Kanatlı Etlerinde Salmonella typhimurium ve Salmonella enteritidis Varlığı ve Antibiyotik Dirençliliğinin Araştırılması

Öz

Kanatlı eti, yüksek besin içeriyle mikroorganizmaların gelişimi için mükemmel bir gıdadır. Çiftliklerde ve işleme birimlerinde uygun koşullarda işlense bile, Salmonella spp. gibi bazı patojen bakterilerle kontamine olabilir ve halk sağlığı açısından risk oluşturabilir. Salmonella enteritidis ve Salmonella typhimurium, gastroenterite neden olan baskın enfeksiyöz alt türlerdir. Kasım-Mayıs 2021 tarihleri arasında toplam 160 adet ambalajlı veya ambalajsız çiğ kanatlı eti örneği (53 kanat, 53 derisiz göğüs ve 54 but) toplanmıştır. İzole edilen Salmonella enteritidis ve Salmonella typhimurium suşlarının yaygınlığı ve antibiyotik direnci araştırılmıştır. Toplamda 43 izolat Salmonella spp. olarak tanımlanmış; bunların 23’ü kanat, 12’si derisiz göğüs ve 8’i but örneklerinden elde edilmiştir. Toplam örneklerin %26,9’u; kanatların %43,4’ü, derisiz göğüslerin %22,6’sı ve butların %14,8’i Salmonella enteritidis ve/veya Salmonella typhimurium ile kontaminasyon tespit edilmiştir. Bazı antibiyotiklere karşı gözlemlenen yüksek antibiyotik direnç profilleri halk sağlığı açısından bir sorun olarak değerlendirilmiştir. Sonuç olarak, kanatlı etinin Salmonella enteritidis ve Salmonella typhimurium ile kontamine olduğu ve bu kontaminasyonu azaltabilmek için çiftlik düzeyinde önlem alınması ve kesimhanelerde gıda kalite güvence sistemlerinin uygulanması gerektiği sonucuna varılmıştır.

Anahtar Kelimeler

• Antibiyotik direnci
• kanatlı eti
• Salmonella enteritidis
• Salmonella typhimurium
• toplum sağlığı

Investigation of the Presence and Antibiotic Resistance of Salmonella Typhimurium and Salmonella Enteritidis in Poultry Meat

Öz

Poultry meat is an excellent foodstuff for the growth of microorganisms due to its high nutritional content. Even handled under appropriate conditions, both in the farms and processing units, it may be contaminated by some pathogenic bacteria such as Salmonella spp. and create public health risks. Salmonella enteritidis and Salmonella typhimurium are the infective predominant subspecies causing gastroenteritis. A total of 160 packaged or unpackaged raw poultry meat samples (53 wings, 53 skinless breasts and 54 legs) were collected between November and May 2021. The prevalence and antibiotic resistance of Salmonella enteritidis and Salmonella typhimurium isolates isolated were investigated. 43 isolates were identified as Salmonella spp., 23 of which were from wings, 12 were from skinless breasts and 8 were from legs. 26.9% of total samples, 43.4% of wings, 22.6% of skinless breasts and 14.8% of legs were contaminated with Salmonella enteritidis and/or Salmonella typhimurium. High antibiotic resistance patterns observed against to some antibiotics tested were considered as a public health problem. It was concluded that poultry meat was contaminated with Salmonella enteritidis and Salmonella typhimurium and to be able to reduce contamination, it is necessary to take precautions at farm level and apply food quality assurance systems at slaughterhouse.

Anahtar Kelimeler

• Antibiotic Resistance
• Poultry Meat
• Public Health
• Salmonella enteritidis
• Salmonella typhimurium

