined according to control DNA (ATCC14028).
Results: Among the genes of teta, tetb.tetc, tetd, tete, tetf, tetg and teth, the presence of tetc was seen in 81% of the samples and not in 19% of them. Other tetracycline resistance genes were not found in the samples. Tracing of genes related to sulfonamide resistance by PCR showed that among the Sul1, Sul2, and Sul3 genes, sulfonamide resistance of Sul2 was observed in 95.5% of the samples and was not seen in 4.5% of the samples. Nitrofurantoin resistance genes in the samples showed that 9.1% of the samples contained nfsa gene and 4.5% contained nfsb gene. Other samples did not have any nitrofurantoin resistance gene.
Conclusion: Improper use of antibiotics has caused multidrug resistance to Salmonella, so the study of genes and resistance mechanisms in Salmonella strains isolated from produced eggs in Iran is vital.
Keywords:
- Salmonella, Multidrug resistance, Sulfanamide, Tetracycline, Nitrofurantoin. Resistance gene
How to Cite
Saram , M. ., Chaichi Nosrati, A., Modiri , L. ., & Issazadeh , K. . (2022). Investigation of Genetic-molecular Sources of Multidrug Resistance of Salmonella Isolated from Eggs. Social Determinants of Health, 8(1), 1–11. https://doi.org/10.22037/sdh.v8i1.39325
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12. McWhorter AR, Chousalkar KK. From hatch to egg grading: monitoring of Salmonella shedding in free-range egg production systems. Vet Res. 2019;50(1):58-70. https://doi.org/10.1186/s13567-019-0677-4
13. Huang X, Zhou X, Jia B, Li N, Jia J, He M, He Y, Qin X, Cui Y, Shi C, Liu Y, Shi X. Transcriptional Sequencing Uncovers Survival Mechanisms of Salmonella enterica Serovar Enteritidis in Antibacterial Egg White. ASM Journals. 2019;4(1):e00700-18. https://doi.org/10.1128/mSphere.00700-18
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15. Kouam MK, Biekop MH, Katte B, Teguia A. Salmonella status of table eggs in commercial layer farms in Menoua Division, West region of Cameroon. Food Control. 2018;85(1):345-349. https://doi.org/10.1016/j.foodcont.2017.09.037
16. Song J, Gao X, Galán JE. Structure and function of the Salmonella Typhi chimaeric A(2)B(5) typhoid toxin. Nature. 2013;499(7458):350-4. https://doi.org/10.1038/nature12377
17. Tajbakhsh M, Hendriksen RS, Nochi Z, Zali MR, Aarestrup FM, Garcia-Migura L. Antimicrobial resistance in Salmonella spp. recovered from patients admitted to six different hospitals in Tehran, Iran from 2007 to 2008. Folia Microbiol (Praha). 2012;57(2):91-7. https://doi.org/10.1007/s12223-012-0099-4
18. Cortés V, Sevilla-Navarro S, García C, Marín C, Catalá-Gregori P. Monitoring antimicrobial resistance trends in Salmonella spp. from poultry in Eastern Spain. Poult Sci. 2022;101(6):101832. https://doi.org/10.1016/j.psj.2022.101832
19. Siriken B, Al G, Erol I. Prevalence and Antibiotic Resistance of Salmonella Enteritidis and Salmonella Typhimurium in Ground Beef and Meatball Samples in Samsun, Turkey. Microb Drug Resist. 2020;26(2):136-144. https://doi.org/10.1089/mdr.2018.0481
20. Fardsanei F, Soltan Dallal MM, Douraghi M, Zahraei Salehi T, Mahmoodi M, Memariani H, Nikkhahi F. Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype Enteritidis isolated from meats and eggs. Microb Pathog. 2017;107(1):451-456. https://doi.org/10.1016/j.micpath.2017.04.026
21. Mąka Ł, Popowska M. Antimicrobial resistance of Salmonella spp. isolated from food. Rocz Panstw Zakl Hig. 2016;67(4):343-358. https://pubmed.ncbi.nlm.nih.gov/27922740/
22. Cortez AL, Carvalho AC, Ikuno AA, Bürger KP, Vidal-Martins AM. Identification of Salmonella spp. isolates from chicken abattoirs by multiplex-PCR. Research in veterinary science. 2006;81(3):340-344. https://doi.org/10.1016/j.rvsc.2006.03.006
23. van Hoek AH, Mevius D, Guerra B, Mullany P, Roberts AP, Aarts HJ. Acquired antibiotic resistance genes: an overview. Front Microbiol. 2011;2(1):203. https://doi.org/10.3389/fmicb.2011.00203
