Decontamination of Salmonella Enteritidis on Eggshell: Assessment of Efficiency of a Bacteriophage and Levulinic Acid-Sodium Dodecyl Sulfate

Year 2024, , 34 - 42, 29.03.2024

Gamze Koçer Alaşalvar , Zeliha Yıldırım

https://doi.org/10.24323/akademik-gida.1460979

Abstract

The majority of food infections caused by consumption of egg and egg products are caused by Salmonella enterica subspecies enterica serovar Enteritidis. In this study, the inhibitory effect against S. Enteritidis was determined by dipping the eggshell into Salmonella-specific bacteriophage SE-P47 and levulinic acid (LVA) plus sodium dodecyl sulfate (SDS) solutions (0.5% LVA+0.05% SDS, 1% LVA+0.05% SDS and 2% LVA+0.5% SDS) separately for 10 minutes. The treatments of phage and 2% LVA+0.5% SDS reduced S. Enteritidis below the detectable level on eggshell (at 2.76, 3.22, 4.48 and 5.30 log CFU/cm2 inoculum levels). After the treatment of 1% LVA+0.05% SDS, 1.94 and 0.89 log reductions were obtained at 4.48 and 5.30 log CFU/cm2 inoculum levels, respectively, while S. Enteritidis decreased below the detectable number at 2.76, 3.22 log CFU/cm2 inoculum levels. Although the lowest antibacterial activity was observed in the treatment of 0.5% LVA+%0.05 SDS, the decrease in the number of S. Enteritidis detected in all samples except 5.30 log CFU/cm2 inoculum level was found to be significant compared to the control sample. The results indicated that the combination of LVA and SDS, and especially SE-P47 phage alone had good potential efficacy for Salmonella decontamination on eggshell.

Keywords

Bacteriophage, Decontamination, Eggshell, Levulinic acid, Salmonella Enteritidis

Yumurta Kabuğunda Salmonella Enteritidis’in Dekontaminasyonu: Bakteriyofaj ve Levülinik Asit-Sodyum Dodesil Sülfatın Etkinliğinin Değerlendirilmesi

Abstract

Yumurta ve yumurta ürünlerinin tüketiminden kaynaklanan enfeksiyonların çoğu, Salmonella enterica subspecies enterica serovar Enteritidis kaynaklıdır. Bu çalışmada, yumurta kabukları Salmonella’ya özgü SE-P47 bakteriyofajı ve levülinik asit (LVA) ile sodyum dodesil sülfat (SDS) çözeltilerine (0.5% LVA+0.05% SDS, 1% LVA+0.05% SDS ve 2% LVA+0.5% SDS) ayrı ayrı 10 dk süreyle daldırılarak S. Enteritidis üzerindeki inhibitör etki belirlenmiştir. Faj ve %2 LVA+%0.5 SDS uygulamaları, yumurta kabuğu üzerinde S. Enteritidis'i tespit edilebilir seviyenin altına düşürmüştür (2.76, 3.22, 4.48 ve 5.30 log kob/cm2 inokulum seviyelerinde). %1 LVA+%0.05 SDS uygulamasından sonra 4.48 ve 5.30 log kob/cm2 inokulum seviyelerinde sırasıyla 1.94 ve 0.89 log azalma elde edilirken, 2.76, 3.22 log kob/cm2 inokulum seviyelerinde S. Enteritidis, tespit edilebilir seviyenin altına düşmüştür. En düşük antibakteriyel aktivite %0.5 LVA+%0.05 SDS uygulamasında gözlemlenmesine rağmen, 5.30 log kob/cm2 inokulum seviyesi hariç tüm örneklerde tespit edilen S. Enteritidis sayısındaki azalma, kontrol örneğine göre önemli bulunmuştur. Sonuçlar, yumurta kabuğunda Salmonella dekontaminasyonu için LVA ile SDS'nin kombinasyonu ve özellikle SE-P47 fajının tek başına iyi bir potansiyel etkinliğe sahip olduğunu göstermiştir.

