Survival of Major Food Pathogens in Natural Zeolite (Clinoptilolite) at Different Ratios and in Chicken Wings After Dipping

Abstract

The aim of this study was to determine the viability of Salmonella Typhimurium and Listeria monocytogenes in solutions prepared with readily available natural zeolite and in chicken wings decontaminated with these solutions. To determine the effect of zeolite on pathogen viability, solutions of different concentrations (5%, 10%, 25%) were prepared and contaminated. Their numbers were then determined at different times (2, 6, and 24 hours) during storage at 4 °C. To determine the effect of zeolite on the viability of pathogens in chicken wings, contaminated chicken wings were immersed in zeolite solutions prepared at three different concentrations (5%, 10%, 25%) for two different times (1.5 min, 3 min) and their numbers were determined. According to the results of this study, the number of S. Typhimurium decreased by approximately 2.5 log10, and the number of L. monocytogenes decreased by approximately 1.4 log10 in zeolite solutions. The number of pathogens was significantly reduced in decontaminated chicken wings (P≤0.05). In addition, increasing the concentration of zeolite and changing the time had a significant effect on the number of S. Typhimurium (P≤0.05). In conclusion, zeolite was found to be antimicrobial against S. Typhimurium and L. monocytogenes and has the potential to be used in the decontamination of poultry meat. It is envisaged that zeolite may be a natural alternative to ensure food safety in the near future. To this end, zeolite should be extensively investigated in other potential food applications.

Keywords

• Chicken wings
• Clinoptilolite
• Listeria monocytogenes
• Salmonella Typhimurium
• Zeolite

Farklı Oranlardaki Doğal Zeolitde (Klinoptilolit) ve Daldırma Sonrası Tavuk Kanatlarda Önemli Gıda Patojenlerin Yaşam Kabiliyetleri

Abstract

Bu çalışmanın amacı kolaylıkla temin edilebilen doğal zeolit ile hazırlanmış solüsyonlarda ve bu solüsyonlar ile dekontamine edilmiş tavuk kanatlarında Salmonella Typhimurium ve Listeria monocytogenes’in yaşam kabiliyetlerini belirlemektir. Zeolitin, patojenlerin yaşam kabiliyeti üzerine etkisini belirlemek için farklı konsantrasyonlarda (%5, %10, %25) solüsyonlar hazırlanıp kontamine edildi. Daha sonra 4 °C’de muhafaza boyunca farklı sürelerde (2., 6., 24. saat) sayıları belirlendi. Zeolitin, tavuk kanatlarında patojenlerin yaşam kabiliyetine etkisinin belirlemesinde ise kontamine edilmiş tavuk kanatları üç farklı konsantrasyonda (%5, %10, %25) hazırlanan zeolit solüsyonlarına iki farklı sürede (1,5 ve 3 dk) daldırma işlemi yapılıp sayısı belirlendi. Bu çalışmanın sonuçlarına göre, zeolit solüsyonlarında S. Typhimurium sayısı yaklaşık 2,5 log10 azaldığını, L. monocytogenes sayısında ise yaklaşık 1,4 log10 azaldığı saptandı. Dekontamine edilmiş tavuk kanatlarında patojenlerin sayısı önemli ölçüde azaldığı saptandı (P≤0,05). Ayrıca zeolit konsantrasyonunun arttırılması ve sürenin değişimi S. Typhimurium sayısı üzerinde önemli etkisinin olduğu tespit edildi (P≤0,05). Sonuç olarak zeolitin S. Typhimurium ve L. monocytogenes’e karşı antimikrobiyal etkisinin olduğu ve kanatlı etlerinin dekontaminasyonunda kullanım potansiyeli olduğu ortaya konuldu. Yakın gelecekte gıda güvenliğinin sağlanması için zeolit doğal bir alternatif olabileceği öngürülmektedir. Bunun için zeolitin diğer potansiyel gıda uygulamaları içinde kapsamlı bir şekilde araştırılması gerekmektedir.

