The Effect of Marinade Containing Lactic Acid Bacteria on the Microbial Quality and Shelf Life of Chicken Wings

Abstract

This study evaluated the survival of Salmonella spp., Listeria monocytogenes, Pseudomonas spp., Enterobacteriaceae, total aerobic mesophilic bacteria (TAMB), lactic acid bacteria (LAB), and yeasts– molds in chicken wings marinated with a homemade sauce enriched with bioprotective lactic acid bacteria (Lactiplantibacillus plantarum, Latilactobacillus sakei, and Latilactobacillus curvatus) during storage at 4 ºC and 8 ºC. Inoculated chicken wings were divided into three groups: unmarinated control, marinated control (M), and marinated with a LAB mixture (M-LAB). Initial pH values were 6.13 for the control, 4.89 for M, and 4.97 for M-LAB. At 4 ºC, Salmonella counts in M and MLAB were reduced by 0.8 and 1.6 log10 cfu/mL compared with the control, while L. monocytogenes counts were 2.1 and 1.3 log10 cfu/mL lower on day 14 (p<0.05). At 8 ºC, reductions in Salmonella and L. monocytogenes in marinated groups reached 1.3 and 1.8 log10 cfu/mL, respectively, compared to the control (p<0.05). Pseudomonas spp. exceeded the spoilage threshold of 7 log10 cfu/mL on day 8 in the control, day 12 in M, and day 14 in M-LAB at 4 ºC. Enterobacteriaceae counts on day 14 at 4 ºC were 8.5, 6.3, and 6.2 log10 cfu/mL in the control, M, and M-LAB groups, respectively (p<0.05). Yeast–mold counts at 4 ºC on day 14 were higher in M but lower in M-LAB than in the control (p<0.05). Overall, marination with LAB effectively inhibited pathogens and spoilage microorganisms, slowed quality deterioration, improved microbial safety and shelf life of marinated chicken wings.

Keywords

• Bio-Protective Cultures
• Chicken Wings
• L. monocytogenes
• Marination
• Salmonella spp.

Supporting Institution

Balikesir University

Project Number

BAP 2022/042

Ethical Statement

“This study is not subject to approval by the Animal Experiments Ethics Committee (HADYEK) in accordance with Article 8 (k) of the Regulation on Working Procedures and Principles of Animal Experiments Ethics Committees. The data, information, and documents presented in this article were obtained within the framework of academic and ethical rules.”

Thanks

This study was supported by Balıkesir University Scientific Research Projects Unit (BAP) (Project No: 2022/042). One of the authors, Enise Begüm Göçmez, received a YÖK 100/2000 PhD scholarship.

Laktik Asit Bakterileri İçeren Sosun Tavuk Kanatlarının Mikrobiyal Kalitesi ve Raf Ömrü Üzerindeki Etkisi

Abstract

Bu çalışma, biyokoruyucu laktik asit bakterileri (LAB) ile zenginleştirilmiş ev yapımı sosla marine edilmiş tavuk kanatlarında Salmonella spp., Listeria monocytogenes, Pseudomonas spp., Enterobacteriaceae, toplam aerobik mezofilik bakteriler (TAMB), laktik asit bakterileri (LAB) ve maya-küflerin inhibisyon düzeyi oranları değerlendirilmiştir. Kontamine edilen tavuk kanatları üç gruba ayrıldı: marine edilmemiş kontrol, marine edilmiş kontrol (M) ve LAB karışımı ile marine edilmiş (M-LAB). Başlangıç pH değerleri kontrol için 6,13, M için 4,89 ve M-LAB için 4,97 idi. 4 ºC'de, M ve M-LAB'daki Salmonella sayıları kontrol grubuna kıyasla 0,8 ve 1,6 log10 kob/mL azalırken, L. monocytogenes sayıları 14. günde 2,1 ve 1,3 log10 kob/mL daha düşüktü (p<0,05). 8 ºC'de, marine edilmiş gruplarda Salmonella ve L. monocytogenes sayılarındaki azalma, kontrole kıyasla sırasıyla 1,3 ve 1,8 log10 kob/mL'ye ulaştı (p<0,05). Pseudomonas spp. 4 ºC'de kontrol grubunda 8. günde, M grubunda 12. günde ve M-LAB grubunda 14. günde 7 log10 kob/mL'lik bozulma eşiğini aştı. 4 ºC'de 14. günde Enterobacteriaceae sayıları kontrol, M ve M-LAB gruplarında sırasıyla 8,5, 6,3 ve 6,2 log10 kob/mL idi (p<0,05). 14. günde 4°C'de maya-küf sayıları M'de daha yüksek, M-LAB'da ise kontrol grubuna göre daha düşüktü (p<0,05). Genel olarak, LAB ile marine etme, patojenleri ve bozulmaya neden olan mikroorganizmaları etkili bir şekilde inhibe etti, kalite bozulmasını yavaşlattı, marine edilmiş tavuk kanatlarının mikrobiyal güvenliğini ve raf ömrünü iyileştirdi.

