Monitoring of <i>Escherichia coli</i>, <i>Salmonella</i> spp. and Staphylococci in Poultry Meat-Based Fast Food in Saudi Arabia — Oak Academic Publishing
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Monitoring of <i>Escherichia coli</i>, <i>Salmonella</i> spp. and Staphylococci in Poultry Meat-Based Fast Food in Saudi Arabia
Department of Microbiology, College of Veterinary Medicine, King Faisal University, Al-Ahsa, Saudi Arabia
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Department of Microbiology, College of Veterinary Medicine, King Faisal University, Al-Ahsa, Saudi Arabia
1 Department of Microbiology, College of Veterinary Medicine, King Faisal University, Al-Ahsa, Saudi Arabia
2 Department of Microbiology, College of Veterinary Medicine, King Faisal University, Al-Ahsa, Saudi Arabia
An investigation was made to survey the possible presence of Staphylococcus aureus , Escherichia coli and Salmonella spp. from fast-food shops in Al-Ahsa Province, Kingdom of Saudi Arabia (KSA), as potential reservoir of human infection and antimicrobial resistance. A total of 100 samples of shawarma poultry meat were collected from different localities of the province. Conventional, commercial VITEK 2 and molecular techniques were used for isolates’ identification and antibiogram detection. Staph aureus was isolated at a rate of 14% and CNS as Staph. sciuri and Staph. xylosus at 2%. E. coli was identified at a rate of 12% and antibiogram analysis showed 41.67% of isolates to be extended-spectrum β -lactamases (ESBL) with evidence of multi-drug resistance (MDR). Molecular analysis of E. coli revealed presence of sero-groups O1 and O2, entero-toxigenic (ETEC), shiga-toxigenic, ST540 and the prototypical ETEC strain H10407 which are potential public health hazard. Salmonella enterica serovar Enteritidis showed 19% prevalence while S. Typhimurium with 8% prevalence. Anti-microbial sensitivity of 15 strains of S. Enteritidis and 5 strains of S. Typhimurium showed multi-drug resistance (MDR).
Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., et al. (2011) Foodborne Illness Acquired in the United States Major Pathogens. Emerging Infectious Diseases, 17, 7-15. https://doi.org/10.3201/eid1701.P11101
Zhao, X., Lin, C.W., Wang, J. and Oh, D.H. (2014) Advances in Rapid Detection Methods for Foodborne Pathogens. Journal of Microbiology and Biotechnology, 24, 297-312. https://doi.org/10.4014/jmb.1310.10013
Lee, N., Kwon, K.Y., Oh, S.K., Chang, H.J., Chun, H.S. and Choi, S.W. (2014) A Multiplex PCR Assay for Simultaneous Detection of Escherichia coli O157:H7, Bacillus cereus, Vibrio parahaemolyticus, Salmonella spp., Listeria monocytogenes, and Staphylococcus aureus in Korea Ready-to-Eat Food. Foodborne Pathogens and Disease, 11, 574-580. https://doi.org/10.1089/fpd.2013.1638
Kloos, W.E. and Bannerman, T.L. (1994) Update on Clinical Significance of Coagulase-Negative Staphylococci. Clinical Microbiology Reviews, 7, 117-140. https://doi.org/10.1128/CMR.7.1.117
Horii, T., Suzuki, Y., Kimura, T., Kanno, T. and Maekawa, M. (2001) Intravenous Catheter Related Septic Shock Caused by Staphylococcus sciuri and Escherichia vulneris. Scandinavian Journal of Infectious Diseases, 33, 930-932. https://doi.org/10.1080/00365540110076750
Stepanovic, S., Jezek, P., Vukovic, D., Dakic, I., Petras, P., et al. (2003) Isolation of Members of the Staphylococcus sciuri Group from Urine and Their Relationship to Urinary Tract Infections. Journal of Clinical Microbiology, 41, 5262-5264. https://doi.org/10.1128/JCM.41.11.5262-5264.2003
Molbak, K., Olsen, J. and Wegener, H. (2006) Salmonella Infections. In: Reimann, H. and Cliver, D., Eds., Foodborne Infections and Intoxications, Academic Press, Cambridge, 55-115. https://doi.org/10.1016/B978-012588365-8/50007-4
Anjay, A.K., Agarwal, R.K., Ramees, T.P., Dubal, Z.B., Kaushik, P., Kumar, M.S., Dudhe, N.C., Milton, A.A.P., Abhishek, B.K. and Shagufta, B. (2015) Molecular Typing of Salmonella typhimurium and S. enteritidis Serovars from Diverse Origin by ERIC-PCR. Journal of Pure and Applied Microbiology, 9, 2627-2634.