24. Trobos M, Christensen H, Sunde M, Nordentoft S, Agerso Y, Simonsen GS, Hammerum AM, Olsen JE. Characterization of sulphonamide-resistant Escherichia coli using comparison of sul2 gene sequences and multilocus sequence typing. Microbiology (Reading). 2009;155(Pt 3):831-836. https://doi.org/10.1099/mic.0.024190-0
25. Antunes P, Machado J, Sousa JC, Peixe L. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Chemother. 2005;49(2):836-9. https://doi.org/10.1128/AAC.49.2.836-839.2005
26. Quon DJ. Monitoring of domestic and imported eggs for veterinary drug residues by the Canadian Food Inspection Agency. J Agric Food Chem. 2000;48(12):6421-7. https://doi.org/10.1021/jf000144x
27. Pérez-Rodríguez M, Pellerano RG, Pezza L, Pezza HR. An overview of the main foodstuff sample preparation technologies for tetracycline residue determination. Talanta. 2018;182(1):1-21. https://doi.org/10.1016/j.talanta.2018.01
28. Sánchez-Salazar E, Gudiño ME, Sevillano G, Zurita J, Guerrero-López R, Jaramillo K, Calero-Cáceres W. Antibiotic resistance of Salmonella strains from layer poultry farms in central Ecuador. J Appl Microbiol. 2020;128(5):1347-1354. https://doi.org/10.1111/jam.14562
29. Xie T, Wu G, He X, Lai Z, Zhang H, Zhao J. Antimicrobial resistance and genetic diversity of Salmonella enterica from eggs. Food Sci Nutr. 2019;7(9):2847-2853. https://doi.org/10.1002/fsn3.1126
30. Li X, Liu L, Li Q, Xu G, Zheng J. Salmonella Contamination in Layer Farms in China: Detection and Genetic Analysis. J Poult Sci. 2018;55(1):1-9. https://doi.org/10.2141/jpsa.0160144
31. Denagamage T, Jayarao B, Patterson P, Wallner-Pendleton E, Kariyawasam S. Risk Factors Associated with Salmonella in Laying Hen Farms: Systematic Review of Observational Studies. Avian Dis. 2015;59(2):291-302. https://doi.org/10.1637/10997-120214-Reg
32. laboudi A, Basha EA, Musallam I. Chlortetracycline and sulfanilamide residues in table eggs: Prevalence, distribution between yolk and white and effect of refrigeration and heat treatment. Food control. 2013;33(1):281-286. https://doi.org/10.1016/j.foodcont.2013.03.014
33. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM; International Collaboration on Enteric Disease 'Burden of Illness' Studies. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50(6):882-9. https://doi.org/10.1086/650733
34. Sirdar MM, Picard J, Bisschop S, Jambalang AR, Gummow B. A survey of antimicrobial residues in table eggs in Khartoum State, Sudan, 2007-2008. Onderstepoort J Vet Res. 2012;79(1):1-9. https://doi.org/10.4102/ojvr.v79i1.360
35. Ehsani A, Hashemi M. Determination of Antibacterial Drug Residues in Commercial Eggs Distributed in Urmia, Iran. J. Food Qual. Hazards Control. 2015;2(2):61-65. http://jfqhc.ssu.ac.ir/article-1-147-en.html
36. Widiasih DA, Drastini Y, Yudhabuntara D, Maya FLRD, Sivalingham PL, Susetya H, et al. Detection of Antibiotic Residues in Chicken Meat and Eggs from Traditional Markets at Yogyakarta City Using Bioassay Method. Acta Vet Indones. 2019;7(4):1-6. https://doi.org/10.29244/avi.0.0.1-6
2. Tadesse G, Gebremedhin EZ. Prevalence of Salmonella in raw animal products in Ethiopia: a meta-analysis. BMC Res Notes. 2015;8(1):163-170. https://doi.org/10.1186/s13104-015-1127-7
3. Lee K. & Runyon M. & Herrman T. & Phillips RW. & Hsieh JJ. Review of Salmonella detection and identification methods: Aspects of rapid emergency response and food safety. Food Control. 2015;47(1):264-276. https://doi.org/10.1016/j.foodcont.2014.07.011
4. Li W, Li H, Zheng S, Wang Z, Sheng H, Shi C, Shi X, Niu Q, Yang B. Prevalence, Serotype, Antibiotic Susceptibility, and Genotype of Salmonella in Eggs from Poultry Farms and Marketplaces in Yangling, Shaanxi Province, China. Front Microbiol. 2020;11(1):1482-1496. https://doi.org/10.3389/fmicb.2020.01482
