Microbiological evaluation of some Egyptian fermented dairy products


Keywords:
Fermented dairy products S. aureus Coliforms E.coli yeast mold
I.M. AMAN
I.I. AL-HAWARY
S.M. ELEWA
W.M. EL-KASSAS
M.A. EL-MAGD
Abstract

This study was carried out to evaluate the microbiological quality of plain and fruit yoghurt and rayeb. Sixty samples of yoghurt (30 plain &30 fruit) and 60 samples of rayeb (30 plain &30 fruit) were randomly collected from different supermarkets in Kafr El-Sheikh city. The obtained results revealed that the pH values of plain and fruit yoghurt were significantly higher than those of plain and fruit rayeb. Staphylococcus aureus counts were 4.33×102 ± 0.42×102 and 4.0×102 ±0.57×102cfu/g, in fruit yoghurt and plain rayeb, respectively. Only two samples of plain yoghurt and fruit rayeb contained S.aureus with counts of 9.0x 102±1.0×102 and 1.1×103± 0.1×103cfu/g, respectively. Coliforms were only detected in plain and fruit yoghurt with counts of 8.82×104 ± 0.81×104 and 5.4×10 ± 1.04×10 cfu/g, respectively. E.coli was isolated from plain and fruit yoghurt with incidence rates of 73.3 and 6.7%, respectively. All E.coli isolates from plain yoghurt were serologically identified as, O91: H21, O26: H11, O121: H7, O163: H2, O114: H4, O128: H2 O111: H2, and O86. Fruit yoghurt had only O111:H2. Yeast and molds were also found in the four dairy products with high frequencies for Penicillium species.The two virulence genes, enterotoxin gene A and Shiga toxins 2, were detected in three isolates of S. aureus and E. coli by multiplex PCR. With these results, we could conclude that yoghurt and rayeb samples collected from Kafr El-Sheikh city supermarkets create a health threat to consumers. Therefore, the application of hygienic measures and sanitary practicesis necessary to produce high-quality fermented products to assure consumer’s safety.

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Abdel Hameed, K. G. 2011. Evaluation of chemical and microbiological quality of raw goat milk in Qena province Assiut Vet. Med. J. 57 (129):131-144.
AbdEllatif, S.S., Magdy, S.E., Ali, A. B. and Mohamed, A.B. 2016. Studies on beneficial yeasts isolated from some Egyptian dairy products. Zagazig Veterinary Journal Volume 44 (1): 75-84.
Abrar, M., Anjum, F.R., Zahoor, T., Rahman S.U., Hussain, S., Ahmad S. 2009. Chemical and sensory characteristics of yoghurt prepared by locally isolated and commercially imported starter cultures. Milchwissenschaft. 64(4): 392-395.
Allam SA, Mostafa NY, Kirrella GAK, Eleiwa NZ, EL-Magd MA. 2019. Molecular detection of inva and hila virulent genes in salmonella serovars isolated from fresh water fish. Slov Vet Res,56:693-698.
Altalhi, A.D., Hassan, S.A. 2009. Bacterial quality of raw milk investigated by Escherichia coli and isolates analysis for specific virulence-gene markers. Food Control,20:913-7.
Amer, A.R. 2017. Sanitary evaluation of milk and its products serving at general hospitals. Ph.D. Thesis, Fac. Vet. Med. Alexandria University. American Public Health Association (APHA) (2004):Standard Methods for the Examination of Dairy Products 17th Edition. Edited by H. Michael Wehr and Joseph H. Frank, Washington, D.C., USA.
Anjum, M.F., Lucchini, S., Thompson, A., Hinton, J.C.D., Woodward, M.J. 2003. Comparative genomic indexing reveals the phylogenomics of Escherichia coli pathogens. Infect. Immun. 71:4674-4683.
Anvari, S.H., Sattari, M.. Forozandehe Moghadam, M., NajarPeerayeh, S.H., ImaneeFouladi, A.A. 2008. Detection of Staph. aureus enterotoxins A to D from clinical samples by PCR. Research J. of Bio. Sci. 3(8):826-829.