Keywords

• Biyo-Koruyucu Kültürler
• L. monocytogenes
• Marinasyon
• Salmonella spp.
• Tavuk Kanat Eti

Supporting Institution

Balıkesir Üniversitesi

Project Number

BAP 2022/042

Ethical Statement

“Bu çalışma, Hayvan Deneyleri Etik Kurullarının Çalışma Usulü ve İlkeleri Hakkındaki Yönetmeliğin 8. maddesinin (k) bendi uyarınca Hayvan Deneyleri Etik Kurulu (HADYEK) onayına tabi değildir. Bu makalede sunulan veriler, bilgiler ve belgeler akademik ve etik kurallar çerçevesinde elde edilmiştir.”

Thanks

Bu çalışma Balıkesir Üniversitesi Bilimsel Araştırma Projeleri Birimi (BAP) tarafından desteklenmiştir (Proje No: 2022/042). Yazarlardan Enise Begüm Göçmez, YÖK 100/2000 doktora bursu almıştır.

References

1. Arriaga-Lorenzo, P., Maldonado-Simán, E., Ramírez-Valverde, R., Martínez-Hernández, P. A., Tirado- González, D. N., & Saavedra-Jiménez, L. A. (2024). Meat cold chain management in Mexican supermarkets. Theory and Practice of Meat Processing, 9(2), 100-107. http://doi.org/10.21323/2414-438X- 2024-9-2-100-107
2. Austrich-Comas, A., Serra-Castelló, C., Jofré, A., Gou, P., & Bover-Cid, S. (2022). Control of Listeria monocytogenes in chicken dry-fermented sausages with bioprotective starter culture and highpressure processing. Frontiers in Microbiology, 13, 983265. https://doi.org/10.3389/fmicb.2022.983265
3. Chen, C.-Y., Armstrong, C. M., He, Y., Counihan, K., Atencia, J., Lee, J., Dykes, G., Johnson, K., Koppenhofer, H., Tilman, S., Martinos, S., & Capobianco, J. (2025). Multiplexed Detection of Salmonella, Escherichia coli, Campylobacter, and Listeria in Raw Poultry. Foods, 14(7), 1137. https://doi.org/10.3390/foods14071137
4. Erdaw, M. M., & Beyene, W. T. (2022). Trends, prospects and the socio-economic contribution of poultry production in sub-Saharan Africa: a review. World's Poultry Science Journal, 78(3), 835-852. https://doi.org/10.1080/00439339.2022.2092437
5. Fan, Y., Zhang, K., Liu, Q., Chen, Q., Xia, Xiufang., Sun, Fangda., & Baohua, Kong. (2025). Mechanism, application, and prospect of bioprotective cultures in meat and meat products. Food Chemistry, 476, 143474. https://doi.org/10.1016/j.foodchem.2025.143474
6. Hoyle, A. R., Brooks, J. C., Thompson, L. D., Palmore, W., Stephens, T. P., & Brashears, M. M. (2009). Spoilage and safety characteristics of ground beef treated with lactic acid bacteria. Journal of Food Protection, 72(11), 2278-2283. https://doi.org/10.4315/0362-028X- 72.11.2278
7. Hulankova, R., Borilova, G., Abdullah, F. A. A., & Buchtova, H. (2018). Microbiological quality of organic chicken meat during refrigerated storage in air and modified atmospheres. British Poultry Science, 59(5), 506-513. https://doi.org/10.1080/00071668.2018.1496399
8. İncili, G. K., Akgöl, M., Aydemir, M. E., Alan, S., Mutlu, M., Ilhak, O. I., & Öksüztepe, G. (2020b). Fate of Listeria monocytogenes and Salmonella Typhimurium in homemade marinade and on marinated chicken drumsticks, wings and breast meat. Lwt-Food Science and Technology, 134, 110231. https://doi.org/10.1016/j.lwt.2020.110231

