PREVALENCE OF ENTEROTOXIGENIC AND MULTI-DRUG-RESISTANT Staphylococcus aureus IN READY TO EAT MEAT SANDWICHES

Alaa Eldin M.A. Morshdy, Mohamed A. Hussein, Ahmed E. Tharwat, Basma A. Fakhry

Abstract


Due to recent spread of multiple drug resistant pathogens, this study was peformed to investigate the presence of multi-drug resistant enterotoxigenic Staphylococcus aureus (S. aureus) in some ready to eat meat products (RTE). For this, one hundred and forty samples of ready to eat meat sandwiches were collected from restaurants and street vendors in Zagazig city, Egypt. Staphylococcus aureus is one of the most important food poisoning bacteria in RTE. The counts were 3.31 ± 0.49, 2.86 ± 0.36, 3.28 ± 0.24, 3.92 ± 0.41, 2.52 ± 0.11, 3.64 ± 0.39 and 3.12 ± 0.35 log10 CFU/g in examined kofta, luncheon, burger, shawarma, hawawshi, liver and sausage sandwiches, respectively. The examined sandwiches were categorized into good (32.1%), acceptable (32.9%), unsatisfactory (26.4%) and potentially hazard (8.6%). About 72.7 % of examined S. aureus strains carry one or more staphylococcal enterotoxin (se) genes and mecA gene detected in 81.8% of coagulase positive S. aureus. The antibiogram showed that 100% of S. aureus isolates were resistant to kanamycin, 92% for penicillin and neomycin, 84% for oxacillin and erythromycin and 68% for ampicillin and nalidixic acid. The average of multi-antibiotic resistant (MAR) index of isolated S. aureus was 0.59. Moreover, five isolates were resistant to all tested antibiotic.

Key words: Staphylococcus aureus; methicillin resistant; enterotoxin; ready to eat

 


Full Text:

PDF

References


Kaneko KI, Hayashidani H, Ohtomo Y, Kosuge J, Kato M, Takahashi K, et al. Bacterial contamination of ready-to-eat foods and fresh products in retail shops and food factories. J Food Prot 1996; 62: 644–9.

Gibbons IS, Adesiyun A, Seepersadsingh N, Rahaman S. Investigation for possible source(s) of contamination of ready-to-eat meat products with Listeria spp. and other pathogens in a meat processing plant in Trinidad. Food Microbiol 2006; 23: 359–66.

Gilbreth SE, Call JE, Wallace FM, Scott VN, Chen Y, Luchansky JB. Relatedness of Listeria monocytogenes isolates recovered from selected ready-to-eat foods and listeriosis patients in the United States. Appl Environ Microbiol 2005; 71: 8115–22.

Angelidis AS, Chronis EN, Papageorgiou DK, Kazakis II, Arsenoglou KC, Stathopoulos GA. Non-lactic acid contaminating flora in ready-to-eat foods A potential food-quality index. Food Microbiol 2006; 23: 95–100.

Colombari V, Mayer MD, Laicini ZM, Mamizuka E, Franco BD, Destro MT. Foodborne outbreak caused by Staphylococcus aureus: Phenotypic and genotypic characterization of stra-ins of food and human sources. J Food Prot 2007; 70: 489–93.

Gundogan N, Ataol O, Torlak FO. Determination of some virulence factors in Staphylococcus aureus, Enterococcus faecalis and Enterococcus Faecium isolated from meat and milk products. Food Saf J 2013; 33: 387–93.

Van TT, Nguyen HN, Smooker PM, Coloe PJ. The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int J Food Microbiol 2012; 154: 98–106.

Sulakvelidze A, Alavidze Z, Glenn Morris J . Bacteriophage Therapy. Antimicrob. Agents Chemother 2001; 45: 649–59.

Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Craig AS. Invasive methicillin-resistant Staphylococcus aureus infecti-ons in the United States. JAMA 2007; 298: 1

–71.

Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, Haesebrouck F. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob agents chemo-ther 2008; 52: 3817–9.

Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL, Aarestrup FM. Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbial 2010; 141: 326–31.

ISO 6888-1.1999 Microbiology of food and animal feeding stuffs -- Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) -- Part 1: Technique using Baird-Parker agar medium.

American Public Health Association APHA. Compendium of Methods for Microbiolo-gical examination of Food. 2001 4th Ed. Washington, DC., USA.

Shah D, Shringi S, Besser T, Call D. Molecular detection of foodborne pathogens, Boca Raton. In: Liu D, eds. Taylor & Francis group: CRC Press , 2009: 369–89.

Rall VLM, Vieira FP, Rall R, Vieitis RL, Fernandes Jr A, Candeias JMG, Araújo Jr JP . PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet Microbial 2008; 132: 408–13.

McClure JA, Conly JM, Lau V, Elsayed S, Louie T, Hutchins W, Zhang K. Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methi-cillin-susceptible from-resistant staphylococci. J Clin Microbiol 2006; 44: 1141–4.‏

Mehrotra M, Wang G, Johnson W. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000; 38: 1032–5.

Deresse D, Solomon G, Dawit Y. Anti-biotic-resistance Staphylococcus aureus isolated from cow’s milk in the Hawassa area, South Ethiopia. Ann Clin Microbiol Antimicrobiol 2012; 11: 26–34.

National Committee for Clinical Laboratory Standards "NCCLS"2001. Performance standards for antimicrobial susceptibility testing. Supplement M100-S11. Villanova, PA, USA.

Singh A, Yadav S, Singh S, Bharti P. Prevalence of Salmonella in chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res Int 2010; 43: 2027–30.

Tambekar DH, Jaiswal VJ, Dhanorkar DV, Gulhane PB, Dudhane MN. Identification of microbiological hazards and safety of ready-to-eat food vended in streets of Amravati City, India. J Appl Biosci 2008; 7: 195–201.

Daelman J, Jacxsens L, Lahou E, Devlieghere F, Uyttendaele M. Assessment of the microbial safety and quality of cooked chilled foods and their production process. Int J Food Microbiol 2013; 160: 193–200.

Fang TJ, Wei QK, Liao CW, Hung MJ, Wang TH. Microbiological quality of 18 C ready-to-eat food products sold in Taiwan. Int J Food Microbiol 2002; 80: 241–50.‏

Ghosh M, Wahi S, Kumar M, Ganguli A. Prevalence of enterotoxigenic Staphylococcus aureus and Shigella spp. in some raw street vended Indian foods. Int J Environ Health Res 2007; 17: 151–6.‏

Food safety regulations in Australia and New Zealand Food Standards. J Sci Food Agric. 2014;94:1970–3.

Bennett SD, Walsh KA, Gould LH. Food borne disease outbreaks caused by Bacillus cereus, Clostridium perfringnes, and Staphylococcus aureus- United States 1998-2008. Clin Infect Dis 2013; 57: 425–33.

Kérouanton A, Hennekinne J A, Letertre C, Petit L, Chesneau O, Brisabois A, De Buyser ML. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol 2007;115: 369–75.

Normanno G, Firinu A, Virgilio S, Mula G, Dambrosio A, Poggiu A, Di Giannatale E . Coagulase-positive Staphylococci and Staphylo-coccus aureus in food products marketed in Italy. Int J Food Microbiol 2005; 98: 73–9.

Pelisser MR, Klein KS, Ascoli K R, Zotti TR, Arisi ACM . Occurrence of Staphylococcus aureus and multi-plex PCR detection of classic enterotoxin genes in cheese and meat products. Braz J Microbiol 2009; 40: 145–8.

Pereira V, Lopes C, Castro A, Silva J, Gibbs P, Teixeira P. Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol 2009; 26: 278–82.

Normanno G, Salandra LG, