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Çanakkale, Türkiye’de Perakende Tavuk Etlerinde Salmonella spp.’nin Yaygınlığı, Virülans Özellikleri ve Antimikrobiyal Duyarlılığı

Year 2025, Volume: 8 Issue: 2, 71 - 78, 29.12.2025
https://doi.org/10.46239/ejbcs.1804245

Abstract

Bu çalışmada, Türkiye’nin Çanakkale ilinde perakende olarak satılan çiğ tavuk etlerinin mikrobiyolojik kalitesi, Salmonella spp. varlığı, bu izolatların virülans özellikleri ve antibiyotiklere duyarlılık profilleri araştırılmıştır. Kasım 2022 ile Nisan 2023 tarihleri arasında 90 tavuk eti örneği (30 göğüs, 30 kanat, 30 but) toplanmıştır. Genel hijyen indikatör mikroorganizmalar (Toplam Aerobik Mezofilik Bakteri -, Toplam Aerobik Psikrofilik Bakteri -, maya-küf, Toplam Koliform - TK, Fekal Koliform - ve Fekal Enterokok -) kabul edilebilir sınırlar içinde yer alsa da, yüksek sayıları üretim aşamalarındaki sanitasyon eksikliklerine işaret etmektedir. Toplam 10 adet Salmonella spp. izolatı tanımlanmış olup, bunların %80’i S. arizonae serotipindedir. Bu izolatlar yüksek düzeyde DNaz (%90) ve proteaz (%90) aktivitesi göstermiş, güçlü biyofilm oluşturma kapasitesine sahip oldukları belirlenmiştir (%40 mükemmel, %30 çok iyi, %30 iyi). Ayrıca önemli düzeyde antibiyotik direnci sergilemişlerdir. Tüm izolatların Çoklu İlaç Direnci indeksi 0,2’nin üzerinde olup, bu durum kanatlı üretiminde yoğun antibiyotik kullanımını düşündürmektedir. Elde edilen bulgular, virülans özellikleri yüksek ve antibiyotiklere dirençli Salmonella suşlarının yayılımı açısından tavuk eti üretim ve tüketim süreçlerinin halk sağlığı için ciddi riskler taşıdığını göstermektedir.

Ethical Statement

Bu çalışma etik kurul onayından muaftır.

Supporting Institution

Çanakkale Onsekiz Mart Üniversitesi- This study is part of Ebru BAŞARAN’s Master's thesis research. This work was supported by the Çanakkale Onsekiz Mart University Scientific Research Projects Coordination Unit (Project No: FYL-2022-4214).