9. İncili, G. K., İlhak, O. İ., & Çalıcıoğlu, M. (2025). Inhibitory effect of cell-free supernatants of Pedicoccous acidilactici and Latilactobacillus sakei/Staphylococcus xylosus in combination with ethylenediaminetetraacetic acid against Escherichia coli O157:H7 strains. Veterinary Research Forum, 16(8), 439 - 446 DOI: 10.30466/vrf.2025.2035776.4368
10. İncili, G. K., Karatepe, P., & İlhak, O. İ. (2020a). Effect of chitosan and Pediococcus acidilactici on E. coli O157: H7, Salmonella Typhimurium and Listeria monocytogenes in meatballs. LWT, 117, 108706. https://doi.org/10.1016/j.lwt.2019.108706
11. James, C., Onarinde, B. A., & James, S. J. (2017). The use and performance of household refrigerators: A review. Comprehensive Reviews in Food Science and Food Safety, 16(1), 160-179. https://doi.org/10.1111/1541-4337.12242
12. Kingkaew, E., Tanasupawat, S. (2023). Application of antimicrobial peptides fromlactic acid bacteria in food preservation and human health. In A. Gupta, & R. Prasad (Eds.), Antimicrobials in Food Science and Technology. (1st ed., pp. 1–29), CRC Press. https://doi.org/10.1201/9781003268949
13. Kralik, G., Kralik, Z., Grčević, M., & Hanžek, D. (2018). Quality of chicken meat. Animal Husbandry and Nutrition, 63. 10.5772/intechopen.72865
14. Lytou, A. E., Tzortzinis, K., Skandamis, P. N., Nychas, G. J. E., & Panagou, E. Z. (2019). Investigating the influence of organic acid marinades, storage temperature and time on the survival/inactivation interface of Salmonella on chicken breast fillets. International Journal of Food Microbiology, 299, 47-57. https://doi.org/10.1016/j.ijfoodmicro.2019.03.019
15. Mohammadi, R., Moradi, M., Tajik, H., & Molaei, R. (2022). Potential application of postbiotics metabolites from bioprotective culture to fabricate bacterial nanocellulose based antimicrobial packaging material. International Journal of Biological Macromolecules, 220, 528-536. https://doi.org/10.1016/j.ijbiomac.2022.08.108
16. Ndoye, B., Dicko, M. H., & Gill, C. (2025). Exploring the spoilage microbiota of raw and processed meats under different storage environments and its related profiling methods: a review. Cogent Food & Agriculture, 11(1). https://doi.org/10.1080/23311932.2025.2562177
17. Olaimat, A. N., Al-Holy, M. A., Shahbaz, H. M., Al-Nabulsi, A. A., Abu Ghoush, M. H., Osaili, T. M., ... & Holley, R. A. (2018). Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: a comprehensive review. Comprehensive Reviews in Food Science and Food Safety, 17(5), 1277- 1292. https://doi.org/10.1111/1541-4337.12387
18. Ovca, A., Škufca, T., & Jevšnik, M. (2021). Temperatures and storage conditions in domestic refrigerators— Slovenian scenario. Food Control, 123, 107715. https://doi.org/10.1016/j.foodcont.2020.107715
19. Ozturk, B., & Sengun, I. Y. (2025). Effects of cell-free supernatants produced by lactic acid bacteria on the safety and quality of poultry meat. British Poultry Science, 1–13. https://doi.org/10.1080/00071668.2025.2500344
20. Pedonese, F., Torracca, B., Mancini, S., Pisano, S., Turchi, B., Cerri, D., & Nuvoloni, R. (2020). Effect of a Lactobacillus sakei and Staphylococcus xylosus protective culture on Listeria monocytogenes growth and quality traits of Italian fresh sausage (salsiccia) stored at abusive temperature. Italian Journal of Animal Science, 19(1), 1363-1374. https://doi.org/10.1080/1828051X.20 20.1844084
21. Phan-Thanh, L., Mahouin, F., & Aligé, S. (2000). Acid responses of Listeria monocytogenes. International Journal of Food Microbiology, 55(1-3), 121-126. https://doi.org/10.1016/S0168-1605(00)00167-7
22. Ray, B. (2021). Fundamental food microbiology. CRC Press, 625 p., Boca Raton- Florida
23. Serter, B., Önen, A., & Osman, I. I. (2024). Antimicrobial efficacy of postbiotics of lactic acid bacteria and their effects on food safety and shelf life of chicken meat. Annals of Animal Science, 24(1), 277-287. https://doi.org/10.2478/aoas-2023-0081
24. Smaoui, S., Echegaray, N., Kumar, M., Chaari, M., D’Amore, T., Shariati, M. A., ... & Lorenzo, J. M. (2024). Beyond conventional meat preservation: saddling the control of bacteriocin and lactic acid bacteria for clean label and functional meat products. Applied Biochemistry and Biotechnology, 196(6), 3604- 3635. http://10.1007/s12010-023-04680-x
25. Wang, Q., Zhang, K., Li, M., Liu, H., Kong, B., & Chen, Q. (2024). Bioprotective potential of Latilactobacillus sakei and Latilactobacillus curvatus in smoked chicken legs with modified atmosphere packaging. Food Control, 164, 110558. https://doi.org/10.1016/j.foodcont.2024.110558
26. Xu, M. M., Kaur, M., Pillidge, C. J., & Torley, P. J. (2023). Culture-dependent and culture-independent evaluation of the effect of protective cultures on spoilage-related bacteria in vacuum-packaged beef mince. Food and Bioprocess Technology, 16(2), 382-394.
27. Zaboli, G., Huang, X., Feng, X., & Ahn, D. U. (2019). How can heat stress affect chicken meat quality?–a review. Poultry science, 98(3), 1551-1556. http://dx.doi.org/10.3382/ps/pey399
28. Zdolec, N., Kiš, M., Vukšić, M., Mazija, H., Bazina, I., & Kazazić, S. (2025). Lactic acid bacteria succession, ıdentification and antilisterial capacity in traditionally produced dry-fermented chicken sausage. Processes, 13(7), 2216. https://doi.org/10.3390/pr13072216
29. Zhang, H., Wu, J. & Guo, X. (2016). Effects of antimicrobial and antioxidant activities of spice extracts on raw chicken meat quality. Food Science and Human Wellness, 5(1), 39–48, https://doi.org/10.1016/j.fshw.2015.11.003.