Kaynakça

1. Acar, S. (2015). Phenotypic and genetic characterization of antimicrobial resistance in Salmonella isolates from different sources in Türkiye [Doctoral dissertation, Middle East Technical University]. METU Theses Archive. https://hdl.handle.net/11511/24633
2. Akil, L., & Ahmad, H.A. (2019). Quantitative Risk Assessment Model of Human Salmonellosis Resulting from Consumption of Broiler Chicken. Diseases 7, 19. https://doi.org/10.3390/diseases7010019
3. Alali W.Q., Gaydashov R., Petrova E., Panin A., Tugarinov O., Kulikovskii A.,…& Doyle M.P. (2012). Prevalence of Salmonella on retail chicken meat in Russian Federation. Journal of Food Protection, 75, 1469-1473. https://doi.org/10.4315/0362-028X.JFP-12-080
4. Altın Gaser, B. (2024). Kanatlı etlerinde Salmonella Typhimurium ve Salmonella Enteritidis varlığı ve antibiyotik dirençliliğinin araştırılması [Doctoral dissertation, Aydın Adnan Menderes University]. Council of Higher Education Thesis Center (YÖK Tez Merkezi). https://tez.yok.gov.tr/UlusalTezMerkezi
5. Alvarez, J., Sota, M., Vivanco, A. B., Perales, I., Cisterna, R., Rementeria, A., & Garaizar, J. (2004). Development of a multiplex PCR technique for detection and epidemiological typing of Salmonella in human clinical samples. Journal of Clinical Microbiology, 42(4), 1734-1738. https://doi.org/10.1128/jcm.42.4.1734-1738.2004
6. Antunes, P., Mourão, J., Campos, J., & Peixe, L. (2016). Salmonellosis: The role of poultry meat. Clinical Microbiology and Infection, 22(2), 110–121. https://doi.org/10.1016/j.cmi.2015.12.004
7. Asal Ulus, C. (2019). Determination of Salmonella serotypes in organic chicken meat and antibiotic resistance profile of serotypes [Doctoral dissertation, Ondokuz Mayıs University, Institute of Health Sciences]. Council of Higher Education Thesis Center (YÖK Tez Merkezi). https://tez.yok.gov.tr/UlusalTezMerkezi/
8. Atabey C., Kahraman T., & Koluman A. (2021). Prevalence and Antibiotic Resistance of Salmonella sp., E. coli O157, and L. monocytogenes in Meat and Dairy Products. Animal Health Production and Hygiene, 10 (1), 17 – 22.

