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Effect of Vinegar and Lemon Juice on Survival of Salmonella in Outer Surface of Chicken Eggshell

Year 2022, Volume: 15 Issue: 4, 490 - 499, 31.12.2022
https://doi.org/10.30607/kvj.1176327

Abstract

In this study, experimentally contaminated eggs with Salmonella were immersed for 3 min in distilled water (DW), lemon juice (L), vinegar (S) and lemon juice+vinegar (LS), and then stored at three different conditions such as: i) 4°C for 28 days, ii) 25°C for 28 days, iii) 4°C for 10 days following 25°C for 18 days. On day 0, Salmonella in control (K, without any treatment), DW, L, S and LS groups were detected 3,2±1,0, 3,6±0,4, 1,7±0,5, 1,9±0,8 and 1,8±0,8 log cfu/eggshell, respectively. The decrease in the number of Salmonella at day 0 in L and LS groups was statistically significant compared to K and DW groups (P<0,05). The Salmonella number decreased below the level of detection on the 18th day of storage in L and LS groups and on the 21st day in S group at 25 °C and 25 °C (18 days)+4 °C (10 days). The difference between Salmonella numbers at 4°C was found significant between DW and S and LS groups on the 6th day of storage (P<0,05). According to SEM observation of eggshell, it was determined that washing with L, S and LS caused significant damage to the cuticle layer of the eggshell. This study demonstrated that the use of lemon juice and vinegar in eggs resulted significant reductions in the number of Salmonella.