5. Ashtiani MT, Monajemzadeh M, Kashi L. Trends in antimicrobial resistance of fecal Shigella and Salmonella isolates in Tehran, Iran. Indian J Pathol Microbiol. 2009;52(1):52-5. https://doi.org/10.4103/0377-4929.44964
6. Sulieman AME, Dafallah FE, Abdel-Rahman EH, Alshammari NI, Shommo SA, Ibrahim SE. Isolation, Identification and Characterization of Salmonella spp. from Chicken purchased at Wad Madani City, Gezira State, Sudan. Advancements in Life Sciences. 2020;8(1):98-102. http://www.als-journal.com/8117-20/
7. Rodrigues GL, Panzenhagen P, Ferrari RG, Paschoalin VMF, Conte-Junior CA. Antimicrobial Resistance in Nontyphoidal Salmonella Isolates from Human and Swine Sources in Brazil: A Systematic Review of the Past Three Decades. Microb Drug Resist. 2020;26(10):1260-1270. https://doi.org/10.1089/mdr.2019.0475
8. Al-Abadi IK, Al-Mayah AA. Observations on the pathogenesis of orally inoculated Salmonella typhimurium in a newly hatched broiler chicks. Iraqi Poultry Sciences Journal. 2013;7(1):42-51. https://search.emarefa.net/detail/BIM-759007
9. Antunes P, Réu C, Sousa JC, Peixe L, Pestana N. Incidence of Salmonella from poultry products and their susceptibility to antimicrobial agents. Int J Food Microbiol. 2003;82(2):97-103. https://doi.org/10.1016/s0168-1605(02)00251-9
10. Cowen P, Currier RW, Steele JH. A Short History of One Health in the United States. Vet Herit. 2016;39(1):1-15. https://pubmed.ncbi.nlm.nih.gov/27344860/
11. Patchanee P, Eiamsam-Ang T, Vanaseang J, Boonkhot P, Tadee P. Determination of regional relationships among Salmonella spp. isolated from retail pork circulating in the Chiang Mai municipality area using a WGS data approach. Int J Food Microbiol. 2017;254(1):18-24. https://doi.org/10.1016/j.ijfoodmicro.2017.05.006
12. McWhorter AR, Chousalkar KK. From hatch to egg grading: monitoring of Salmonella shedding in free-range egg production systems. Vet Res. 2019;50(1):58-70. https://doi.org/10.1186/s13567-019-0677-4
13. Huang X, Zhou X, Jia B, Li N, Jia J, He M, He Y, Qin X, Cui Y, Shi C, Liu Y, Shi X. Transcriptional Sequencing Uncovers Survival Mechanisms of Salmonella enterica Serovar Enteritidis in Antibacterial Egg White. ASM Journals. 2019;4(1):e00700-18. https://doi.org/10.1128/mSphere.00700-18
14. Moffatt CRM, Musto J, Pingault N, Combs B, Miller M, Stafford R, Gregory J, Polkinghorne BG, Kirk MD. Recovery of Salmonella enterica from Australian Layer and Processing Environments Following Outbreaks Linked to Eggs. Foodborne Pathog Dis. 2017;14(8):478-482. https://doi.org/10.1089/fpd.2016.2268
15. Kouam MK, Biekop MH, Katte B, Teguia A. Salmonella status of table eggs in commercial layer farms in Menoua Division, West region of Cameroon. Food Control. 2018;85(1):345-349. https://doi.org/10.1016/j.foodcont.2017.09.037
16. Song J, Gao X, Galán JE. Structure and function of the Salmonella Typhi chimaeric A(2)B(5) typhoid toxin. Nature. 2013;499(7458):350-4. https://doi.org/10.1038/nature12377
17. Tajbakhsh M, Hendriksen RS, Nochi Z, Zali MR, Aarestrup FM, Garcia-Migura L. Antimicrobial resistance in Salmonella spp. recovered from patients admitted to six different hospitals in Tehran, Iran from 2007 to 2008. Folia Microbiol (Praha). 2012;57(2):91-7. https://doi.org/10.1007/s12223-012-0099-4
18. Cortés V, Sevilla-Navarro S, García C, Marín C, Catalá-Gregori P. Monitoring antimicrobial resistance trends in Salmonella spp. from poultry in Eastern Spain. Poult Sci. 2022;101(6):101832. https://doi.org/10.1016/j.psj.2022.101832
19. Siriken B, Al G, Erol I. Prevalence and Antibiotic Resistance of Salmonella Enteritidis and Salmonella Typhimurium in Ground Beef and Meatball Samples in Samsun, Turkey. Microb Drug Resist. 2020;26(2):136-144. https://doi.org/10.1089/mdr.2018.0481