9. Babacan O., & Karadeniz H. (2019). Çiğ Tavuk Etlerinden İzole Edilen Salmonella spp. Suşlarının Antibiyotik Duyarlılıklarının Araştırılması. Veteriner Hekimler Derneği Dergisi, 90(2), 105-114. https://doi.org/10.33188/vetheder.497569
10. Batz M.B., Hoffmann S., & Morris Jr J.G. (2012). Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. Journal of Food Protection. 7, 1278 –1291. https://doi.org/10.4315/0362-028X.JFP-11-418
11. Borges, K. A., Furian, T. Q., Souza, S. N., Salle, C. T. P., Moraes, H. L. S., & Nascimento, V. P. (2019). Antimicrobial resistance and molecular characterization of Salmonella enterica serotypes isolated from poultry sources in Brazil. Brazilian Journal of Poultry Science, 21(1), 1–8. https://doi.org/10.1590/1806-9061-2018-0827
12. Bozkurt, B. (2018). Çiğ ve yarı-pişmiş bazı et ürünlerinde Salmonella spp. ve Staphylococcus aureus’un belirlenmesi ve antibiyotik dirençliliklerinin araştırılması [Master’s thesis, Balıkesir University, Institute of Science]. Council of Higher Education Thesis Center (YÖK Tez Merkezi).https://tez.yok.gov.tr/UlusalTezMerkezi/
13. Capita, R., Álvarez-Astorga, M., Alonso-Calleja, C., Moreno, B., & del Camino Garcıá -Fernández, M. (2003). Occurrence of salmonellae in retail chicken carcasses and their products in Spain. International Journal of Food Microbiology, 81(2), 169-173. https://doi.org/10.1016/S0168-1605(02)00195-2
14. Castro-Vargas, R.E., Herrera-Sánchez, M.P., Rodríguez-Hernández, R., & Rondón-Barragán, I.S. (2020). Antibiotic resistance in Salmonella spp. isolated from poultry: A global overview. Veterinary World, 13(10), 2070–2084. https://doi.org/10.14202/vetworld.2020.2070-2084
15. CDC (Centers for Disease Control and Prevention) (2024a). Outbreaks of Salmonella. National Outbreak Reporting System (Nors) dashboard https://www.cdc.gov/nors/about/index.html Last access 01.04.2024 CDC (Centers for Disease Control and Prevention) (2024b). Salmonella infection. https://www.cdc.gov/salmonella/index.html Last access 09.05.2024
16. Chagas, F.F., Crispim, B.A., Oliveira, K.M.P., & Grisolia, A.B. (2013). Identification and detection of Salmonella strains isolated from chicken carcasses and environmental sources in Dourados, MS, Brasil. African Journal of Microbiology Research, 7, 3222-3228. https://doi.org/10.5897/AJMR12.830.
17. Chai S. J., Cole, D., Nisler, A., & Mahon, B. E. (2017). Poultry: the most common food in outbreaks with known pathogens, United States, 1998–2012. Epidemiology and Infection,145, 316–325. https://doi.org/10.1017/S0950268816002375
18. Chaomuang, N., Flick, D., Denis, A., & Laguerre, O. (2019). Experimental analysis of heat transfer and airflow in a closed refrigerated display cabinet. Journal of Food Engineering, 244, 101-114. https://doi.org/10.1016/j.jfoodeng.2018.09.009
19. Cherubin, C. E. (1981). Antibiotic resistance of Salmonella in Europe and the United States. Reviews of Infectious Diseases, 3(6), 1105–1126. https://doi.org/10.1093/clinids/3.6.1105
20. Cufaoglu, G., Ambarcıoglu, P., Derinöz, A.N., & Ayaz, N.D. (2023). Prevalence, Serotype Diversity and Antibiotic Resistance of Salmonella Among Poultry Meat and Eggs in Türkiye: A Metaanalysis. Journal of Agricultural Sciences, 29(2),519-533. https://doi.org/10.15832/ankutbd.1108594
21. Dong, S., Li, L., Hao, F., Fang, Z., Zhong, R., Wu, J. & Fang, X. (2024). Improving quality of poultry and its meat products with probiotics, prebiotics, and phytoextracts. Poultry Science, 103,103287. https://doi.org/10.1016/j.psj.2023.103287
22. Dümen, E., Aydın, A., & Issa, G. (2015). Prevalence, Serological Typing and PCR Sensitivity Comparision of Salmonella Typhimurium, Salmonella Enteritidis and Salmonella spp. Isolated from Raw Chicken Carcasses. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 21(5), 653-658. https://doi.org/10.9775/kvfd.2015.12972
23. EFSA & ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). (2023). The European Union One Health 2022 Zoonoses Report. EFSA Journal, 21(12), e8442. https://doi.org/10.2903/j.efsa.2023.8442
24. Ehuwa, O., Jaiswal, A.K., & Jaiswal, S. (2021). Salmonella, Food Safety and Food Handling Practices. Foods. 10, 907. https://doi.org/10.3390/foods10050907
25. European Committee on Antimicrobial Susceptibility Testing [EUCAST] (2020). Antimicrobial Susceptibility Testing EUCAST Disk Diffusion Method, 2020, https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_10.0_Breakpoint_Tables.pdf. Last acces 18.06.202