Project Number

FYL-2022-4214

References

  • Akgül Ö, Gülhan T, Güdücüoğlu H. 2016. Phenotypic and genotypic analysis of antibiotic resistance in Enterococcus species isolated from chicken and gull sources. J Fac Vet Med. 63: 235 244. doi.org/ 10.1501/vetfak_0000002735
  • Aksoy D. 2019. Determination of in vitro biofilm formation abilities of food borne Salmonella enterica isolates. Trak Univ J Nat Sci. 20(1): 57 62. doi.org/10.23902/trkjnat.471236
  • Al-Qadiri H, Al-Holy A, Al-Abdallat M, Olaimat A, Saleh M, Ghalib Bakri F, Abutarbush S, Rasco B. 2025. Antimicrobial resistance of Salmonella spp. recovered from raw chicken meat at abattoirs and retail markets in Jordan. Ital J Food Sci. 37(2): 216-227. doi.org/10.15586/ijfs.v37i2.2898.
  • Anonymous. 2003. ISO 4833. Microbiology of food and animal feeding stuffs. Horizontal method for the enumeration of microorganisms. Colony count technique at 30 degrees C. Geneva, Switzerland: International Organization for Standardization, 2003.
  • Anonymous. 2006. ISO 4831. Microbiology of food food and animal feeding stuffs ‐‐ Horizontal method for the enumaration of coliforms ‐ Colony‐count technique. Geneva, Switzerland: International Organization for Standardization.
  • Anonymous. 2008. ISO 21527‐1 Microbiology of food and animal feeding stuffs. Horizontal m ethod for the enumeration of yeasts and moulds. Part 1: Colony count technique in products with water activity greater than 0,95. Geneva, Switzerland: International Organization for Standardization, 2008.
  • Anonymous. 2017. ISO 6579-1:2017. Microbiology of the food chain — Horizontal method for the detection, enumeration and serotyping of Salmonella — Part 1: Detection of Salmonella spp. International Organization for Standardization, Geneva, Switzerland.
  • Augustyńska-Prejsnar A, Kačániová M, Hanus P, Sokołowicz Z, Słowiński M. 2024. Microbial and sensory quality changes in broiler chicken breast meat during refrigerated storage. Foods. 13(24): 4063. doi.org/10.3390/foods13244063.
  • Bauer AW. 1966. Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45, 493-496.
  • Bhunia AK. 2018. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis. Springer.
  • CDC 2022. Salmonella. Centers for Disease Control and Prevention. https://www.cdc.gov/salmonella/index.html
  • CLSI 2009. Clinical and Laboratory Standarts Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard-Seventh Edition. M07- A7, Villanova, PA, USA.
  • Çiftçi A, Güran HŞ. 2019. Evaluation of microbial contamination and shelf life of packaged chicken meat. J Food Sci Tech. 56(5): 2341–2347. doi.org/10.1007/s13197-019-03752-8
  • Çufaoğlu G, Ambarcıoğlu P, Derinöz AN, Ayaz ND. 2023. Prevalence, serotype diversity and antibiotic resistance of Salmonella among poultry meat and eggs in Türkiye: A Meta-analysis. J Agric Sci, 29(2): 519-533. doi.org/10.15832/ankutbd.1108594
  • Dışhan A, Hızlısoy H, Ertaş Onmaz N, Yıldırım Y, Gönülalan Z, Al S. 2024. Comprehensive analysis of Salmonella in poultry meat and products in Türkiye: Prevalence, antibiotic susceptibility and genomic characterisation. Int J Food Sci Technol. 59(5): 3412-3422. doi.org/10.1111/ijfs.17097
  • EFSA. 2021. The European Union One Health 2020 Zoonoses Report. EFSA J., 19(12): e06971.
  • Elbayoumi Z, Ibrahim G, Zayda M, Shawish R. 2023. Prevalence and molecular characterization of Salmonella spp. in poultry meat and its products. J Curr Vet Res. 5(2): 1-9. doi: 10.21608/jcvr.2023.320405. FAO/WHO. 2019. Food Safety and Quality. Food and Agriculture Organization of the United Nations & World Health Organization.
  • Halkman K (ed). 2005. Merck Gıda Mikrobiyolojisi Uygulamaları. Ed. AK Halkman. Başak Matbaacılık Ltd. Şti., Ankara, 358 s.
  • Krumperman P. 1983. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol, 46: 165-170.
  • Kundakçı A, Yücel A, Uylaşer V, Konca R, Can S. 1991. Microflora and quality of chicken meat stored under cold conditions and offered for sale. In Proceedings of the 2nd International Food Symposium, Bursa, pp. 191–200.
  • Rivera D, Allel K, Dueñas F, Tardone R, Soza P, Hamilton-West C, Moreno-Switt AI. 2021. Screening the presence of non-typhoidal Salmonella in different animal systems and the assessment of antimicrobial resistance. Animals 11(6): 1532. doi.org/10.3390/ ani11061532.
  • Sağun E, Sancak YC, Ekici K, Durmaz H. 1996. A study on the hygenic quality of chicken breast and thigh consumed in Van.. Van Vet J. 7(1-2): 62-66.
  • Sharma V, Singh M. 2023. Bacteriological quality of poultry meat from local markets of Jammu city. Indian J Anim Health. 62(2): 182–188. doi.org/10.36062/ijah.2023.15322.
  • Singh DV. Sanyal SC. 1992. Haemolysin and enterotoxin production by Aeromonas caviae isolated from diarrhoeal patients. Fish Environ J Diarrhoeal Dis Res. 10(1): 16-20.
  • Sokol PA, Ohman DE. Iglewski BH. 1979. A more sensitive plate assay for detection of protease production by Pseudomonas aeruginosa. J Clinic Microbiol. 9: 538-540.
  • Sonkar A, Rathi MN, Gole VC. 2018. Biofilm-forming ability of foodborne pathogens and their resistance to sanitizers in meat processing environments. J Food Saf, 38(6): e12559.
  • Şahin S, Kalın R, Arslanbaş E. Moğulkoç MN. 2017. Satışa sunulan tavuk etlerinde bazı bakteri ve indikatör mikroorganizmaların belirlenmesi. Manas J Agr Vet Life Sci. 7 (1): 47‐56.
  • Tamer AÜ, Uçar F, Ünver E, Karaboz İ, Bursalıoğlu M. Oğultekin (Eltem) R. 1989. 3. ve 4.Sınıf Mikrobiyoloji laboratuvar kılavuzu”. T.C. Anadolu Üniv. Eğitim, Sağlık ve Bilimsel Araş. Çalışmal. Vakfı Yayın., No:74, Eskişehir.
  • Telli R. 2006. Afyon’da tütketime sunulan tavuk karkas ve tavuk Eti örneklerinde Salmonella spp. varlığının klasik kültür tekniği ile saptanması, Yüksek Lisans Tezi, Afyon Kocatepe Üniversitesi, Sağlık Bilimleri Enstitüsü, Afyonkarahisar.
  • Turkish Statistical Institute (TÜİK). 2022. Poultry and egg production and sales [Data set]. Turkish Statistical Institute. https://data.tuik.gov.tr/ [Accessed October 15, 2025]
  • Van Boeckel T.P, Brower C, Gilbert M. 2015. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci. 112(18): 5649–5654.
  • Wang X, Wang H, Li T. 2013. Modeling and predicting the biofilm formation of different Salmonella strains. J Food Safe. 33(4): 503–508. doi.org/10.1111/jfs.12082.
  • WHO. 2020. Food Safety. World Health Organization. https://www.who.int/news-room/fact-sheets/detail/food-safety
  • Yanık HD, Müştak HK, Sarıçam İnce S. 2025. Effects of environmental and genetic factors on biofilm formation of various Salmonella serotypes. Turk J Vet Anim Sci. 49(2): 70–75. doi.org/10.55730/1300-0128.4372
  • Yıldırım M, Ünlü A, Yıldırım Z. 2015. Microbiological quality of retail chicken meat in Turkey. J Food Safe. 35(2): 123–130. doi.org/10.1111/jfs.12145.

Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye

Year 2025, Volume: 8 Issue: 2, 71 - 78, 29.12.2025
https://doi.org/10.46239/ejbcs.1804245

Abstract

This study investigated the microbiological quality of raw chicken meats retailed in Çanakkale province, Türkiye, focusing on the presence of Salmonella spp., their virulence properties, and antibiotic susceptibility profiles. A total of 90 chicken meat samples (30 breast, 30 wing, 30 thigh) were collected between November 2022 and April 2023. While general hygiene indicator microorganisms (Total Aerobic Mesophilic Bacteria, Total Aerobic Psychrophilic Bacteria, yeast-mold, total coliform, fecal coliform, and fecal enterococci) were within acceptable limits, their high counts indicated sanitation issues during production stages. Ten Salmonella spp. isolates were identified, with 80% being S. arizonae serotype. These isolates demonstrated significant virulence, exhibiting high DNase (90%) and protease (90%) activities, strong biofilm-forming capacities (40% excellent, 30% very good, 30% good), and notable antibiotic resistance profiles. All isolates showed a Multi-Drug Resistance index greater than 0.2, suggesting intensive antibiotic use in poultry production. These findings highlight significant public health risks associated with chicken meat production and consumption processes, particularly concerning the spread of virulent and antibiotic-resistant Salmonella strains.

