Assessment of the Chemical and Microbiological Quality of Some Cheese Assortment in Egypt: Highlighting the incidence of multidrug-resistant Staphylococcus Species | ||||
| Journal of Applied Veterinary Sciences | ||||
| Article 9, Volume 9, Issue 1, January 2024, Page 85-93 PDF (687.27 K) | ||||
| Document Type: Original Article | ||||
| DOI: 10.21608/javs.2023.243014.1285 | ||||
 View on SCiNiTO | ||||
| Authors | ||||
Mostafa A. Shawki 1; Eman F. Abdel-Latif 2; Samah F. Darwish3; Adel M. Saudi2; Zeinab I. Ali  2
| ||||
| 1Senior Food Safety Consultant (Preverisk) 5124 El Meraag, El Maadi, Cairo, 11742, Egypt | ||||
| 2Department of Food Hygiene and Control, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt | ||||
| 3Biotechnology Research Unit, Animal Reproduction Research Institute (ARRI), Agricultural Research Center (ARC), Giza, 12556, Egypt | ||||
| Abstract | ||||
| Hard and semi-hard cheeses are popular dairy products in Egypt, but they may convey a health risk for consumers due to their poor hygienic quality and safety. One of the common problems that consumers face when buying these cheeses from the Egyptian market is the bad odour that shortly develops after purchase even though they are refrigerated. This problem may indicate a high bacterial count in the cheese or the presence of undesirable microorganisms. Therefore, the current study aimed to assess the hygienic quality and safety of some retailed cheese sold in Egyptian markets. One hundred hard and semi-hard cheese samples locally manufactured (including 34 Ras, 33 Cheddar, and 33 Gouda) were analyzed for their microbiological and chemical quality. The results indicated that the Ras cheese samples had the highest bacterial counts, salt, and fat content, while the Cheddar cheese samples had the highest acidity, moisture content and the lowest microbial load. The Gouda cheese samples had the lowest fat/total solids ratio and a variable bacterial count. Forty-five Staphylococcus aureus strains were isolated from the cheese samples; 25 of them were coagulase-positive. The antibiotic susceptibility of twenty isolates was phenotypically and genotypically evaluated. All isolates were resistant to Cefixime, Oxacillin, and Metronidazole, while sensitive to Amoxicillin/Clavulanic Acid and Linezolid. The resistance to other antibiotics varied among the isolates. The antibiotic resistance genes were detected by polymerase chain reaction (PCR). The obtained results indicate that the hard and semi-hard cheeses sold in many markets were poor in hygienic quality and safety and posed a health risk for consumers due to the presence of multidrug-resistant Staphylococcus species. Ras cheese was the worst cheese type in most quality and safety parameters. | ||||
| Keywords | ||||
| Antibiotic resistance genes; Cheddar; Gouda; Ras; Staphylococcus | ||||
| References | ||||
|
ABBAS, A., SRIVASTAVA, P., NIRWAN, P. S. J. J. O. C., and JCDR, D. R., 2015. Prevalence of MLSB resistance and observation of erm A and erm C genes at A tertiary care hospital. J. Clin Diagn Res. 9, DC08. https://doi.org/10.7860/jcdr/2015/13584.6112 AHLAM, A., AMER, A. A., and YOUSSEF, M. R., 2014. Assessment of sanitary measures of ras cheese in manufacturing dairy plant in Alexandria governorate. Alexandria Journal of Veterinary Sciences 40 (1):87-94. https://doi.org/10.5455/ajvs.48184 ALI, Z. I., HANAFY, M., HANSEN, C., SAUDI, A. M., and TALAAT, A. M., 2021. Genotypic analysis of nontuberculous mycobacteria isolated from raw milk and human cases in Wisconsin. Journal of Dairy Science, 104, 211-220. https://doi.org/10.3168/jds.2020-18214. AMER, D. A., ALBADRI, A. A. M., EL-HAMSHARY, H. A., NEHELA, Y., MAKHLOUF, A. H., EL-HAWARY, M. Y., and AWAD, S. A., 2023. Changes in Sensory Properties, Physico-Chemical Characteristics, and Aromas of Ras Cheese under