Soultose, N., Koidis, P. and Madden, R.H. (2003) Prevalence of Listeria and Salmonellae in Retail Chicken in Northern Ireland. Applied Microbiology, 37, 421-423. https://doi.org/10.1046/j.1472-765X.2003.01423.x
Carraminana, J.J., Agustin, I. and Herrera, A. (2004) High Prevalence of Multiple Resistance to Antibiotics in Salmonellae Serovars Isolated from a Poultry Slaughterhouse in Spain. Veterinary Microbiology, 104, 133-139. https://doi.org/10.1016/j.vetmic.2004.08.010
Bailey, J.S. and Cosby, D.E. (2003) Detection of Salmonellae from Chicken Rinses and Chicken Hot Dogs with Automated Bax PCR System. Journal of Food Protection, 66, 2138-2140. https://doi.org/10.4315/0362-028X-66.11.2138
Kimura, A.C., Reddy, V. and Marcus, R. (2004) Chicken Consumption Is a Newly Identified Risk Factor for Sporadic Salmonellae Enteric Serotype Enteritidis Infections in the United States. Clinical Infectious Diseases, 38, 244-252. https://doi.org/10.1086/381576
Singer, R.S. (2015) Urinary Tract Infections Attributed to Diverse ExPEC Strains in Food Animals: Evidence and Data Gaps. Frontiers in Microbiology, 6, Article No. 28. https://doi.org/10.3389/fmicb.2015.00028
Oloso, N.O., Fagbo, S., Garbati, M., et al. (2018) Antimicrobial Resistance in Food Animals and the Environment in Nigeria: A Review. International Journal of Environmental Research and Public Health, 15, 1284. https://doi.org/10.3390/ijerph15061284
Huber, L., Gow, S.P., Carson, C.A., et al. (2021) Reduction in Antimicrobial Use and Resistance to Salmonella, Campylobacter, and Escherichia coli in Broiler Chickens, Canada, 2013-2019. Emerging Infectious Diseases, 27, 2434-2444. https://doi.org/10.3201/eid2709.204395
Koutsoumanis, K., Allende, A., álvarez-Ordóñez, A., et al. (2021) Role Played by the Environment in the Emergence and Spread of Antimicrobial Resistance (AMR) through the Food Chain. EFSA Journal, 19, e06651. https://doi.org/10.2903/j.efsa.2021.6651
Clothier, K.A., Kim, P., Mete, A., et al. (2018) Frequency, Serotype Distribution, and Antimicrobial Susceptibility Patterns of Salmonella in Small Poultry Flocks in California. Journal of Veterinary Diagnostic Investigation, 30, 471-475. https://doi.org/10.1177/1040638718755418
Herrera-Sánchez, M.P., Rodríguez-Hernández, R., et al. (2020) Antibiotic Resistance in Salmonella spp. Isolated from Poultry: A Global Overview. Veterinary World, 13, 2070-2084. https://doi.org/10.14202/vetworld.2020.2070-2084
Luo, W., Chen, D., Wu, M., et al. (2019) Pharmacokinetics/Pharmacodynamics Models of Veterinary Antimicrobial Agents. Journal of Veterinary Science, 20, e40. https://doi.org/10.4142/jvs.2019.20.e40
Hathcock, T., Butaye, P., Kang, Y., et al. (2019) Multidrug-Resistant Escherichia coli, Klebsiella pneumoniae and Staphylococcus spp. in Houseflies and Blowflies from Farms and Their Environmental Settings. International Journal of Environmental Research and Public Health, 16, 3583. https://doi.org/10.3390/ijerph16193583
