Microbiological Quality of Table Eggs Sold at Different Sales Location

Yıl 2020, Cilt: 35 Sayı: 2, 115 - 124, 29.12.2020

Fatma Yenilmez , Ayşen Bulancak

https://doi.org/10.36846/CJAFS.2020.25

Öz

In this study, we will compare the microbiological quality of table eggs and aim to shed light on consumer preferences in terms of egg safety. Totally 150 eggs randomly selected and grouped into three groups from 225 eggs which have been purchased 5 different market+brand (in cooler cabinet), grocery+brand (open) and bazaar (village egg). A total number of Mesophilic Aerobic Bacteria (TMAB), total mold-yeast, Enterobacteriaceae and Salmonella spp. loads were determined by using commercial kits. According to the research results, market eggs shell had the lowest load in terms of TMAB and Mold-Yeast (P≤0.05), but higher Enterobacteriaceae load (P>0.05). Salmonella spp. determined in one sample from the village and 2 samples from grocery eggs, but none from market eggs. TMAB and total mold-yeast amount were found to be highest in village egg albumens. Market egg albumens and yolk samples were detected free from microorganisms. The results of the analysis show that it would be more safety to prefer market eggs from the cooler cabinets with cold chains. It is necessary to be more careful about village egg consumption because of their microorganism load which can penetrate into eggs by outdoor sale conditions like heat and moisture.