Ethical Statement

This study is exempt from ethical committee approval.

Supporting Institution

Çanakkale Onsekiz Mart University This study is part of Ebru BAŞARAN’s Master's thesis research. This work was supported by the Çanakkale Onsekiz Mart University Scientific Research Projects Coordination Unit (Project No: FYL-2022-4214).

Project Number

FYL-2022-4214

References

  • Akgül Ö, Gülhan T, Güdücüoğlu H. 2016. Phenotypic and genotypic analysis of antibiotic resistance in Enterococcus species isolated from chicken and gull sources. J Fac Vet Med. 63: 235 244. doi.org/ 10.1501/vetfak_0000002735
  • Aksoy D. 2019. Determination of in vitro biofilm formation abilities of food borne Salmonella enterica isolates. Trak Univ J Nat Sci. 20(1): 57 62. doi.org/10.23902/trkjnat.471236
  • Al-Qadiri H, Al-Holy A, Al-Abdallat M, Olaimat A, Saleh M, Ghalib Bakri F, Abutarbush S, Rasco B. 2025. Antimicrobial resistance of Salmonella spp. recovered from raw chicken meat at abattoirs and retail markets in Jordan. Ital J Food Sci. 37(2): 216-227. doi.org/10.15586/ijfs.v37i2.2898.
  • Anonymous. 2003. ISO 4833. Microbiology of food and animal feeding stuffs. Horizontal method for the enumeration of microorganisms. Colony count technique at 30 degrees C. Geneva, Switzerland: International Organization for Standardization, 2003.
  • Anonymous. 2006. ISO 4831. Microbiology of food food and animal feeding stuffs ‐‐ Horizontal method for the enumaration of coliforms ‐ Colony‐count technique. Geneva, Switzerland: International Organization for Standardization.
  • Anonymous. 2008. ISO 21527‐1 Microbiology of food and animal feeding stuffs. Horizontal m ethod for the enumeration of yeasts and moulds. Part 1: Colony count technique in products with water activity greater than 0,95. Geneva, Switzerland: International Organization for Standardization, 2008.
  • Anonymous. 2017. ISO 6579-1:2017. Microbiology of the food chain — Horizontal method for the detection, enumeration and serotyping of Salmonella — Part 1: Detection of Salmonella spp. International Organization for Standardization, Geneva, Switzerland.
  • Augustyńska-Prejsnar A, Kačániová M, Hanus P, Sokołowicz Z, Słowiński M. 2024. Microbial and sensory quality changes in broiler chicken breast meat during refrigerated storage. Foods. 13(24): 4063. doi.org/10.3390/foods13244063.
  • Bauer AW. 1966. Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45, 493-496.
  • Bhunia AK. 2018. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis. Springer.
  • CDC 2022. Salmonella. Centers for Disease Control and Prevention. https://www.cdc.gov/salmonella/index.html
  • CLSI 2009. Clinical and Laboratory Standarts Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard-Seventh Edition. M07- A7, Villanova, PA, USA.
  • Çiftçi A, Güran HŞ. 2019. Evaluation of microbial contamination and shelf life of packaged chicken meat. J Food Sci Tech. 56(5): 2341–2347. doi.org/10.1007/s13197-019-03752-8
  • Çufaoğlu G, Ambarcıoğlu P, Derinöz AN, Ayaz ND. 2023. Prevalence, serotype diversity and antibiotic resistance of Salmonella among poultry meat and eggs in Türkiye: A Meta-analysis. J Agric Sci, 29(2): 519-533. doi.org/10.15832/ankutbd.1108594
  • Dışhan A, Hızlısoy H, Ertaş Onmaz N, Yıldırım Y, Gönülalan Z, Al S. 2024. Comprehensive analysis of Salmonella in poultry meat and products in Türkiye: Prevalence, antibiotic susceptibility and genomic characterisation. Int J Food Sci Technol. 59(5): 3412-3422. doi.org/10.1111/ijfs.17097
  • EFSA. 2021. The European Union One Health 2020 Zoonoses Report. EFSA J., 19(12): e06971.