Keywords

Bakteriyofaj, Dekontaminasyon, Yumurta kabuğu, Levülinik asit, Salmonella Enteritidis

References

• [1] Dhama, K., Rajagunalan, S., Chakraborty, S., Verma, A.K., Kumar, A., Tiwari, R., Kapoor, S. (2013). Food-borne pathogens of animal origin-diagnosis, prevention, control and their zoonotic significance: a review. Pakistan Journal of Biological Sciences, 16(20), 1076–1085.
• [2] Heredia, N., García, S. (2018). Animals as sources of food-borne pathogens: A review. Animal Nutrition, 4(3), 250–255.
• [3] WHO, (2015). WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007-2015. In World Health Organization. Available from: https://apps.who.int/iris/handle/10665/199350 (Accessed 25 May 2022).
• [4] Jaffee, S., Henson, S., Unnevehr, L., Grace, D., Cassou, E. (2018). The safe food imperative: Accelerating progress in low-and middle-income countries. Evidence on the Burden of Unsafe Food in Low- and Middle- Income Countries. Washington, D.C.: World Bank. pp. 27-67. ISBN 978-1-4648-1346-7 (online).
• [5] Scallan, E., Hoekstra, R.M., Mahon, B.E., Jones, T.F., Griffin, P.M. (2015). An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiology & Infection, 143(13), 2795–2804.
• [6] CDC, (2022). Centers of Disease Control and Prevention. Salmonella Homepage. Available from: https://www.cdc.gov/salmonella/general/index.html (Accessed 25 May 2022).
• [7] Eng, S.K., Pusparajah, P., Ab Mutalib, N.S., Ser, H.L., Chan, K.G., Lee, L.H. (2015). Salmonella: A review on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Science, 8(3), 284–293.
• [8] Lamas, A., Miranda, J.M., Regal, P., Vázquez, B., Franco, C.M., Cepeda, A. (2018). A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiological Research, 206, 60–73.
• [9] Ferrari, R.G., Rosario, D.K.A., Cunha-Neto, A., Mano, S.B., Figueiredo, E.E.S., Conte-Juniora, C.A. (2019). Worldwide epidemiology of Salmonella serovars in animal-based foods: A meta-analysis. Applied and Environmental Microbiology, 85(14), e00591-19.
• [10] Gut, A.M., Vasiljevic, T., Yeager, T., Donkor, O.N. (2018). Salmonella infection – prevention and treatment by antibiotics and probiotic yeasts: a review. Microbiology, 164(11), 1327–1344.
• [11] Antunes, P., Réu, C., Sousa, J.C., Peixe, L., Pestana, N. (2003). Incidence of Salmonella from poultry products and their susceptibility to antimicrobial agents. International Journal of Food Microbiology, 82(2), 97–103.
• [12] Pande, V.V., Devon, R.L., Sharma, P., McWhorter, A.R., Chousalkar, K.K. (2016). Study of Salmonella Typhimurium infection in laying hens. Frontiers in Microbiology, 7, 203.
• [13] Wright, A.P., Richardson, L., Mahon, B.E., Rothenberg, R., Cole, D.J. (2016). The rise and decline in Salmonella enterica serovar Enteritidis outbreaks attributed to egg-containing foods in the United States, 1973–2009. Epidemiology & Infection, 144(4), 810–819.
• [14] Upadhyaya, I., Yin, H.B., Nair, M.S., Venkitanarayanan, K. (2017). Natural approaches for improving postharvest safety of egg and egg products. Producing safe eggs: Microbial Ecology of Salmonella, Edited by S.C. Ricke, R.K. Gast, Academic Press, Amsterdam, 391–420p.
• [15] Howard, Z.R., O’Bryan, C.A., Crandall, P.G., Ricke, S.C. (2012). Salmonella Enteritidis in shell eggs: Current issues and prospects for control. Food Research International, 45(2), 755–764.
• [16] Ricke, S.C., Birkhold, S.G., Gast, R.K. (2001). Eggs and egg products. Compendium of Methods for the Microbiological Examination of Foods, Edited by F.P. Downes, K. Ito, American Public Health Association, Washington, D.C. 473–479p.