References

  • Al-Haq MI, Junichi S, Seiichiro I. Applications of electrolyzed water in agriculture & food industries. Food Sci Technol Res. 2005; 11(2): 135-150.
  • Anonim.(2009). http://www.legislation.gov.uk/uksi/2009/2163/pdfs/uksi_20092163_en.pdf; Erişim Tarihi: 07.09.2022.
  • Anonim.(2022a). https://arastirma.tarimorman.gov.tr/tepge/Menu/27/Tarim-Urunleri-Piyasalari; Erişim Tarihi: 23.05.2022.
  • Anonim. (2022b). https://www.fsis.usda.gov/food-safety/safe-food-handling-and-preparation/eggs/shell-eggs-farm-table#:~:text=Back%20to%20Top%5DShould%20you%20wash%20eggs%3F,the%20outside%20by%20the%20hen; Erişim Tarihi: 07.09.2022
  • Anonim. (2014) Türk Gıda Kodeksi Yumurta ve Yumurta Ürünleri Tebliği. Tebliğ No: 2014/55. Resmi Gazete 20.12.2014-29211, 2014. Baker R. Survival of Salmonella enteritidis on and in shelled eggs, liquid eggs and cooked egg products. Dairy Food Environ Sanit. 1990; 10(5): 273-275.
  • Bingöl EB, Cetin O, Muratoglu K. Effect of lemon juice on the survival of Salmonella enteritidis and Escherichia coli in cig kofte (raw meatball). Br Food J. 2011; 113(9): 1183-1194
  • Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis. 2015; 12(1): 32-38.
  • Cemeroğlu B, Yemenicioğlu A, Özkan M. Meyve ve sebzelerin bileşimi. Meyve ve sebze işleme teknolojisi 2004; 1: 1-188.
  • De Knegt LV, Pıres SM, Hald T. Attributing foodborne salmonellosis in humans to animal reservoirs in the European Union using a multi-country stochastic model. Epidemiology & Infection. 2015; 143(6): 1175-1186.
  • De Souza PM, de Melo R, de Aguilar Santos MA, Lima FR, Vieira KH. Risk Management of Egg and Egg Products: Advanced Methods Applied. J Food Eng. IntechOpen; 2019.
  • EFSA. The European Union One Health 2020 Zoonoses Report. EFSA J. 2021; 19(12): e06971.
  • Elhan S. Farkli Sirke Çeşitleri Ve Konsantrasyonlarinin Salata Bileşenlerinin Dezenfeksiyonunda Kullanim İmkanlarinin Araştirilmasi. Doktora Tezi, Atatürk Üniversitesi Fen Bilimleri Enstitüsü, Erzurum, 2014.
  • Galiş AM, Marcq C, Marlier D, Portetelle D, Van I, Beckers Y, Théwis A. Control of Salmonella contamination of shell eggs—Preharvest and postharvest methods: A review. Compr Rev Food Sci Food Saf. 2013; 12(2): 155-82.
  • Gökırmaklı Ç, Budak HN, Güzel-Seydim ZB. Antimicrobial Effect of Vinegar. Turkish JAF Sci Tech. 2019; 7(10): 1635-1640.
  • Grudlewska-Buda K, Wiktorczyk-Kapischke N, Wałecka-Zacharska E, Kwiecińska-Piróg J, Gryń G, Skowron KJ, Skowron K. Effect of Radiant Catalytic Ionization and Ozonation on Salmonella spp. on Eggshells. Foods. 2022; 11(16): 2452.
  • Hawkins J, Vimini B, Schwarz JG, Nichols P, Parveen S. Application of antimicrobial agents via commercial spray cabinet to inactivate Salmonella on skinless chicken meat. J Food Prot. 2016; 79(4): 569-573.
  • Henley SC, Jeanne G, Jennifer JQ. Don’t wash your chicken!: A food safety education campaign to address a common food mishandling practice. Food Prot Trends. 2016; 36: 43-53.
  • Henley SC, Launchı N, Quınlan JJ. Survival of Salmonella on raw poultry exposed to 10% lemon juice and vinegar washes. Food Control. 2018; 94: 229-232.
  • Henley, SC. "Don't Wash Your Chicken!" Results of an Interdisciplinary Approach to Reduce Incidence of Infectious Foodborne Diseases. Philadelphia: Drexel University, 2013.
  • Ilhak OI, Guran HS. Combined Antimicrobial Effect of Thymol and Sodium Lactate against Listeria monocytogenes and Salmonella typhimurium in Fish Patty. J. Food Saf. 2014; 34(3), 211-217.
  • Jay JM, Loessner MJ, Golden DA. Protection of foods with low-temperatures, and characteristics of psychrotrophic microorganisms. J Microbiol Biotechnol Food Sci. 2005; 395-413.
  • Juven BJ, Pierson MD. Antibacterial effects of hydrogen peroxide and methods for its detection and quantitation. J Food Prot. 1996; 59(11): 1233-1241.
  • Keerthirathne TP, Ross K, Fallowfield H, Whiley H. Reducing risk of Salmonellosis through egg decontamination processes. Int J Environ Res Public Health. 2017; 14(3): 335.
  • Kışla D, Üzgün Y. Microbiological evaluation of stuffed mussels. J Food Prot. 2008; 71(3): 616-620.
  • Koppel K, Suwonsichon S, Chitra U, Lee J, Chambers IVE. Eggs and poultry purchase, storage, and preparation practices of consumers in selected Asian countries. Foods. 2014; 3(1): 110-127.
  • Lakins DG, Alvarado CZ, Thompson LD, Brashears MT, Brooks JC, Brashears MM. Reduction of Salmonella enteritidis in shell eggs using directional microwave technology. Poultry Science. 2008; 87(5): 985-991.
  • Li Z, Guo R, Wang F, Geng S, Kang X, Meng C, Pan Z. Inactivation of Salmonella enteritidis on eggshells by lactic acid spray. Food Control. 2019; 104: 201-207.
  • Lytou AE, Tzortzinis K, Skandamis PN, Nychas GJE, Panagou EZ. Investigating the influence of organic acid marinades, storage temperature and time on the survival/inactivation interface of Salmonella on chicken breast fillets. Int J Food Microbiol. 2019; 299: 47-57.
  • Mattioli S, Ortenzi R, Scuota S, Mancinelli AC, Dal Bosco A, Cotozzolo E, Castellini C. Impact of ozone and UV irradiation sanitation treatments on the survival of Salmonella and the physical–chemical characteristics of hen eggs. J Appl Poult Res. 2020; 29(2): 409-419.
  • Ofongo RTS, Ohımaın EI. Utilization Of İn-Feed Acidifier As A Control Measure For Salmonella Contamination Of Eggs from laying hens. Niger J Anim Prod. 2022; 49(3): 60-68.
  • Öncül N, Karabiyikli Ş. Antibacterial effect of verjuice against food-borne pathogens. Br Food J. 2019; 121: 2265-2276.
  • Park S, Choi S, Kim H, Kim Y, Kim BS, Beuchat LR, Ryu JH. Fate of mesophilic aerobic bacteria and Salmonella enterica on the surface of eggs as affected by chicken feces, storage temperature, and relative humidity. Food Microbiol. 2015; 48: 200-205.
  • Prior G, Hall L, Morris S, Draper A. Exploring food attitudes and behaviours in the UK: findings from the Food and You Survey 2010. Food Standards Agency. 2011.
  • Radkowski, M. Effect of moisture and temperature on survival of Salmonella enteritidis on shell eggs. Archiv für Geflügelkunde. 2002; 66(3): 119-123.
  • Réhault-Godbert S, Guyot N, Nys Y. The golden egg: nutritional value, bioactivities, and emerging benefits for human health. Nutrients. 2019; 11(3): 684.
  • SAS. Version 8: SAS institute Inc., Cary, NC, USA; 1999.
  • Şengün İY, Karapinar M. Bazı Sebzelere İnokule Edilen Salmonella typhimurium’un Limon Suyu ve Sirke ile İnaktivasyonu. Gıda. 2006; 31(3): 161-167.
  • Şengun IY, Karapinar M. Effectiveness of lemon juice, vinegar and their mixture in the elimination of Salmonella typhimurium on carrots (Daucus carota L.). Int J Food Microbiol. 2004; 96(3): 301-305.
  • Sırıken B, Haldun T. Poultry Meat and Salmonellosis. Animal Health Production and Hygiene. 2013; 2(1): 174-182.
  • Vatral CD, Quinlan JJ. Identification of barriers to consumers adopting the practice of not washing raw poultry. Food Control 2021; 123: 107682.
  • Wang H, Slavik ME. Bacterial penetration into eggs washed with various chemicals and stored at different temperatures and times. J Food Prot. 1998; 61(3): 276-279.

Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi

Year 2022, Volume: 15 Issue: 4, 490 - 499, 31.12.2022
https://doi.org/10.30607/kvj.1176327

Abstract

Bu araştırmada deneysel olarak Salmonella ile kontamine edilen yumurtalar kontrol (K) grubu hariç, distile su (DS), limon suyu (L), sirke (S) ve limon suyu+sirke (LS) yıkama sıvılarına daldırılıp 3 dakika bekletildikten sonra i) 4°C’de 28 gün, ii) 25 °C’de 28 gün, iii) 25 °C’de 18 gün ve sonrasında 4°C’de 10 gün olmak üzere üç farklı koşulda muhafaza edildi. K ve DS gruplarında 0. günde Salmonella sayısı sırasıyla 3,2±1,0 ve 3,6±0,4 log kob/yumurta kabuğu, L, S ve LS gruplarında ise sırasıyla 1,7±0,5, 1,9±0,8 ve 1,8±0,8 log kob/yumurta kabuğu olarak saptandı. L ve LS gruplarında 0. günde Salmonella sayısındaki azalma K ve DS gruplarına göre istatistiksel açıdan önemli bulundu (P<0,05). Salmonella sayısının 25 °C ve 25 °C (18 gün)+4 °C (10 gün) muhafazası sırasında L ve LS gruplarında muhafazanın 18. gününde, S grubunda ise 21. gününde tespit seviyesinin altına düştüğü belirlendi. Muhafaza sırasında (4 °C) Salmonella sayıları arasındaki farklılık DS ile S ve LS grupları arasında muhafazanın 6. gününde istatistiksel açıdan önemli bulundu (P<0,05). Tarayıcı elektron mikroskop görüntülerine göre L, S ve LS uygulamasının yumurtalarda kütikül tabakasında hasarlara neden olduğu saptandı. Bu çalışma; limon suyu ve sirkenin yumurtalarda Salmonella sayısında önemli derecede azalmalara neden olduğunu göstermektedir.