Anahtar Kelimeler

Consumer preference, egg, microbiological load, sales location, Salmonella

Kaynakça

• Adesiyun, A., Offıah, N., Seepersadsıngh, N., Rodrıgo, S., Lashley, V., Musaı, L., Georges, K. (2005) Microbial health risk posed by table eggs in Trinidad. Epidemiology and Infection, 133(6): 1049-1056. Ahmed, H.F., Deeb, M.M.A., Aman, I.M. (2002) Studies on market hen eggs in Kafr El-Sheikh and El-Gharbia Governorates. Vet Med J Giza., 50 (4): 610-615.
• Akbaş, E. (2014) Ulusal Mikrobiyoloji Standartları. Volume I: Bulaşıcı Hastalıklar Laboratuvar Tanı Rehberi; Ankara, Turkey.
• AL-Ashmawy, M.A.M. (2013) Prevalence of Enterobacteriaceae in table eggs with particular reference to enterovirulent Escherichia coli strains. International Journal of Poultry Science, 12 (7): 430-435.
• Ansah, T., Dzoagbe, G.S.K., Teye, G.A., Adday, S., Danquah J.K. (2009) Microbial quality of table eggs sold on selected markets in the Tamale municipality in the Northern Region of Ghana. Livestock Research for Rural Development, 21 (8): 1-12.
• Arathy, S., Vanpee, G., Belot, G., Vanessa, M., Claude, D., Ravindra, N.S. (2009) Bacterial contamination of commercial chicken eggs in Canada, West Indies. West Ind. Vet. J., 9 (2): 4-7.
• Awny, C., Amer, A.A., Abo El-Makarem, H.S. (2018) Microbial hazards associated with consumption of table eggs. AJVS., 58 (1): 139-146.
• Aygün, A. (2017) The eggshell microbial activity. In: Hester, P.Y. (eds), Egg innovations and strategies for improvements. Chapter 13, Academic Press. pp. 135-144. United States. ISBN: 978-0-12-800879-9
• Bahobail, A.A.S, Hassan, S.A., El-Deeb, B.A. (2012) Microbial quality and content aflatoxins of commercially available eggs in Taif, Saudi Arabia. Afr J Microbiol Res., 6 (13): 3337-3342.
• Bulancak, A., Baylan, M., Ergınkaya, Z., Toy, N. (2016) Effects of propolis and thyme essential oil as a bio-fumigants on microbiological load of hatching eggs and incubation performance parameters. World's Poultry Science Journal, Volume 72, Supplement I, 5th Mediterranean Poultry Summit, Oral sessions, 20-25 October, Italy-Spain- France, page 41.
• Casey, B.B., Ian, T.W., Robert, V.T. (2012) Emerging food borne pathogens and problems; expanding prevention efforts before slaughter or harvest. Improving food safety through one health approach. Work shop summary. National academies press (US), 500 Fifth Street, NW. Washington DC. pp 1-418.
• Carter G.R., Cole R.J. (1990) Diagnostic procedures in veterinary bacteriology and mycology. 5th ed. San Diego, California, USA.
• Chaemsanit, S., Akbar, A., and Anal, A.K. (2015) Isolation of total aerobic and pathogenic bacteria from table eggs and its contents. Food and Applied Bioscience Journal, 3 (1): 1-9.
• De Reu, K., Messens, W., Heyndrickx, M., Rodenburg, T.B., Uyttendaelle, M., Herman, L. (2008) Bacterial contamination of table eggs and the influence of housing systems. World’s Poult.Sci. J., 64: 5-19.
• De Reu, K., Rodenburd, T.B., Grijspreerdt, K., Heyndrickx, M., Tuyttens, F.A.M., Sonck, B., Zoons, J., Herman, L. (2009) Bacteriological contamination, dirt, and crack of eggshells in furnished cages and noncage systems for laying hens: an international on-farm comparison. Poultry Science, 88: 2442-2448.
• EFSA (European Food Safety Authority) (2005) Opinion of the Scientific Panel on biological hazards (BIOHAZ) related to the Microbiological risks on washing of Table Eggs. EFSA Journal, 269: 1-39.
• EFSA (European Food Safety Authority) (2014) European Food Safety Authority, BIOHAZ Panel (EFSA Panel on Biological Hazards). Scientific Opinion on the public health risks of table eggs due to deterioration and development of pathogens. EFSA Journal, 12 (7): 3782-3929.
• EFSA (European Food Safety Authority) (2015) The European Union summary report on trends and sources of Zoonoses, Zoonotic agents and food-borne outbreaks in 2014. EFSA Journal, 13 (12): 4329.
• Eke, M.O., Olaitan, N.I., Ochefu, J.H. (2013) Effect of storage conditions on the quality attributes of shell (table) eggs. NIFOJ. 31: 18-24.