• [17] Baker, R.C., Bruce, C. (1994). Effects of Processing on the Microbiology of Eggs. Microbiology of the Avian Egg, Edited by R.G. Board, R. Fuller, Chapman & Hall, London, England, 153–173p.
• [18] Tayel, A.A., El-Sedfy, M.A., Ibrahim, A.I., Moussa, S.H. (2018). Application of Quercus infectoria extract as a natural antimicrobial agent for chicken egg decontamination. Revista Argentina de Microbiología, 50(4), 391–397.
• [19] Latimer, H.K., Jaykus, L.A., Morales, R.A., Cowen, P., Crawford-Brown, D. (2002). Sensitivity analysis of Salmonella Enteritidis levels in contaminated shell eggs using a biphasic growth model. International Journal of Food Microbiology, 75(1-2), 71–87.
• [20] Lombardi, M.E., Ladman, B.S., Alphin, R.L., Benson, E.R. (2008). Inactivation of avian ınfluenza virus using common detergents and chemicals. Avian Diseases, 52(1), 118-123.
• [21] Maktabi, S., Zarei, M., Rashnavady, R. (2018). Effect of sequential treatments with sodium dodecyl sulfate and citric acid or hydrogen peroxide on the reduction of some foodborne pathogens on eggshell. Iranian Journal of Veterinary Research, 19(2), 113-117.
• [22] Rodriguez-Romo, L.A., Yousef, A.E. (2005). Inactivation of Salmonella enterica serovar Enteritidis on shell eggs by ozone and UV radiation. Journal of Food Protection, 68(4), 711–717.
• [23] Li, Z., Guo, R., Wang, F., Geng, S., Kang, X., Meng, C., Gu, D., Jiao, X., Pan, Z. (2019). Inactivation of Salmonella Enteritidis on eggshells by lactic acid spray. Food Control, 104, 201–207.
• [24] Abdel-Salam, B., Nader, M., Emam, R. (2018). Decontamination of eggshell contaminated with Salmonella Typhimurium using natural plant extracts. International Journal of Pharmaceutical Research & Allied Sciences, 7(3), 10–19.
• [25] Park, S.Y., Jung, S.J., Ha, S. Do. (2018). Synergistic effects of combined X-ray and aqueous chlorine dioxide treatments against Salmonella Typhimurium biofilm on quail egg shells. LWT - Food Science and Technology, 92, 54–60.
• [26] Manfreda, G., Cevoli, C., Lucchi, A., Pasquali, F., Fabbri, A., Franchini, A. (2010). Hot air treatment for surface decontamination of table eggs experimentally infected with Salmonella, Listeria, and Escherichia coli. Veterinary Research Communications, 34(1), 179–182.
• [27] Turtoi, M., Borda, D. (2014). Decontamination of egg shells using ultraviolet light treatment. World’s Poultry Science Journal, 70(2), 265-278.
• [28] Keklik, N.M., Demirci, A., Patterson, P.H., Puri, V.M. (2010). Pulsed UV light inactivation of Salmonella Enteritidis on eggshells and its effects on egg quality. Journal of Food Protection, 73(8), 1408–1415.
• [29] Lasagabaster, A., Arboleya, J.C., De Marañón, I.M. (2011). Pulsed light technology for surface decontamination of eggs: Impact on Salmonella inactivation and egg quality. Innovative Food Science & Emerging Technologies, 12(2), 124–128.
• [30] Alkaya, G.B., Erdogdu, F., Halkman, A.K., Ekiz, H.I. (2016). Surface decontamination of whole-shell eggs using far-infrared radiation. Food and Bioproducts Processing, 98, 275–282.
• [31] Dasan, B.G., Yildirim, T., Boyaci, I.H. (2018). Surface decontamination of eggshells by using non-thermal atmospheric plasma. International Journal of Food Microbiology, 266, 267–273.
• [32] Wan, Z., Chen, Y., Pankaj, S.K., Keener, K.M. (2017). High voltage atmospheric cold plasma treatment of refrigerated chicken eggs for control of Salmonella Enteritidis contamination on egg shell. LWT - Food Science and Technology, 76, 124–130.