References

  • Al-Haq MI, Junichi S, Seiichiro I. Applications of electrolyzed water in agriculture & food industries. Food Sci Technol Res. 2005; 11(2): 135-150.
  • Anonim.(2009). http://www.legislation.gov.uk/uksi/2009/2163/pdfs/uksi_20092163_en.pdf; Erişim Tarihi: 07.09.2022.
  • Anonim.(2022a). https://arastirma.tarimorman.gov.tr/tepge/Menu/27/Tarim-Urunleri-Piyasalari; Erişim Tarihi: 23.05.2022.
  • Anonim. (2022b). https://www.fsis.usda.gov/food-safety/safe-food-handling-and-preparation/eggs/shell-eggs-farm-table#:~:text=Back%20to%20Top%5DShould%20you%20wash%20eggs%3F,the%20outside%20by%20the%20hen; Erişim Tarihi: 07.09.2022
  • Anonim. (2014) Türk Gıda Kodeksi Yumurta ve Yumurta Ürünleri Tebliği. Tebliğ No: 2014/55. Resmi Gazete 20.12.2014-29211, 2014. Baker R. Survival of Salmonella enteritidis on and in shelled eggs, liquid eggs and cooked egg products. Dairy Food Environ Sanit. 1990; 10(5): 273-275.
  • Bingöl EB, Cetin O, Muratoglu K. Effect of lemon juice on the survival of Salmonella enteritidis and Escherichia coli in cig kofte (raw meatball). Br Food J. 2011; 113(9): 1183-1194
  • Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis. 2015; 12(1): 32-38.
  • Cemeroğlu B, Yemenicioğlu A, Özkan M. Meyve ve sebzelerin bileşimi. Meyve ve sebze işleme teknolojisi 2004; 1: 1-188.
  • De Knegt LV, Pıres SM, Hald T. Attributing foodborne salmonellosis in humans to animal reservoirs in the European Union using a multi-country stochastic model. Epidemiology & Infection. 2015; 143(6): 1175-1186.
  • De Souza PM, de Melo R, de Aguilar Santos MA, Lima FR, Vieira KH. Risk Management of Egg and Egg Products: Advanced Methods Applied. J Food Eng. IntechOpen; 2019.
  • EFSA. The European Union One Health 2020 Zoonoses Report. EFSA J. 2021; 19(12): e06971.
  • Elhan S. Farkli Sirke Çeşitleri Ve Konsantrasyonlarinin Salata Bileşenlerinin Dezenfeksiyonunda Kullanim İmkanlarinin Araştirilmasi. Doktora Tezi, Atatürk Üniversitesi Fen Bilimleri Enstitüsü, Erzurum, 2014.
  • Galiş AM, Marcq C, Marlier D, Portetelle D, Van I, Beckers Y, Théwis A. Control of Salmonella contamination of shell eggs—Preharvest and postharvest methods: A review. Compr Rev Food Sci Food Saf. 2013; 12(2): 155-82.
  • Gökırmaklı Ç, Budak HN, Güzel-Seydim ZB. Antimicrobial Effect of Vinegar. Turkish JAF Sci Tech. 2019; 7(10): 1635-1640.
  • Grudlewska-Buda K, Wiktorczyk-Kapischke N, Wałecka-Zacharska E, Kwiecińska-Piróg J, Gryń G, Skowron KJ, Skowron K. Effect of Radiant Catalytic Ionization and Ozonation on Salmonella spp. on Eggshells. Foods. 2022; 11(16): 2452.
  • Hawkins J, Vimini B, Schwarz JG, Nichols P, Parveen S. Application of antimicrobial agents via commercial spray cabinet to inactivate Salmonella on skinless chicken meat. J Food Prot. 2016; 79(4): 569-573.
  • Henley SC, Jeanne G, Jennifer JQ. Don’t wash your chicken!: A food safety education campaign to address a common food mishandling practice. Food Prot Trends. 2016; 36: 43-53.
  • Henley SC, Launchı N, Quınlan JJ. Survival of Salmonella on raw poultry exposed to 10% lemon juice and vinegar washes. Food Control. 2018; 94: 229-232.
  • Henley, SC. "Don't Wash Your Chicken!" Results of an Interdisciplinary Approach to Reduce Incidence of Infectious Foodborne Diseases. Philadelphia: Drexel University, 2013.
  • Ilhak OI, Guran HS. Combined Antimicrobial Effect of Thymol and Sodium Lactate against Listeria monocytogenes and Salmonella typhimurium in Fish Patty. J. Food Saf. 2014; 34(3), 211-217.
  • Jay JM, Loessner MJ, Golden DA. Protection of foods with low-temperatures, and characteristics of psychrotrophic microorganisms. J Microbiol Biotechnol Food Sci. 2005; 395-413.
  • Juven BJ, Pierson MD. Antibacterial effects of hydrogen peroxide and methods for its detection and quantitation. J Food Prot. 1996; 59(11): 1233-1241.
  • Keerthirathne TP, Ross K, Fallowfield H, Whiley H. Reducing risk of Salmonellosis through egg decontamination processes. Int J Environ Res Public Health. 2017; 14(3): 335.
  • Kışla D, Üzgün Y. Microbiological evaluation of stuffed mussels. J Food Prot. 2008; 71(3): 616-620.
  • Koppel K, Suwonsichon S, Chitra U, Lee J, Chambers IVE. Eggs and poultry purchase, storage, and preparation practices of consumers in selected Asian countries. Foods. 2014; 3(1): 110-127.
  • Lakins DG, Alvarado CZ, Thompson LD, Brashears MT, Brooks JC, Brashears MM. Reduction of Salmonella enteritidis in shell eggs using directional microwave technology. Poultry Science. 2008; 87(5): 985-991.
  • Li Z, Guo R, Wang F, Geng S, Kang X, Meng C, Pan Z. Inactivation of Salmonella enteritidis on eggshells by lactic acid spray. Food Control. 2019; 104: 201-207.
  • Lytou AE, Tzortzinis K, Skandamis PN, Nychas GJE, Panagou EZ. Investigating the influence of organic acid marinades, storage temperature and time on the survival/inactivation interface of Salmonella on chicken breast fillets. Int J Food Microbiol. 2019; 299: 47-57.
  • Mattioli S, Ortenzi R, Scuota S, Mancinelli AC, Dal Bosco A, Cotozzolo E, Castellini C. Impact of ozone and UV irradiation sanitation treatments on the survival of Salmonella and the physical–chemical characteristics of hen eggs. J Appl Poult Res. 2020; 29(2): 409-419.
  • Ofongo RTS, Ohımaın EI. Utilization Of İn-Feed Acidifier As A Control Measure For Salmonella Contamination Of Eggs from laying hens. Niger J Anim Prod. 2022; 49(3): 60-68.
  • Öncül N, Karabiyikli Ş. Antibacterial effect of verjuice against food-borne pathogens. Br Food J. 2019; 121: 2265-2276.
  • Park S, Choi S, Kim H, Kim Y, Kim BS, Beuchat LR, Ryu JH. Fate of mesophilic aerobic bacteria and Salmonella enterica on the surface of eggs as affected by chicken feces, storage temperature, and relative humidity. Food Microbiol. 2015; 48: 200-205.
  • Prior G, Hall L, Morris S, Draper A. Exploring food attitudes and behaviours in the UK: findings from the Food and You Survey 2010. Food Standards Agency. 2011.
  • Radkowski, M. Effect of moisture and temperature on survival of Salmonella enteritidis on shell eggs. Archiv für Geflügelkunde. 2002; 66(3): 119-123.
  • Réhault-Godbert S, Guyot N, Nys Y. The golden egg: nutritional value, bioactivities, and emerging benefits for human health. Nutrients. 2019; 11(3): 684.
  • SAS. Version 8: SAS institute Inc., Cary, NC, USA; 1999.
  • Şengün İY, Karapinar M. Bazı Sebzelere İnokule Edilen Salmonella typhimurium’un Limon Suyu ve Sirke ile İnaktivasyonu. Gıda. 2006; 31(3): 161-167.
  • Şengun IY, Karapinar M. Effectiveness of lemon juice, vinegar and their mixture in the elimination of Salmonella typhimurium on carrots (Daucus carota L.). Int J Food Microbiol. 2004; 96(3): 301-305.
  • Sırıken B, Haldun T. Poultry Meat and Salmonellosis. Animal Health Production and Hygiene. 2013; 2(1): 174-182.
  • Vatral CD, Quinlan JJ. Identification of barriers to consumers adopting the practice of not washing raw poultry. Food Control 2021; 123: 107682.
  • Wang H, Slavik ME. Bacterial penetration into eggs washed with various chemicals and stored at different temperatures and times. J Food Prot. 1998; 61(3): 276-279.
There are 41 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Sciences
Journal Section RESEARCH ARTICLE
Authors