Koutsoumanis, K., Allende, A., Alvarez-Ordóñez, A., et al. (2019) Salmonella Control in Poultry Flocks and Its Public Health Impact. EFSA Journal, 17, e05596. https://doi.org/10.2903/j.efsa.2019.5596
Gowda, T.K.G.M., Latha, C., Sunil, B. and Van Damme, I. (2017) Occurrence and Antibiotic Susceptibility of Listeria Species and Staphylococcus aureus in Cattle Slaughterhouses of Kerala, South India. Foodborne Pathogens and Disease, 14, 573-579. https://doi.org/10.1089/fpd.2017.2293
Khambaty, F.M., Bennett, R.W. and Shah, D.B. (1994) Application of Pulse Field Gel Electrophoresis to the Epidemiological Characterisation of Staphylococcus intermedius Implicated in a Food-Related Outbreak. Epidemiology and Infection, 113, 75-81. https://doi.org/10.1017/S0950268800051487
Okoli, C.E., Njoga, E.O., Enem, S.I., Godwin, E.E., Nwanta, J.A. and Chah, K.F. (2018) Prevalence, Toxigenic Potential and Antimicrobial Susceptibility Profile of Staphylococcus Isolated from Ready-to-Eat Meats. Veterinary World, 11, 1214-1221. https://doi.org/10.14202/vetworld.2018.1214-1221
Pyzik, E., Marek, A., Stępień-Pyśniak, D., Urban-Chmiel, R., Jarosz, Ł.S. and Jagiełło-Podębska, I. (2019) Detection of Antibiotic Resistance and Classical Enterotoxin Genes in Coagulase-Negative Staphylococci Isolated from Poultry in Poland. Journal of Veterinary Research, 63, 183-190. https://doi.org/10.2478/jvetres-2019-0023
Shittu, A., Lin, J., Morrison, D. and Kolawole, D. (2004) Isolation and Molecular Characterization of Multiresistant Staphylococcus sciuri and Staphylococcus haemolyticus Associated with Skin and Soft-Tissue Infections. Journal of Medical Microbiology, 53, 51-55. https://doi.org/10.1099/jmm.0.05294-0
Sato, T., Usui, M., Konishi, N., et al. (2017) Closely Related Methicillin-Resistant Staphylococcus aureus Isolates from Retail Meat, Cows with Mastitis, and Humans in Japan. PLoS ONE, 12, e0187319. https://doi.org/10.1371/journal.pone.0187319
Bush, K. and Jacoby, G.A. (2010) Updated Functional Classification of β-Lactamases. Antimicrobial Agents and Chemotherapy, 54, 969-976. https://doi.org/10.1128/AAC.01009-09
Momtaz, H., Rahimi, E. and Moshkelani, S. (2012) Molecular Detection of Antimicrobial Resistance Genes in E. coli Isolated from Slaughtered Commercial Chickens in Iran. Veterinarni Medicina, 57, 193-197. https://doi.org/10.17221/5916-VETMED
Apostolakos, I., Mughini-Gras, L., Fasolato, L. and Piccirillo, A. (2019) Assessing the Occurrence and Transfer Dynamics of ESBL/pAmpC-Producing Escherichia coli across the Broiler Production Pyramid. PLoS ONE, 14, e0217174. https://doi.org/10.1371/journal.pone.0217174
Kawamura, K., Nagano, N., Suzuki, M., Wachino, J., Kimura, K. and Arakawa, Y. (2017) ESBL-Producing Escherichia coli and Its Rapid Rise among Healthy People. Food Safety (Tokyo), 5, 122-150. https://doi.org/10.14252/foodsafetyfscj.2017011