• Englmaierova, M., Tůmová, E., Charvátová, V., Skřivan, M. (2014) Effects of laying hens housing system on laying performance, egg quality characteristics, and egg microbial contamination. Czech J. Anim. Sci., 59 (8): 345-352.
• European Communities (EC) (1993) Microbiological criteria for egg products. The egg products regulations, Available at: http://www.legislation.gov.uk/uksi/1993/1520/made Accessed 24 June 2020.
• European Commission (EC) (2004) Regulation No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for the hygiene of foodstuffs. Official Journal of the European Union, L 139/55.
• European Commission (EC) (2008) Commission Regulation No. 589/2008 of 23 June 2008 laying down detailed rules for implementing Council Regulation (EC) No. 1234/2007 as regards marketing standards for eggs. Official Journal of the European Union, L 163/6.
• Fikiin, K., Akterian, S., Stankov, B. (2020) Do raw eggs need to be refrigerated along the food chain? Is the current EU regulation ensuring high-quality shell eggs for the European consumers?, Trends in Food Science & Technology, 100: 359-362.
• Gole, V.C., Chousalkar, K.K., Roberts, J.R. (2013) Survey of Enterobac-teriaceae contamination of table eggs collected from layer flocks in Australia. Int J Food Microbiol. 164 (2-3): 161-165.
• Gordon, R.F., Tucker, J.F. (1965) The Epizootiology of Salmonella menston infection of fowls and the effect of feeding poultry food artificially infected with Salmonella. British Poultry Science, 6 (3): 251-264.
• Harry, E.G. (1963) The relationship between egg spoilage and the environment of the egg when laid. British Poultry Science, 4 (1): 91-100.
• Hilbert F., Paulsen P., Smulders F.J.M. (2014) Safety of food and beverages. In: Motarjemi, Y. (eds), Poultry and eggs. Volume III: Encyclopedia of Food Safety, Academic Press. pp.280-284. San Diego, USA.
• IBM Corp. Released (2010) IBM SPSS Statistics for Windows, Version 19.0. IBM Corp. Armonk, NY, USA.
• Indhu, B., Muthusami, S., Thirunavukkarasu, N. (2014) Studies on Microflora and their Role on Eggshell Contamination and Infection. Int. J. Pharm. Chem. Bio. Sci., 4 (3): 518-521.
• ISO 6579 (1993) Microbiology – General guidance on methods for the detection of Salmonella. International Organization for Standardization, Geneva, Switzerland.
• ISO 4832 (2006) Microbiology of food and animal feeding stuffs – Horizontal method for the enumeration of coliforms – Colony-count technique; ISO: Geneva, Switzerland.
• ISO 21528-2 (2011) Turkish food safety criteria. https://www.magenta.com.tr/img/cat/29.12.2011-turk-gIda-kodeksi-mikrobiyolojik-kriterler-yonetmeligi-ekleri-140.pdf Accessed 27 June 2020.
• İncili, G.K., Durmuşoğlu, H., Güngören, A., İlhak, O.I. (2019) Investigation of Microbiological Quality of Conventional (cage type) and Village Eggs Sold in Elazig. The Journal of Faculty of Veterinary Medicine, 12 (2): 97-102.
• İskender H., Kanbay Y. (2014) Determination of Egg Consumption Habits University Students. The Journal of The Faculty of Veterinary Medicine University of Yuzuncu Yil, 25 (3): 57-62.
• Jones, D.R., Musgrove, M.T., Northcutt, J.K. (2004) Variation in external and internal microbial populations in shell eggs during extended storage. J. Food Prot., 67 (12): 2657-2660.
• Jones, D.R., Musgrove M.T. (2007) Pathogen prevalence and microbial levels associated with restricted shell eggs. J Food Prot., 70 (9): 2004-2007.
• Jones, D.R., Ward, G.E., Regmi, P., Karcher, D.M. (2018) Impact of egg handling and conditions during extended storage on egg quality. Poult. Sci., 97: 716-723.
• Karadal, F., Onmaz, N.E., Hızlısoy, H., Yıldırım, Y., Al, S., Gönülalan, Z., Ülger, İ. (2018) The Microbiological quality of the village and market eggs sold at retail in Nigde and Kayseri. Journal of Faculty of Veterinary Medicine, 15 (1): 51-57.
• Keller, L.H., Benson, C.E., Krotec, K., Eckroade, R.J. (1995) Microorganisms colonization of the reproductive tract of forming and freshly laid eggs of chicken. Infect Immun, 63 (7): 2443-2449.
• Mallet, S., Huneau-Salaun, A., Herman L., De Reu, K. (2010) Laying hen breeding systems and hygienic status of the eggs. Productions Animals, 23: 183–191.