26. Galán-Relaño, Á., Valero Díaz, A., Huerta Lorenzo, B., Gómez-Gascón, L., Mena Rodríguez, M.Á., Carrasco Jiménez, E., … & Astorga Márquez, R.J. (2023). Salmonella and Salmonellosis: An Update on Public Health Implications and Control Strategies. Animals. 13, 3666. https://doi.org/10.3390/ani13233666
27. Goluch, Z., Słupczynska, M., Okruszek, A., Haraf, G., Werenska, M., & Wołoszyn, J. (2023). The Energy and Nutritional Value of Meat of Broiler Chickens Fed with various Addition of wheat germ expeller. Animals, 13, 499. https://doi.org/10.3390/ani13030499
28. Gomes, V.T.M., Moreno, L.Z., Silva, A.P.S., Thakur, S., LA Ragione, R.M., … & Moreno, A.M. (2022). Characterization of Salmonella enterica Contamination in Pork and Poultry Meat from São Paulo/ Brazil: Serotypes, Genotypes and Antimicrobial Resistance Profiles. Pathogens, 11, 358. https://doi.org/10.3390/pathogens11030358
29. Goncagül, G., Günaydın, E., & Carlı, K.T. (2005). Prevalence of Salmonella Serogroups in Chicken Meat. Turkish Journal of Veterinary & Animal Sciences, 29,103-106.
30. Guo, C., Hoekstra, R.M., Schroeder, C.M., Pires, S.M., Ong, K.L., Hartnett, E., … & Cole, D. (2011). Application of Bayesian techniques to model the burden of human salmonellosis attributable to U.S. food commodities at the point of processing: adaptation of a Danish model. Foodborne Pathogens and Disease. 8, 509–516. https://doi.org/10.1089/fpd.2010.0714
31. IFSAC (The Interagency Food Safety Analytics Collaboration). (2020). Foodborne Illness Source Attribution Estimates for 2015 for Salmonella, Escherichia coli 0157, Listeria monocytogenes, and Campylobacter Using Multi-Year Outbreak Surveillance Data (United States). The Interagency Food Safety Analytics Collaboration (IFSAC) December 2020. https://www.cdc.gov/ifsac/media/pdfs/ P19-2020-report-TriAgency-508.pdf Last access 14.11.2024.
32. IFSAC (The Interagency Food Safety Analytics Collaboration). (2021). Foodborne illness source attribution estimates for 2019 for Salmonella, Escherichia coli O157, Listeria monocytogenes, and Campylobacter using multi-year outbreak surveillance data, United States. PP7. October 2021. https://www.cdc.gov/ifsac/media/pdfs/P19-2019-report-TriAgency-508.pdf Last access 01.04.2024.
33. Inbaraj, S., Agrawal, R.K., Thomas, P., Mohan, C., Agarwal, S., Verma, M.R., & Chaudhuri, P. (2022). Antimicrobial Resistance in Indian Isolates of NonTyphoidal Salmonella of Livestock, Poultry and Environmental Origin From 1990 to 2017. Comparative Immunology, Microbiology and Infectious Diseases, 80. https://doi.org/10.1016/j.cimid.2021.101719
34. International Standardization Organization [ISO]. (2017). Microbiology of the food chain — Horizontal Method For The Detection, Enumeration and Serotyping of Salmonella. 6579-I, Switzerland.
35. Kasımoğlu Doğru, A., Ayaz, A.D., & Gencay, Y.E. (2010). Serotype identification and antimicrobial resistance profiles of Salmonella spp. isolated from chicken carcasses. Tropical Animal Health and Production, 42, 893-897. https://doi.org/10.1007/s11250-009-9504-7
36. Khan, A.S., Georges, K., Rahaman, S., Abdela, W., & Adesiyun, A.A. (2018). Prevalence and serotypes of Salmonella spp. on chickens sold at retail outlets in Trinidad. PLoS ONE. 13, e0202108. https://doi.org/10.1371/journal.pone.0202108
37. Kozacinski, L., Cvrtila Fleck, Ž., Kozacinski, Z., Filipovic, I., Mitak, M., Bratulic, M., & Mikuš, T. (2012). Evaluation of shelf life of prepacked cut poultry meat. Veterinarski arhiv, 82, 47-58.
38. Küçük, B. (2020). Tavuk orijinli Salmonella Enteritidis suşlarında siprofloksasin direncinin araştırılması [Master’s thesis, Ankara University, Institute of Health Sciences]. Council of Higher Education Thesis Center (YÖK Tez Merkezi). https://tez.yok.gov.tr/UlusalTezMerkezi/
39. Lin, C.K., & Tsen, H.Y. (1996). Use of two 16S DNA targeted oligonucleotides as PCR primers for the specific detection of Salmonella in foods Journal of Applied Bacteriology, 80(6), 659-66. https://doi.org/10.1111/j.1365-2672.1996.tb03271.x
40. Oludairo, O.O, Kwaga, J.K.P., Dzilwi, A.A., & Kabir J. (2013). The genus Salmonella, isolation and occurrence in wildlife. International Journal of Microbiology and Immunology Research, 1, 047-052.
41. Pavelquesi, S.L.S., Ferreira, A.C.A.O., Rodrigues, L.F.S., de Souza Silva, M.C., da Silva, I.C.R., & Orsi, D.C. (2023). Prevalence and Antimicrobial Resistance of Salmonella spp. Isolated From Chilled Chicken Meat Commercialized at Retail in Federal District, Brazil. Journal of Food Protection, 86, 100130. https://doi.org/10.1016/j.jfp.2023.100130
42. Perin, A.P., Martins, B.T.F., Barreiros, M.A.B., Yamatogi R.S., Nero L.A., & Bersot L.D.S. (2020). Occurrence, quantification, pulse types, and antimicrobial susceptibility of Salmonella sp. isolated from chicken meat in the state of Paraná, Brazil. Brazilian Journal of Microbiology, 51, 335–345. https://doi.org/10.1007/s42770-019-00188-x