  • Elbayoumi Z, Ibrahim G, Zayda M, Shawish R. 2023. Prevalence and molecular characterization of Salmonella spp. in poultry meat and its products. J Curr Vet Res. 5(2): 1-9. doi: 10.21608/jcvr.2023.320405. FAO/WHO. 2019. Food Safety and Quality. Food and Agriculture Organization of the United Nations & World Health Organization.
  • Halkman K (ed). 2005. Merck Gıda Mikrobiyolojisi Uygulamaları. Ed. AK Halkman. Başak Matbaacılık Ltd. Şti., Ankara, 358 s.
  • Krumperman P. 1983. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol, 46: 165-170.
  • Kundakçı A, Yücel A, Uylaşer V, Konca R, Can S. 1991. Microflora and quality of chicken meat stored under cold conditions and offered for sale. In Proceedings of the 2nd International Food Symposium, Bursa, pp. 191–200.
  • Rivera D, Allel K, Dueñas F, Tardone R, Soza P, Hamilton-West C, Moreno-Switt AI. 2021. Screening the presence of non-typhoidal Salmonella in different animal systems and the assessment of antimicrobial resistance. Animals 11(6): 1532. doi.org/10.3390/ ani11061532.
  • Sağun E, Sancak YC, Ekici K, Durmaz H. 1996. A study on the hygenic quality of chicken breast and thigh consumed in Van.. Van Vet J. 7(1-2): 62-66.
  • Sharma V, Singh M. 2023. Bacteriological quality of poultry meat from local markets of Jammu city. Indian J Anim Health. 62(2): 182–188. doi.org/10.36062/ijah.2023.15322.
  • Singh DV. Sanyal SC. 1992. Haemolysin and enterotoxin production by Aeromonas caviae isolated from diarrhoeal patients. Fish Environ J Diarrhoeal Dis Res. 10(1): 16-20.
  • Sokol PA, Ohman DE. Iglewski BH. 1979. A more sensitive plate assay for detection of protease production by Pseudomonas aeruginosa. J Clinic Microbiol. 9: 538-540.
  • Sonkar A, Rathi MN, Gole VC. 2018. Biofilm-forming ability of foodborne pathogens and their resistance to sanitizers in meat processing environments. J Food Saf, 38(6): e12559.
  • Şahin S, Kalın R, Arslanbaş E. Moğulkoç MN. 2017. Satışa sunulan tavuk etlerinde bazı bakteri ve indikatör mikroorganizmaların belirlenmesi. Manas J Agr Vet Life Sci. 7 (1): 47‐56.
  • Tamer AÜ, Uçar F, Ünver E, Karaboz İ, Bursalıoğlu M. Oğultekin (Eltem) R. 1989. 3. ve 4.Sınıf Mikrobiyoloji laboratuvar kılavuzu”. T.C. Anadolu Üniv. Eğitim, Sağlık ve Bilimsel Araş. Çalışmal. Vakfı Yayın., No:74, Eskişehir.
  • Telli R. 2006. Afyon’da tütketime sunulan tavuk karkas ve tavuk Eti örneklerinde Salmonella spp. varlığının klasik kültür tekniği ile saptanması, Yüksek Lisans Tezi, Afyon Kocatepe Üniversitesi, Sağlık Bilimleri Enstitüsü, Afyonkarahisar.
  • Turkish Statistical Institute (TÜİK). 2022. Poultry and egg production and sales [Data set]. Turkish Statistical Institute. https://data.tuik.gov.tr/ [Accessed October 15, 2025]
  • Van Boeckel T.P, Brower C, Gilbert M. 2015. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci. 112(18): 5649–5654.
  • Wang X, Wang H, Li T. 2013. Modeling and predicting the biofilm formation of different Salmonella strains. J Food Safe. 33(4): 503–508. doi.org/10.1111/jfs.12082.
  • WHO. 2020. Food Safety. World Health Organization. https://www.who.int/news-room/fact-sheets/detail/food-safety
  • Yanık HD, Müştak HK, Sarıçam İnce S. 2025. Effects of environmental and genetic factors on biofilm formation of various Salmonella serotypes. Turk J Vet Anim Sci. 49(2): 70–75. doi.org/10.55730/1300-0128.4372
  • Yıldırım M, Ünlü A, Yıldırım Z. 2015. Microbiological quality of retail chicken meat in Turkey. J Food Safe. 35(2): 123–130. doi.org/10.1111/jfs.12145.
There are 35 citations in total.