20. Fardsanei F, Soltan Dallal MM, Douraghi M, Zahraei Salehi T, Mahmoodi M, Memariani H, Nikkhahi F. Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype Enteritidis isolated from meats and eggs. Microb Pathog. 2017;107(1):451-456. https://doi.org/10.1016/j.micpath.2017.04.026
21. Mąka Ł, Popowska M. Antimicrobial resistance of Salmonella spp. isolated from food. Rocz Panstw Zakl Hig. 2016;67(4):343-358. https://pubmed.ncbi.nlm.nih.gov/27922740/
22. Cortez AL, Carvalho AC, Ikuno AA, Bürger KP, Vidal-Martins AM. Identification of Salmonella spp. isolates from chicken abattoirs by multiplex-PCR. Research in veterinary science. 2006;81(3):340-344. https://doi.org/10.1016/j.rvsc.2006.03.006
23. van Hoek AH, Mevius D, Guerra B, Mullany P, Roberts AP, Aarts HJ. Acquired antibiotic resistance genes: an overview. Front Microbiol. 2011;2(1):203. https://doi.org/10.3389/fmicb.2011.00203
24. Trobos M, Christensen H, Sunde M, Nordentoft S, Agerso Y, Simonsen GS, Hammerum AM, Olsen JE. Characterization of sulphonamide-resistant Escherichia coli using comparison of sul2 gene sequences and multilocus sequence typing. Microbiology (Reading). 2009;155(Pt 3):831-836. https://doi.org/10.1099/mic.0.024190-0
25. Antunes P, Machado J, Sousa JC, Peixe L. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Chemother. 2005;49(2):836-9. https://doi.org/10.1128/AAC.49.2.836-839.2005
26. Quon DJ. Monitoring of domestic and imported eggs for veterinary drug residues by the Canadian Food Inspection Agency. J Agric Food Chem. 2000;48(12):6421-7. https://doi.org/10.1021/jf000144x
27. Pérez-Rodríguez M, Pellerano RG, Pezza L, Pezza HR. An overview of the main foodstuff sample preparation technologies for tetracycline residue determination. Talanta. 2018;182(1):1-21. https://doi.org/10.1016/j.talanta.2018.01
28. Sánchez-Salazar E, Gudiño ME, Sevillano G, Zurita J, Guerrero-López R, Jaramillo K, Calero-Cáceres W. Antibiotic resistance of Salmonella strains from layer poultry farms in central Ecuador. J Appl Microbiol. 2020;128(5):1347-1354. https://doi.org/10.1111/jam.14562
29. Xie T, Wu G, He X, Lai Z, Zhang H, Zhao J. Antimicrobial resistance and genetic diversity of Salmonella enterica from eggs. Food Sci Nutr. 2019;7(9):2847-2853. https://doi.org/10.1002/fsn3.1126
30. Li X, Liu L, Li Q, Xu G, Zheng J. Salmonella Contamination in Layer Farms in China: Detection and Genetic Analysis. J Poult Sci. 2018;55(1):1-9. https://doi.org/10.2141/jpsa.0160144
31. Denagamage T, Jayarao B, Patterson P, Wallner-Pendleton E, Kariyawasam S. Risk Factors Associated with Salmonella in Laying Hen Farms: Systematic Review of Observational Studies. Avian Dis. 2015;59(2):291-302. https://doi.org/10.1637/10997-120214-Reg
32. laboudi A, Basha EA, Musallam I. Chlortetracycline and sulfanilamide residues in table eggs: Prevalence, distribution between yolk and white and effect of refrigeration and heat treatment. Food control. 2013;33(1):281-286. https://doi.org/10.1016/j.foodcont.2013.03.014
33. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM; International Collaboration on Enteric Disease 'Burden of Illness' Studies. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50(6):882-9. https://doi.org/10.1086/650733
34. Sirdar MM, Picard J, Bisschop S, Jambalang AR, Gummow B. A survey of antimicrobial residues in table eggs in Khartoum State, Sudan, 2007-2008. Onderstepoort J Vet Res. 2012;79(1):1-9. https://doi.org/10.4102/ojvr.v79i1.360
35. Ehsani A, Hashemi M. Determination of Antibacterial Drug Residues in Commercial Eggs Distributed in Urmia, Iran. J. Food Qual. Hazards Control. 2015;2(2):61-65. http://jfqhc.ssu.ac.ir/article-1-147-en.html
36. Widiasih DA, Drastini Y, Yudhabuntara D, Maya FLRD, Sivalingham PL, Susetya H, et al. Detection of Antibiotic Residues in Chicken Meat and Eggs from Traditional Markets at Yogyakarta City Using Bioassay Method. Acta Vet Indones. 2019;7(4):1-6. https://doi.org/10.29244/avi.0.0.1-6
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