Keywords

• Tavuk kanat
• Klinoptilolit
• Listeria monocytogenes
• Salmonella Typhimurium
• Zeolit

References

1. Aydemir ME, Arslan A, 2023: Investigation the Effects of Jerusalem Thorn (Paliurus spina-christi Mill.), Oriental Hackberry (Celtis tournefortii L.) Fruits and Black Cumin (Nigella sativa L.) Seed on Microbial Quality and Physicochemical Properties of Meatballs. Harran Üniv Vet Fak Derg, 12(1), 27-34.
2. Chung D, Cho TJ, Rhee MS, 2018: Citrus fruit extracts with carvacrol and thymol eliminated 7-log acid-adapted Escherichia coli O157: H7, Salmonella typhimurium, and Listeria monocytogenes: A potential of effective natural antibacterial agents. Int Food Res, 107, 578-588.
3. Deshmukh RK, Hakim L, Akhila K, Ramakanth D, Gaikwad KK, 2023: Nano clays and its composites for food packaging applications. Int Nano Lett, 13(2), 131-153.
4. Dikić J, Lukić I, Pajnik J, Pavlović J, Hrenović J, Rajić N, 2021: Antibacterial activity of thymol/carvacrol and clinoptilolite composites prepared by supercritical solvent impregnation. J Porous Mater, 28(5), 1577-1584.
5. Dutta P, Wang B, 2019: Zeolite-supported silver as antimicrobial agents. Coord Chem Rev, 383, 1-29.
6. Eroglu N, Emekci M, Athanassiou CG, 2017: Applications of natural zeolites on agriculture and food production. J Sci Food Agri, 97(11), 3487-3499.
7. Güngören A, Güngören G, Şimşek ÜG, Yilmaz Ö, Bahşi M, Aslan, S. 2023: Quality properties and fatty acids composition of breast meat from Japanese quails with different varieties grown under warm climate. Veterinaria, 72(2), 163-173.
8. Hrenović J, Tibljaš D, Orhan Y, Büyükgüngör H, 2005: Immobilisation of Acinetobacter calcoaceticus using natural carriers. Water SA, 31(2), 261-266.