Details

Primary Language English
Subjects Bacteriology, Basic Food Processes
Journal Section Research Article
Authors

Ebru Başaran This is me

Nurcihan Hacıoğlu Doğru

Project Number FYL-2022-4214
Submission Date October 17, 2025
Acceptance Date December 9, 2025
Publication Date December 29, 2025
Published in Issue Year 2025 Volume: 8 Issue: 2

Cite

APA Başaran, E., & Hacıoğlu Doğru, N. (2025). Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye. Eurasian Journal of Biological and Chemical Sciences, 8(2), 71-78. https://doi.org/10.46239/ejbcs.1804245
AMA Başaran E, Hacıoğlu Doğru N. Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye. Eurasian J. Bio. Chem. Sci. December 2025;8(2):71-78. doi:10.46239/ejbcs.1804245
Chicago Başaran, Ebru, and Nurcihan Hacıoğlu Doğru. “Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella Spp. In Retail Chicken Meats in Çanakkale, Türkiye”. Eurasian Journal of Biological and Chemical Sciences 8, no. 2 (December 2025): 71-78. https://doi.org/10.46239/ejbcs.1804245.
EndNote Başaran E, Hacıoğlu Doğru N (December 1, 2025) Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye. Eurasian Journal of Biological and Chemical Sciences 8 2 71–78.
IEEE E. Başaran and N. Hacıoğlu Doğru, “Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye”, Eurasian J. Bio. Chem. Sci., vol. 8, no. 2, pp. 71–78, 2025, doi: 10.46239/ejbcs.1804245.
ISNAD Başaran, Ebru - Hacıoğlu Doğru, Nurcihan. “Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella Spp. In Retail Chicken Meats in Çanakkale, Türkiye”. Eurasian Journal of Biological and Chemical Sciences 8/2 (December2025), 71-78. https://doi.org/10.46239/ejbcs.1804245.
JAMA Başaran E, Hacıoğlu Doğru N. Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye. Eurasian J. Bio. Chem. Sci. 2025;8:71–78.
MLA Başaran, Ebru and Nurcihan Hacıoğlu Doğru. “Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella Spp. In Retail Chicken Meats in Çanakkale, Türkiye”. Eurasian Journal of Biological and Chemical Sciences, vol. 8, no. 2, 2025, pp. 71-78, doi:10.46239/ejbcs.1804245.
Vancouver Başaran E, Hacıoğlu Doğru N. Prevalence, Virulence Characteristics, and Antimicrobial Susceptibility of Salmonella spp. in Retail Chicken Meats in Çanakkale, Türkiye. Eurasian J. Bio. Chem. Sci. 2025;8(2):71-8.