Different Coating Techniques. Foods, 12. https://doi.org/10.3390/foods12102023 A.P.H.A., 2004. Standard methods for the examination of dairy products, American Public Health Association https://doi.org/10.2105/9780875530024 ASFOUR, H. A., and DARWISH, S. F., 2014. Evaluation of phenotypic methods versus molecular methods for differentiation of Coagulase positive staphylococci causing bovine mastitis with a special reference to atypical Staphylococcus Aureus Int.J.Curr.Microbiol.App.Sci. 3, 543-58. BENDAHOU, A., LEBBADI, M., ENNANEI, L., ESSADQUI, F. Z., and ABID, M. J. T. J. O. I. I. D. C., 2008. Characterization of Staphylococcus species isolated from raw milk and milk products (lben and jben) in North Morocco. . J. Infect Dev Ctries. 2, 218-225 https://doi.org/10.3855/jidc.266 BERHILEVYCH, O. М., KASIANCHUK, V. V., KUKHTYN, M. D., LOTSKIN, I. М., GARKAVENKO, T. O. and SHUBIN, P. A. 2017. Characteristics of antibiotic sensitivity of Staphylococcus aureus isolated from dairy farms in Ukraine. Regulatory Mechanisms in Biosystems, 8, 559-563. https://doi.org/10.15421/021786 D’AMICO, D., and DONNELLY, C. J., 2010. Microbiological quality of raw milk used for small-scale artisan cheese production in Vermont: effect of farm characteristics and practices. Journal of Dairy Science 93, 134-147. https://doi.org/10.3168/jds.2009-2426 DARWISH, S. F., and ASFOUR, H. A., 2013. Investigation of biofilm forming ability in Staphylococci causing bovine mastitis using phenotypic and genotypic assays. ScientificWorldJournal, 2013, 378492. https://doi.org/10.1155/2013/378492 EISSA, A. A. 2012. Structure and function of food engineering, BoD–Books on Demand, https://doi.org/10.5772/1615 ELRAMLY, M., LEBOUDY, A., and ANSARY, M., 2019. Mycological Evaluation of Egyptian Ras Cheese with Special Reference to Mycotoxins. Alexandria Journal of Veterinary Sciences, 63. https://doi.org/10.5455/ajvs.58688 ES:1007-2/2020 (Egyptian standards), 2020. Hard cheese - part 2 - Cheddar cheese. Egyptian Organization for Standardization., ES:1007-5/2005 (Egyptian standards), 2005. Hard cheese - part 5 - Ras cheese. Egyptian Organization for Standardization., ES:1183-1/2020 (Egyptian standards), 2020. Semi-Hard cheese - part 1 - Gouda cheese. Egyptian Organization for Standardization., FERRI, M., RANUCCI, E., ROMAGNOLI, P., and GIACCONE, V., 2017. Antimicrobial resistance: A global emerging threat to public health systems. Crit Rev Food Sci Nutr. J. 57, 2857-2876. https://doi.org/10.1080/10408398.2015.1077192 FOX, P. F., GUINEE, T. P., COGAN, T. M., and MCSWEENEY, P. L. 2017. Fundamentals of cheese science, Springer, https://doi.org/10.1007/978-1-4899-7681-9 FOX, P. F., MCSWEENEY, P. L., COGAN, T. M., and GUINEE, T. P., 2004. Cheese: Chemistry, physics and microbiology, Volume 1: General aspects, Elsevier, https://doi.org/10.1016/s1874-558x(04)80060-5 GUINEE, T. 2004. Salting and the role of salt in cheese. International Journal of Dairy Technology. 57, 99-109. https://doi.org/10.1111/j.1471-0307.2004.00145.x HABLIZA, R., ABD ELHAMID, A., SHAMSIA, S., SALAMA, W., and AWAD, S., 2022. Production of Ras Cheese Analogue by Partially or Totally Substitution of Milk Fat with Palm Oil. Alexandria Science Exchange Journal, 43, 343-352. https://doi.org/10.21608/asejaiqjsae.2022.248650 HEGAB, O. W., ABDEL-LATIF, E. F., and MOAWAD, A. A., 2020. Isolation of enterotoxigenic Staphylococcus aureus harboring seb gene and enteropathogenic Escherichia coli (serogroups O18, O114, and O125) from soft and hard artisanal cheeses in Egypt. Open Vet J, 10, 297-307. https://doi.org/10.4314/ovj.v10i3.8 HELAL, A., and TAGLIAZUCCHI, D., 2023. Peptidomics Profile, Bioactive Peptides Identification and Biological Activities of Six Different Cheese Varieties. Biology J. 12, 78. https://doi.org/10.3390/biology12010078 AOAC 2020: ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS INTERNATIONAL. SECTIONS. AOAC official methods of analysis. 