Nahar, A., Awasthi, S.P., Hatanaka, N., Okuno, K., Hoang, P.H., Hassan, J., Hinenoya, A. and Yamasaki, S. (2018) Prevalence and Characteristics of Extended-Spectrum β-Lactamase-Producing Escherichia coli in Domestic and Imported Chicken Meats in Japan. The Journal of Veterinary Medical Science, 80, 510-517. https://doi.org/10.1292/jvms.17-0708
Apostolakos, I., Feudi, C., Eichhorn, I., Palmieri, N., Fasolato, L., Schwarz, S. and Piccirillo, A. (2020) High-Resolution Characterisation of ESBL/pAmpC-Producing Escherichia coli Isolated from the Broiler Production Pyramid. Scientific Reports, 10, Article No. 11123. https://doi.org/10.1038/s41598-020-68036-9
Delannoy, S., Beutin, L., Mariani-Kurkdjian, P., Fleiss, A., Bonacorsi, S. and Fach, P. (2017) The Escherichia coli Serogroup O1 and O2 Lipopolysaccharides Are Encoded by Multiple O-antigen Gene Clusters. Frontiers in Cellular and Infection Microbiology, 7, 30. https://doi.org/10.3389/fcimb.2017.00030
Joya, J.E., Suji, T.T., Jacalne, A.V., Arita, M., Sukamoto, T.T., Honda, T. and Miwatani, T. (1990) Demonstration of Enterotoxigenic Escherichia coli in Diarrheic Broiler Chicks. European Journal of Epidemiology, 6, 88-90. https://doi.org/10.1007/BF00155557
Crofts, A.A., Simone, M., Giovanetti, E.J., Rubin, F.M., et al. (2018) Enterotoxigenic E. coli Virulence Gene Regulation in Human Infections. PNAS, 115, E8968-E8976. https://doi.org/10.1073/pnas.1808982115
Hugas, M. and Beloeil, P. (2014) Controlling Salmonella along the Food Chain in the European Union—Progress over the Last Ten Years. Eurosurveillance, 19, 20804. https://doi.org/10.2807/1560-7917.ES2014.19.19.20804
Cosby, D.E., Cox, N.A., Harrison, M.A., Wilson, J.L., Buhr, R.J. and Fedorka-Cray, P.J. (2015) Salmonella and Antimicrobial Resistance in Broilers: A Review. Journal of Applied Poultry Research, 24, 408-426. https://doi.org/10.3382/japr/pfv038
EFSA European Food Safety Authority (2015) The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Foodborne Outbreaks in 2013. EFSA Journal, 13, 165. https://doi.org/10.2903/j.efsa.2015.3991
Scallan, E., Griffin, P.M., Angulo, F.J., Tauxe, R.V. and Hoekstra, R.M. (2011) Foodborne Illness Acquired in the United States-Unspecified Agents. Emerging Infectious Diseases, 17, 16-22. https://doi.org/10.3201/eid1701.P21101
Harakeh, S., Yassine, H., Gharios, M., et al. (2005) Isolation, Molecular Characterization and Antimicrobial Resistance Patterns of Salmonella and Escherichia coli Isolates from Meat-Based Fast Food in Lebanon. Science of the Total Environment, 341, 33-44. https://doi.org/10.1016/j.scitotenv.2004.09.025
Karp, B.E., Tate, H., Plumblee, J.R., et al. (2017) National Antimicrobial Resistance Monitoring System: Two Decades of Advancing Public Health Through Integrated Surveillance of Antimicrobial Resistance. Foodborne Pathogens and Disease, 14, 545-557. https://doi.org/10.1089/fpd.2017.2283