Uğur Uçar 0000-0002-7394-3355

Hüsnü Şahan Güran 0000-0002-6674-5510

Early Pub Date December 12, 2022
Publication Date December 31, 2022
Acceptance Date December 13, 2022
Published in Issue Year 2022 Volume: 15 Issue: 4

Cite

APA Uçar, U., & Güran, H. Ş. (2022). Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi. Kocatepe Veterinary Journal, 15(4), 490-499. https://doi.org/10.30607/kvj.1176327
AMA Uçar U, Güran HŞ. Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi. kvj. December 2022;15(4):490-499. doi:10.30607/kvj.1176327
Chicago Uçar, Uğur, and Hüsnü Şahan Güran. “Sirke Ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi”. Kocatepe Veterinary Journal 15, no. 4 (December 2022): 490-99. https://doi.org/10.30607/kvj.1176327.
EndNote Uçar U, Güran HŞ (December 1, 2022) Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi. Kocatepe Veterinary Journal 15 4 490–499.
IEEE U. Uçar and H. Ş. Güran, “Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi”, kvj, vol. 15, no. 4, pp. 490–499, 2022, doi: 10.30607/kvj.1176327.
ISNAD Uçar, Uğur - Güran, Hüsnü Şahan. “Sirke Ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi”. Kocatepe Veterinary Journal 15/4 (December 2022), 490-499. https://doi.org/10.30607/kvj.1176327.
JAMA Uçar U, Güran HŞ. Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi. kvj. 2022;15:490–499.
MLA Uçar, Uğur and Hüsnü Şahan Güran. “Sirke Ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi”. Kocatepe Veterinary Journal, vol. 15, no. 4, 2022, pp. 490-9, doi:10.30607/kvj.1176327.
Vancouver Uçar U, Güran HŞ. Sirke ve Limon Suyunun Tavuk Yumurta Kabuğu Dış Yüzeyinde Salmonella’nın Yaşamı Üzerine Etkisi. kvj. 2022;15(4):490-9.

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