• Martelli, F., Davies, R.H. (2012) Salmonella serovars isolated from table eggs: An overview. Food Research International, 45 (2): 745-754.
• Mayes, F. J., Takeballi, M.A. (1983) Microbial contamination of the hen’s egg: A rewiev. J. Food Prot., 46: 1092-1098.
• Messens, W., Grijspeerdt, K., Herman, L. (2005) Eggshell penetration by Salmonella: A rewiev. Worlds Poult Sci J., 61 (1): 71-86.
• Mızrak, C., Durmuş, İ., Kamanlı, S., Demirtaş, Ş.E., Kalebaşı, S., Karademir, E., Doğu, M. (2012) Determination egg consumption and consumer habits in Turkey. Turk J Vet Anim Sci., 36 (6): 592-60.
• Musgrove, M.T., Jones, D.R., Northcutt, J.K. (2004) Identification of Enterobacteriacae from washed and unwashed commercial shell eggs. J. Food Prot., 67: 2613-2616.
• Musgrove, M.T., Jones, D.R., Northcutt, J.K., Cox, N.A., Harrison, M.A. (2005) Shell rinse and shell crush methods for the recovery of aerobic microorganisms and Enterobacteriaceae from shell eggs. Journal of Food Protection, 68: 2144-2148.
• Musgrove, M.T., Jones, D.R., Northcutt, J.K., Cox, N.A., Harrison, M.A. (2005) Shell rinse and shell crush methods for the recovery of aerobic microorganisms and Enterobacteriaceae from shell eggs. Journal of Food Protection, 68: 2144-2148.
• Nordenskjöld, J. (2010) Study of microflora on egg shells in egg production in Jordan. Independent project/degree project in food science Uppsala Biocenter University of agricultural sciences. EX0426 Independent project/degree project in Food Science. pp.1-30.
• Pasquali, F., Klein, G., Reich, F., Manfreda, G., Valero, A. (2016) Modelling survival behaviour of Salmonella enterica ser. Enteritidis, Typhimurium and Tennessee on table eggs during storage at different temperatures. Food Control, 59: 314-319.
• Regulation on Turkish Food Codex Microbiological Criteria (2011) 28157. https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6.htm Accessed 27 June 2020.
• Regulation on Turkish Food Codex Egg Notification (2014) 29211. https://www.resmigazete.gov.tr/eskiler/2014/12/20141220-5.htm Accessed 27 June 2020.
• Ricke, S.C., Birkhold, S.G., Gast, R.K. (2001) Eggs and egg products. In: Downes, F.P., Ito, K (eds), Compendium of methods for the microbiological examination of foods, 4th edn. pp. 473-479. Washington, DC.
• Roberts, D., Greenwood, M. (1995) Practical food microbiology. Roberts, D (eds), Third Edition, Massachusetts, USA.
• Roberts, S.J.R., Chousalkar, K.K. (2014) Effect of production system and flock age on egg quality and total bacterial load in commercial laying hens. Journal of Applied Poultry Research, 23 (1): 59-70.
• Sabarinath A., Guillaume V., Guillaume B., Mathew V., DeAllie C., Sharma R.N. (2009) Bacterial contamination of commercial chicken eggs in Grenada. West Indian Veterinary Journal, 9 (2): 4-7.
• Salem, R.M., El-Kaseh R.M., El-Diasty E.M.A. (2009) Study on the fungal contamination and prevalence of Aflatoxins and some antibiotic residues in table eggs. Arab J Biotech., 12 (1): 65-72.
• Stepien-Pysniak, D. (2010) Occurrence of Gram-negative bacteria in hens’ eggs depending on their source and storage conditions. Polish J Vet Sci., 13(3): 507-513.
• Techer, C., Baron, F., Jan, S. (2013) Microbial spoilage of eggs and egg products. Egg Meat Symposia. Bergamo, 15-19 September 2013, World’s Poultry Science Journal, Volume 69, Supplement. pp.1-6.
• Tomczyk, L., Szablewski, T., Stuper-Szablewska, K.,Nowaczewski, S., Cegielska-Radziejewska, R. (2019) The influence of the conditions of acquisition and storage of table eggs on changes in their quality and the presence of mycobiota and Fusarium mycotoxins. Poultry Science, 98: 2964-2971.
• Wall, H., Tauson, R., Sorgjerd, S. (2008) Bacterial contamination of eggshells in furnished and conventional cages. J. Appl. Poult. Res. 17 (1): 11-16.
• WHO/FAO (2002) Risk assessments of Salmonella in eggs and broiler chickens. In Microbiological Risk Assessment Series No.2. Geneva, Switzerland.
• Zeidler, G. (2002) Processing and Packaging Shell Eggs. In: Bell D.D. and Weaver W.D (eds), Commercial Chicken Meat and Egg Production. 5th edn. pp. 1129-1161. New York, USA.