Argudin M.A., Mendoza M.C., Rodicio M.R. 2010. Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2: 1751-1773.
Arnott, D.R., Duitschaever, C.L. and Bullock, D.H. 1974. Microbiological evaluation of yoghurt produced commercially in Ontario. J. Milk Food Technol., 37(1): 11-13.
Atef, N., Mohamed I., Al-Shimaa A.S., Abdel-Rahman A-M. 2017. Molecular Characterization of Pathogenic E. coli and Staphylococcus Aureus Isolated from Some Fermented Milk Products by Using PCR. Alexandria Journal of Veterinary Sciences, 54: 127-134.
Bachir, R.G., Benattouche, Z. 2013. Evaluation of the quality of steamed yogurt treated by Lavandula and Chamaemelum species essential oils. Global Sci. Res. J., 1 (1), pp. 053-058.
Bailey, W.R. and Scott, E.G. 1998. Diagnostic Microbiology. A textbook for the Isolation and Identification of Pathogenic Microorganisms. The C.V. Mosby Company Saint Louis.
Barakat, S.M. 2019. Mycological evaluation of serving some dairy products with special reference to aflatoxin production in student hostel at faculty of vet. Med. Alexandria University, Edfina. M. V. Sc. Thesis, Fac. Vet. Med. Alexandria University.
Benkerroum, M.N. and Tamine, A.Y. (2004): Technology transfer of Moroccan traditional dairy products (Lben, jben and smen) to small industrial scale. Food Microbiology 21: 399-413.
Bettelheim, K.A. 2003. Non-O157 Verotoxin-producing Escherichia coli: a problem, paradox, and paradigm. Exp. Biol. Med. 228:333-344.
Collins, N., Ateba, M.M., Modisane, S., Moneoang, C.C., Bezuidenhout, C. 2010. Antibiotic Resistant S. aureus Isolated from Milk in the Mafikeng Area, North West Province, South Africa. South African Journal of Science, 106:1-6.
De Boer, E., and Heuvelink, A.E. 2000. Methods for the detection and isolation of Shiga toxin producing Escherichia coli. J. Appl. Microbiol. 88,133-43.
Dipineto, L., Santaniello, A., Fontanella, M., Lagos, K., Fioretti, A. and Menna, L.F. 2006. Presence of Shiga toxin-producing Escherichia coli O157:H7 in living layer hens. Letters in Applied Microbiology 43 (2006) 293-295.
El-Ansary, M.A. 2014. Assessment of Microbiological Quality of Yoghurt Sold in El-Behera Governorate. Alexandria Journal of Veterinary Sciences, 43: 52-57.
El-Baz, A.H. 2019. Prevalence, Molecular Characterization and Antimicrobial Resistance of Vero Toxigenic E.coli in Fresh Soft Cheese, Ice Cream and Yoghurt in Mansoura City. Alexandria Journal of Veterinary Sciences, 62(1): 38-46.
El-Leboudy, A.A., Amer A.A., El-Ansary M.A., El Asuoty, M.S., Marwa, R.A. 2017. Evaluation of some fermented milks sold in Alexandria city. Assiut Vet. Med. J. 63 (154):59-66.
Fleet, G.H. and Mian, M. 1987. The occurrence and growth of yeasts in dairy products. International Journal of Food Microbiology, 4(2): 145-155.
EOSQC (2005) Egyptian Organization for Standardization and Quality Control. Egyptian Standards (E.S.): “Domiati cheese 1008-3/ Kareish cheese1008-4/ Ice cream 1185-1/ Yoghurt 1633”.
Heaton J.C. and Jones, K., 2008. Microbial contamination of fruit, vegetables, and the behavior of enteropathogens in the phyllosphere: a review. J. Appl. Microbiol., 104 (3): 613-626.
Hervert, C.J., Martin, N. H., Boor, K.J., and Wiedmann, M. 2017. Survival and detection of coliforms, Enterobacteriaceae, and gram-negative bacteria in Greek yogurt. J. Dairy Sci. 100:950-960.
Huang, S., Weng, Y., Chiou, R. 2001. Survival of Staphylococcus aureus and Escherichia coli as Affected by Ethanol and NaCl. Journal of Food Protection, 64:546-550.