43. Plummer, R.A.S., Blissett, S.J., & Dodd, C.E.R. (1995). Salmonella contamination of retail chicken products sold in the UK. Journal of Food Protection, 58, 843-846. https://doi.org/10.4315/0362-028X-58.8.843
44. Qin, X., Yang, M., Cai, H., Liu, Y., Gorris, L., Aslam, M. Z., … & Dong, Q. (2022). Antibiotic Resistance of Salmonella Typhimurium Monophasic Variant 1,4,[5],12:i:-in China: A Systematic Review and Meta-Analysis. Antibiotics, 11, 532. https://doi.org/10.3390/antibiotics11040532
45. Ravindran, V. (2013). Poultry Feed Availability and Nutrition in Developing Countries. Poultry Development Review, 2, 60–63.https://www.fao.org/4/al703e/al703e00.pdf
46. Reardon, S. (2014). Antibiotic resistance sweeping developing world: Bacteria are increasingly dodging extermination as drug availability outpaces regulation. Nature, 509(7499), 141–143. https://doi.org/10.1038/509141a
47. Regalado-Pineda, I.D., Rodarte-Medina, R., Resendiz-Nava, C.N., Saenz-Garcia, C.E., Castañeda-Serrano, P., & Nava, G.M. (2020). Three Year Longitudinal Study: Prevalence of Salmonella enterica in Chicken Meat is Higher in Supermarkets than Wet Markets from Mexico. Foods, 9, 264. https://doi.org/10.3390/foods9030264
48. Rortana, C., Nguyen-Viet, H., Tum, S., Unger, F., Boqvist, S., Dang-Xuan, S., ... & Lindahl, J. F. (2021). Prevalence of Salmonella spp. and Staphylococcus aureus in chicken meat and pork from Cambodian markets. Pathogens, 10(5), 556. https://doi.org/10.3390/pathogens10050556
49. Salehi, Z.T., Mahzonieh, M., & Saeedzadeh, A. (2005). The isolation of antibiotic resistant Salmonella from intestine and liver of poultry in Shiraz province of Iran. International Journal of Poultry Science, 4(5), 320-322. https://doi.org/10.3923/ijps.2005.320.322
50. Scheinberg, J., Doores, S., & Cutter, C.N. (2013). A Microbiological Comparison of Poultry Products Obtained from Farmers’ Markets and Supermarkets in Pennsylvania. Journal of Food Safety, 33, 259–264. https://doi.org/10.1111/jfs.12047
51. Seif, Y., Kavvas, E., Lachance, J.C., Yurkovich, J.T., Nuccio, S.P., Fang, X.,… & Monk, J.M. (2018). Genome-scale metabolic reconstructions of multiple Salmonella strains reveal serovar-specific metabolic traits. Nature Communications, 9, 3771. https://doi.org/10.1038/s41467-018-06112-5
52. Sepin, Ö. (2020). Afyonkarahisar’da satışa sunulan tavuk iç organlarından Salmonella spp. ve Listeria monocytogenes’in immonomagnetik seperasyon yöntemiyle izolasyonu ve izolatların antibiyotik dirençliliğinin belirlenmesi [Doctoral dissertation, Afyon Kocatepe University, Institute of Health Sciences]. Council of Higher Education Thesis Center (YÖK Tez Merkezi). https://tez.yok.gov.tr/UlusalTezMerkezi/
53. Shahdadi, M., Safarirad, M., Berizi, E., Mazloomi, S.M., Hosseinzadeh, S., Zare, M., … & Rajabi, S. (2023). A systematic review and modeling of the effect of bacteriophages on Salmonella spp. Reduction in chicken meat. Heliyon 9, e14870. https://doi.org/10.1016/j.heliyon.2023.e14870
54. Telsaç, R., & Tuncay RM (2022). Prevalence and antibiotic resistance profiles of Salmonella spp. in chicken meat. Turkish Journal of Veterinary & Animal Sciences, 46, 708-717, https://doi.org/10.55730/1300-0128.4245
55. Thames, H.T., & Sukumaran, A.T. (2020). A Review of Salmonella and Campylobacter in Broiler Meat: Emerging Challenges and Food Safety Measures. Foods, 9, 776, https://doi.org/10.3390/foods9060776
56. Turkish Food Codex (2025). Turkish Food Codex Microbiological Criteria Regulation. Official Gazette of the Republic of Türkiye, No. 32812, Ankara. Retrieved February 13, 2025, from https://www.resmigazete.gov.tr/eskiler/2025/02/20250213-2.htm
57. Uyttendaele, M.R., Debevere, J.M., Lips, R.M., & Neyts, K.D. (1998). Prevalence of Salmonella in poultry carcasses and their products in Belgium. International Journal of Food Microbiology, 40, 1-8. https://doi.org/10.1016/S0168-1605(98)00012-9
58. Yang, B., Xi, M., Wang, X., Cui, S., Yue, T., Hao, H., … & Doyle, M.P. (2011). Prevalence of Salmonella on raw poultry at retail markets in China. Journal of Food Protection, 74, 1724-1728. https://doi.org/10.4315/0362-028X.JFP-11-215
59. Zahli, R., Scheu, A.K., Abrini, J., Copa-Patino, J.L., Naida, A., … & Soliveri, J. (2022). Salmonella Spp: Prevalence, Antimicrobial Resistance and Molecular Typing of Strains Isolated From Poultry in Tetouan-Morocco. Food Science and Technology, 153. https://doi.org/10.1016/j.lwt.2021.112359