• [33] Zhao, T., Zhao, P., Doyle, M.P. (2009). Inactivation of Salmonella and Escherichia coli O157:H7 on lettuce and poultry skin by combinations of levulinic acid and sodium dodecyl sulfate. Journal of Food Protection, 72(5), 928-936.
• [34] FDA, (2022a). U.S. Food and Drug Administration. CFR - Code of Federal Regulations Title 21. Available from: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/cfrsearch.cfm?fr=172.822 (Accessed 25 May 2022).
• [35] FDA, (2022b). U.S. Food and Drug Administration. CFR - Code of Federal Regulations Title 21. Available from: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=172.515 (Accessed 25 May 2022).
• [36] Zhou, M., Doyle, M.P., Chen, D. (2019). Combination of levulinic acid and sodium dodecyl sulfate on inactivation of foodborne microorganisms: A review. Critical Reviews in Food Science and Nutrition, 60(15), 2526-2531.
• [37] Chen, D., Zhao, T., Doyle, M.P. (2015). Single- and mixed-species biofilm formation by Escherichia coli O157:H7 and Salmonella, and their sensitivity to levulinic acid plus sodium dodecyl sulfate. Food Control, 57, 48-53.
• [38] Zhao, T., Zhao, P., Cannon, J.L., Doyle, M.P. (2011). Inactivation of Salmonella in biofilms and on chicken cages and preharvest poultry by levulinic acid and sodium dodecyl sulfate. Journal of Food Protection, 74(12), 2024–2030.
• [39] Chen, D., Zhao, T., Doyle, M.P. (2014). Transfer of foodborne pathogens during mechanical slicing and their inactivation by levulinic acid-based sanitizer on slicers. Food Microbiology, 38, 263–269.
• [40] Webb, C.C., Erickson, M.C., Davey, L.E., Doyle, M.P. (2015). Effectiveness of levulinic acid and sodium dodecyl sulfate employed as a sanitizer during harvest or packing of cantaloupes contaminated with Salmonella Poona. International Journal of Food Microbiology, 207, 71–76.
• [41] Zhou, Z., Zuber, S., Cantergiani, F., Butot, S., Li, D., Stroheker, T., Devlieghere, F., Lima, A., Piantini, U., Uyttendaele, M. (2017). Inactivation of viruses and bacteria on strawberries using a levulinic acid plus sodium dodecyl sulfate based sanitizer, taking sensorial and chemical food safety aspects into account. International Journal of Food Microbiology, 257, 176–182.
• [42] Greer, G.G. (2005). Bacteriophage control of foodborne bacteria. Journal of Food Protection, 68(5), 1102–1111.
• [43] Loc-Carrillo, C., Abedon, S.T. (2011). Pros and cons of phage therapy. Bacteriophage, 1(2), 111–114.
• [44] Sillankorva, S.M., Oliveira, H., Azeredo, J. (2012). Bacteriophages and Their Role in Food Safety. International Journal of Microbiology, 2012.
• [45] Aydin Demirarslan, Ö., Alasalvar, H., Yildirim, Z. (2021). Biocontrol of Salmonella Enteritidis on chicken meat and skin using lytic SE-P3, P16, P37, and P47 bacteriophages. LWT - Food Science and Technology, 137, 110469.
• [46] Moye, Z.D., Woolston, J., Sulakvelidze, A. (2018). Bacteriophage applications for food production and processing. Viruses, 10(4), 205.
• [47] Spricigo, D.A., Bardina, C., Cortés, P., Llagostera, M. (2013). Use of a bacteriophage cocktail to control Salmonella in food and the food industry. International Journal of Food Microbiology, 165(2), 169–174.
• [48] Şanlıbaba, P. Uymaz, B. (2015). Gıdalarda Listeria monocytogenes’in biyokontrolünde faj uygulaması. Akademik Gıda, 13 (1), 81-88.
• [49] Ergin, F., Yıldız, G., Çomak Göçer, E.M. Küçükçetin, A. (2017). Bakteriyofajların antibakteriyel ajan olarak kullanımı. Akademik Gıda, 15 (2), 172-181.