Hussain, K.I.S. 2010. Microorganisms involved in (Roub) traditional fermented milk in Sudan. M. Sc. Thesis, University of Khartoum, Sudan. Kavas, G., Kinik, O., Uysal, H., Kilic, S., Celikel, N. 2006. Characterization of yeasts Isolated from artisanal Turjish dairy products. Int. J. Dairy
Sci., 1: 44-50.
Khan, K.R., Khan, S.U., Anwar, M.A., Bhadar, F.S. 2008. Physical and chemical quality appraisal of commercial yoghurt brands sold at Lahore. ARPN. Journal of agricultural and biological science 3(3):14-24.
Kok, T., Worswich, D., Gowans, E. 1996. Some serological techniques for microbial and viral infections. In Practical Medical Microbiology (Collee, J.; Fraser, A.; Marmion, B. and Simmons, A., eds.), 14th ed., Edinburgh, Churchill Livingstone, UK.
Kuyucuoglu, Y., Kenar, B., Konak, S., Gurler, Z., &Acaroz, U. (2012). Antibacterial Resistance of Commensal E-coli and E-coli O157: H7 Strains Isolated from Cattle and Calves Faeces Samples. Journal of Animal and Veterinary Advances, 11(1), 52-55.
Lourens-Hattingh, A. and Viljoen, B. 2001. Growth and survival of a probiotic yeast in dairy products. Food Research International, 34(9): 791-796.
MacFaddin J.F. 2000. Biochemical Tests for Identification of Medical Bacteria, 3rd ed. Philadelphia: Lippicott Williams and Wilkins, 2000.
Mbaeyi-Nwaoha, I.E. and Egbuche, N.I., 2012. Microbiological evaluation of sachet water and street vended yoghurt and Zobo drinks sold in Nsukka Metropolis. Int. J. Biol. Chem. Sci., 6(4): 1703-1717.
Mehrotra, M.; WANG, G. and, Johnson, W.M. 2000. Multiplex PCR for Detection of Genes for Staphylococcus aureus Enterotoxins, Exfoliative Toxins, Toxic Shock Syndrome Toxin 1, and Methicillin Resistance. JOURNAL OF CLINICAL MICROBIOLOGY.Vol. 38, No. 3.
Mohamed Eman, F. and MazyedEbtesam, M. 2015. Incidence of Staphylococcus aureus and its enterotoxins in yoghurt Benha Veterinary Medical Journal, 28 (2):107-114.
Neven A., Mohamed I., Al-Shimaa A. S., Abdel-Rahman Abdel-Mageed 2017. Molecular Characterization of Pathogenic E. Coli and Staphylococcus Aureus Isolated from Some Fermented Milk Products by Using PCR. Alexandria Journal of Veterinary Sciences, 54: 127-134.
Omokaro, O. and Telema, B.B. 2014. Microorganisms associated with street vended yoghurt in mile 1 Diobu area of Port Harcourt, Nigeria. e-Journal of Science & Technology (e-JST), 5(9):179-186.
Osman, O.M.M. 2015. Quality evaluation of some fermented milk sold at local market. Ph.D. thesis, Fac. Vet. Med. Alexandria University, Egypt. Oyeleke, S.B. 2009. Microbial assessment of some commercially prepared yogurt retailed in Minna, Niger State. Afr. J. Microbiol. Res. 3: 245-248.
Paton JC, Paton AW. 1998. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11:450-479.
Pearce MC, Evans J, McKendrick IJ, Smith AW, Knight HI, Mellor DJ, Woolhouse MEJ, Gunn GJ, Low JC. 2006. Prevalence and virulence factors of Escherichia coli serogroups O26, O103, O111, and O145 shed by cattle in Scotland. Appl. Environ. Microbiol. 72:653-659.
Pitt, J.I. and Hocking, A.D. 2009. Fungi and Food spoilage (3rd Ed.). Springer Science + Business Media, LLC, 233 Spring Street, New York, NY 10013, USA.