50, 992.905. LE LOIR, Y., BARON, F., and GAUTIER, M., 2003. Staphylococcus aureus and food poisoning. Genet Mol Res, 2, 63-76. M HASSAN, G., MS MESHREF, A., MA ZEINHOM, M., and S ABDEL-HALEM, M. J. A. V. M. J., 2019. Impact of spoilage microorganisms on some dairy products. Assiut Veterinary Medical Journal 65, 133-141. https://doi.org/10.21608/avmj.2019.168769 MEDVEĎOVá, A., VALíK, Ľ. J. S., and ENGINEERING, F. O. F., 2012. Staphylococcus aureus: Characterisation and quantitative growth description in milk and artisanal raw milk cheese production. Structure and Function of Food Engineering 71-102. https://doi.org/10.5772/48175 MIKKELSEN, P . 2014. World cheese market PM Food and Dairy Consulting, 2000–2020. MONDAY, S. R., and BOHACH, G. A., 1999. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in Staphylococcal isolates. J Clin Microbiol, 37, 3411-4. https://doi.org/10.1128/jcm.37.10.3411-3414.1999 OWUSU-APENTEN, R., and VIEIRA, E., 2022. Dairy Products. In Elementary Food Science (pp. 399-431). Cham: Springer International Publishing. PALUDETTI, L. F., O'CALLAGHAN, T. F., SHEEHAN, J. J., GLEESON, D., and KELLY, A. L., 2020. Effect of Pseudomonas fluorescens proteases on the quality of Cheddar cheese. J Dairy Sci, 103, 7865-7878. https://doi.org/10.3168/jds.2019-18043 QUIGLEY, L., O'SULLIVAN, O., STANTON, C., BERESFORD, T. P., ROSS, R. P., FITZGERALD, G. F., and COTTER, P. D., 2013. The complex microbiota of raw milk. FEMS Microbiol Review J. 37, 664-698. https://doi.org/10.1111/1574-6976.12030 RODRIGUES, D. E. B., DA PAIXãO, L. L., SANTANA, V. R., CARDOZO, R. M. D., and MACHADO, S. G., 2021. Proteolytic potential of psychrotrophic microorganisms isolated from fresh cheese. Revista do Instituto de Laticínios Cândido Tostes, 75, 232-242. https://doi.org/10.14295/2238-6416.v75i4.822 SALAMA, H., AL-SAID, A. A., and EL-ASUOTY, M.S., 2021. The Effect of Haccp System on Various Microbiological Hazards in Cheese Factories. 67, 158-173. Assiut Vet. Med. J. https://doi.org/10.21608/avmj.2021.205280 SHARMA, C., ROKANA, N., CHANDRA, M., SINGH, B. P., GULHANE, R. D., GILL, J. P. S., RAY, P., PUNIYA, A. K., and PANWAR, H., 2017. Antimicrobial Resistance: Its Surveillance, Impact, and Alternative Management Strategies in Dairy Animals. Front Vet Sci, 4, 237. https://doi.org/10.3389/fvets.2017.00237 STROMMENGER, B., KETTLITZ, C., WERNER, G., and WITTE, W., 2003. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol, 41, 4089-94. https://doi.org/10.1128/jcm.41.9.4089-4094.2003 SULIEMAN, A. M. E., OHAG, O. M., HASSAN, H. M., ALRESHIDI, M. M., and VEETTIL, 2018. Some chemical and microbiological characteristics of Gouda cheese. Advances in Bioresearch 9, 1-6. TODARO, A., ADLY, F. A., and OMAR, O. A., 2013. History, processing and quality enhancement of traditional Egyptian Kariesh cheese: a review. Food Science and Technology 1, 1-6. https://doi.org/10.13189/fst.2013.010101 VESTERHOLM-NIELSEN, M., ØLHOLM LARSEN, M., ELMERDAHL OLSEN, J., and MøLLER AARESTRUP, 1999. Forekomst af blaZ genet i penicillinresistente Staphylococcus aureus isoleret fra bovin mastitis i Danmark. Acta vet. scand. 40, 279-286. https://doi.org/10.1186/bf03547026 ZEHRA, A., SINGH, R., KAUR, S., and GILL, J., 2017. Molecular characterization of antibiotic-resistant Staphylococcus aureus from livestock (bovine and swine). Vet World. J. 10, 598. https://doi.org/10.14202/vetworld.2017.598-604 ZHANG, K., MCCLURE, J. A., ELSAYED, S., LOUIE, T., and CONLY, J. M., 2005. Novel multiplex PCR assay for characterization and concomitant subtyping of Staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol, 43, 5026-33. https://doi.org/10.1128/jcm.43.10.5026-5033.2005 | ||||
|
Statistics Article View: 249 PDF Download: 240 |
||||