9. Huwei S, Asghari M, Zahedipour-Sheshglani P, Alizadeh M, 2021: Modeling and optimizing the changes in physical and biochemical properties of table grapes in response to natural zeolite treatment. LWT, 141, 110854.
10. İncili GK, Akgöl M, Aydemir ME, Alan S, Mutlu M, İlhak Oİ, Öksüztepe G, 2020: Fate of Listeria monocytogenes and Salmonella Typhimurium in homemade marinade and on marinated chicken drumsticks, wings and breast meat. LWT, 134, 110231.
11. İncı̇lı̇ GK, Aydemı̇r ME, Akgöl M, Kaya B, Kanmaz H, Öksüztepe G, Hayaloğlu AA, 2021: Effect of Rheum ribes L. juice on the survival of Listeria monocytogenes, Escherichia coli O157: H7 and Salmonella Typhimurium and chemical quality on vacuum packaged raw beef. LWT, 150, 112016.
12. Janićijević D, Uskoković-Marković S, Ranković D, Milenković M, Jevremović A, Vasiljević BN, Bajuk-Bogdanović D, 2020: Double active BEA zeolite/silver tungstophosphates–Antimicrobial effects and pesticide removal. Sci Total Environ, 735, 139530.
13. Keykhosravy K, Khanzadi S, Hashemi M, Azizzadeh M, 2020: Chitosan-loaded nanoemulsion containing Zataria Multiflora Boiss and Bunium persicum Boiss essential oils as edible coatings: Its impact on microbial quality of turkey meat and fate of inoculated pathogens. Int J Biol Macromol, 150, 904-913.
14. Kombaya-Touckia-Linin EM, Gaucel S, Sougrati MT, Stievano L, Gontard N, Guillard V, 2019: Elaboration and Characterization of Active Films Containing Iron–Montmorillonite Nanocomposites for O2 Scavenging. Nanomater, 9(9), 1193.
15. Lopes MM, Coutinho TC, Malafatti JOD, Paris EC, de Sousa CP, Farinas CS, 2021: Immobilization of phytase on zeolite modified with iron (II) for use in the animal feed and food industry sectors. Process Biochem, 100, 260-271.
16. Lu L, Chen C, Samarasekera C, Yeow JT, 2017: Influence of zeolite shape and particle size on their capacity to adsorb uremic toxin as powders and as fillers in membranes. J Biomed Mater Res B Appl Biomater, 105(6), 1594-1601.
17. Mallek Z, Fendri I, Khannous L, Ben Hassena A, Traore AI, Ayadi MA, Gdoura R, 2012: Effect of zeolite (clinoptilolite) as feed additive in Tunisian broilers on the total flora, meat texture and the production of omega 3 polyunsaturated fatty acid. Lipids Health Dis, 11, 1-7.
18. Mehdizadeh T, Langroodi AM, 2019: Chitosan coatings incorporated with propolis extract and Zataria multiflora Boiss oil for active packaging of chicken breast meat. Int J Biol Macromol, 141, 401-409.
19. Özbay SD, Sarıçoban C, 2014: Et ve Et Ürünlerine Uygulanan Bazı Dekontaminasyon Yöntemleri. Eur. J. Sci. Thecnol, 1 (3): 92-99.
20. Pajnik J, Lukić I, Dikić J, Asanin J, Gordic M, Misic D, Korzeniowska M, 2020: Application of supercritical solvent impregnation for production of zeolite modified starch-chitosan polymers with antibacterial properties. Mol, 25(20), 4717.
21. Papaioannou DS, Kyriakis SC, Papasteriadis A, Roumbies N, Yannakopoulos A, Alexopoulos C, 2002: Effect of in-feed inclusion of a natural zeolite (clinoptilolite) on certain vitamin, macro and trace element concentrations in the blood, liver and kidney tissues of sows. Res J Vet Sci, 72(1), 61-68.
22. Prabhu R, Devaraju A, 2018: Developing an antimicrobial packaging to improve the shelf life of meat using silver zeolite coating on BOPP film. Mater Today: Proceedings, 5(6), 14553-14559.
23. Prasai TP, Walsh KB, Bhattarai SP, Midmore DJ, Van TT, Moore RJ, Stanley D, 2017: Zeolite food supplementation reduces abundance of enterobacteria. Microbiol Res, 195, 24-30.
24. Sánchez MJ, Mauricio JE, Paredes AR, Gamero P, Cortés D, 2017: Antimicrobial properties of ZSM-5 type zeolite functionalized with silver. Mater Lett, 191, 65-68.
25. Sharma P, Sutar PP, Xiao H, Zhang Q, 2023: The untapped potential of zeolites in techno-augmentation of the biomaterials and food industrial processing operations: A review. J Future Foods, 3(2), 127-141.
26. Silva F, Domingues FC, Nerín C, 2018: Trends in microbial control techniques for poultry products. Crit Rev Food Sci Nutr, 58(4), 591-609.
27. Singh R, Kumar S, 2023: Nanomaterials: Plethora of Opportunities as Smart Packaging, Preserving, and Processing Agent in Food Industry. In Nanotechnology Advancement in Agro-Food Industry (pp. 43-79). Singapore: Springer Nature Singapore.
28. Soysal Ç, Bozkurt H, Dirican E, Güçlü M, Bozhüyük ED, Uslu AE, Kaya S, 2015: Effect of antimicrobial packaging on physicochemical and microbial quality of chicken drumsticks. Food Control, 54, 294-299.
29. Tunç S, Duman O, 2011: Preparation of active antimicrobial methyl cellulose/carvacrol/montmorillonite nanocomposite films and investigation of carvacrol release. LWT-Food Sci Technol, 44(2), 465-472.
30. Tzia C, Zorpas AA, 2012: Zeolites in food processing industries. Handbook of natural zeolites, 601-651.
31. Uchida T, Maru N, Furuhata M, Fujino A, Muramoto S, Ishibashi A, Koshiba K, Shiba T, Kikuchi T, 1992: Anti-bacterial zeolite balloon catheter and its potential for urinary tract infection control. Hinyokika Kiyo, 38, 8, 973-978.
32. Villa CC, Valencia GA, Córdoba AL, Ortega-Toro R, Ahmed S, Gutiérrez TJ, 2022: Zeolites for food applications: A review. Food Biosci, 46, 101577.
33. Wang L, Dionysiou DD, Wu W, Chen H, Xie X, Lin J, 2019: Zinc oxide-coated zeolite adsorbs and inactivates waterborne Staphylococcus aureus. Chemosphere, 229, 1-7.
34. Wu QJ, Wang LC, Zhou YM, Zhang JF, Wang T, 2013: Effects of clinoptilolite and modified clinoptilolite on the growth performance, intestinal microflora, and gut parameters of broilers. Poult sci, 92(3), 684-692.