Presscott, L.M., Harley, J.P. and Klein, D.A. 2012. Textbook of Microbiology. Brown Publishers. 5th ed: 441-442.
Raper, K.B. and Fennell, D.I. 1965. The genus Aspergillus.1st Ed. Williams and Wilkins Company, Baltimore.
Raper, K.B. and Thom, C. 1969. A manual of the penicillia, Williams and Wilkins Company, Baltimor.
Salvatierra, M., Molina, A., GamboaMdel, M., Arias, M. 2004. Evaluation of the Effect of Probiotic Cultures on Two Different Yoghurt Brands over a Known Population of Staphylococcus aureus and the Production of Thermonuclease. ArchivosLatinoamericanos de Nutrición, 54:298-302.
Sambrook, J., Fritscgh, E.F., and Mentiates 1989. Molecular cloning. A laboratory manual.Vol !., Cold spring Harbor Laboratory press, New York.
Samet-Bali, O. and Attia, H. (2012): Characterization of typical Tunisian fermented milk, rayeb. African Journal of Biotechnology 11(25): 6744-6749.
Samet-Bali, O., Felfoul, I., Lajnaf, R., Attia, H. and Ayadi, M. A. (2016): Hygienic quality of “Rayeb”, a traditional Tunisian fermented cow’s milk. International Food Research Journal 23(1): 366-369.
Samson, R.A. 1979. A complication of Aspergilli. Studies in Mycology 3: 198-202.
Samson, R.A., Stalk, A. and Hadlok, R. 1976. Revision on the subsection subsectionfasiculata of Penicillium and some alliedspecies. Studies in Mycology 2: 75-78.
Singh, P. and Prakash, A. 2008. Isolation of Escherichia coli, Staphylococcus aureus and Listeria monocytogenes from milk products sold under market conditions at Agra Region. Acta Agri. Slov., 92(1): 83-88.
Tyler, J.S.; Livny, J.; Friedman, D.I. 2005. Lambdoid Phages and Shiga Toxin. In Phages: Their Role in Bacterial Pathogenesis and Biotechnology; Waldor, M.K., Friedman, D.I., Adhya, S.L., Eds.; ASM Press: Washington, DC, USA, 2005; pp. 131-164.
Uccello, M., Malaguarnera, G., Basile, F., D’agata, V., Malaguarnera, M., Bertino, G., Vacante, M., Drago, F. and Biondi, A. (2012): Potential role of probiotics on colorectal cancer prevention. BMC Surgery 12:45-49.
Vanbelkum, A. 2003. Molecular diagnostics in medical microbiology: Yesterday, today and tomorrow. Curr. Opin. Pharmacol., 3(5): 497-501.
Verma, J. K., Greene, K. D., Relter, M. E., Trother, J. and Nowickiki, S. F. 1999. An outbreak of Escherichia coli infection following exposure to contaminated food. JANA: 290- 2178.
Vilchez, S., Reyes, D., Paniagua, M., Bucardo, F., Möllby, R., Weintraub, A. 2009. Prevalence of diarrhoeagenic Escherichia coli in children from León, Nicaragua. J. Med. Microbiol., 58:630-7.
Virpari, P.K., Nayak, J.B., Brahmbhatt, M.N., Thaker, H.C. 2013. Study on isolation, molecular detection of virulence gene and antibiotic sensitivity pattern of Escherichia coli isolated from milk and milk products. Vet world, 41-545.
Weerasekara, M., Karunarathne, R., Gamika, A. 2010. Assessment of quality parameters in North Central province. Wayamba Journal of Animal Science. 578: 26-29.
Yabaya, A. and Idris, A. 2012. Bacteriological quality assessment of some yoghurt brands sold in kaduna metropolis. Jorind10 (2): 35-39.
Zouharova, M. and Rysanek, D. 2008. Multiplex PCR and RPLA Identification of Staphylococcus aureus Strains from Bulk Tank Milk. Zoonoses Public Health, 55: 313-319.
Zycha, H., Siepman, R., Linnemann, G. 1969. Mucorales Eine Besebreibung alter Gattunger und Artendiesserpilzgruppever lag Von. J. Carmer.