• [50] Cooper, I.R. (2016). A review of current methods using bacteriophages in live animals, food and animal products intended for human consumption. Journal of Microbiological Methods, 130, 38–47.
• [51] Yildirim, Z., Sakin, T., Çoban, F. (2018). Isolation of lytic bacteriophages infecting Salmonella Typhimurium and Salmonella Enteritidis. Acta Biologica Hungarica, 69(3), 350–369.
• [52] Yildirim, Z., Sakin, T., Akçelik, M., Akçelik, N. (2019). Characterization of SE-P3, P16, P37, and P47 bacteriophages infecting Salmonella Enteritidis. Journal of Basic Microbiology, 59(10), 1049–1062.
• [53] Adams, M.H. (1959). Methods of study of bacterial viruses. Bacteriophages.
• [54] Bhat, R. S., & Al-Daihan, S. (2014). Phytochemical constituents and antibacterial activity of some green leafy vegetables. Asian Pacific Journal of Tropical Biomedicine, 4(3), 189-193.
• [55] Aydin, A., Cannon, J.L., Zhao, T., Doyle, M.P. (2013). Efficacy of a levulinic acid plus sodium dodecyl sulfate (SDS)-based sanitizer on inactivation of influenza a virus on eggshells. Food and Environmental Virology, 5(4), 215–219.
• [56] Gantois, I., Ducatelle, R., Pasmans, F., Haesebrouck, F., Gast, R., Humphrey, T.J., Van Immerseel, F. (2009). Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiology Reviews, 33(4), 718–738.
• [57] Himathongkham, S., Riemann, H., Ernst, R. (1999). Efficacy of disinfection of shell eggs externally contaminated with Salmonella Enteritidis: Implications for egg testing. International Journal of Food Microbiology, 49(3), 161–167.
• [58] Miyamoto, T., Horie, T., Baba, E., Sasai, K., Fukata, T., Arakawa, A. (1998). Salmonella penetration through eggshell associated with freshness of laid eggs and refrigeration. Journal of Food Protection, 61(3), 350–353.
• [59] EFSA, (2014). EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on the public health risks of table eggs due to deterioration and development of pathogens. EFSA Journal, 12(7), 3782–3929.
• [60] UNECE Standards, (1986). Hens Egg Products For Use in the Food Industry. 63. Available from: https://unece.org/fileadmin/DAM/trade/agr/standard/eggs/e/63produc.pdf (Accessed 7 March 2022).
• [61] Anonymous, (2011). Regulation on Turkish Food Codex microbiological criteria. Law of Authorization: 5996. Official Gazette of Publication, No. 28157. Available from: https://www.tarimorman.gov.tr/Belgeler/ENG/Legislation/regulation_microbiological_criteria.pdf (Accessed 25 May 2022).
• [62] Akarca, G., Istek, Ö., Tomar, O. (2021). The effect of resin coating on the quality characteristics of chicken eggs during storage. Journal of Food Science, 86(4), 1243-1257.
• [63] Sritha, K.S., Bhat, S.G. (2021). In vitro efficiency evaluation of phage cocktail for biocontrol of Salmonella spp. in food products. Archives of Microbiology, 203(9), 5445–5452.
• [64] Henriques, A., Sereno, R., Almeida, A. (2013). Reducing Salmonella horizontal transmission during egg incubation by phage therapy. Foodborne Pathogens and Disease, 10(8), 718–722.
• [65] Clavijo, V., Baquero, D., Hernandez, S., Farfan, J.C., Arias, J., Arévalo, A., Donado-Godoy, P., Vives-Flores, M. (2019). Phage cocktail SalmoFREE® reduces Salmonella on a commercial broiler farm. Poultry Science, 98(10), 5054–5063.
• [66] Waseh, S., Hanifi-Moghaddam, P., Coleman, R., Masotti, M., Ryan, S., Foss, M., MacKenzie, R., Henry, M., Szymanski, C.M., Tanha, J. (2010). Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: prospects of a novel therapy against bacterial ınfections. PLos One, 5(11), e13904.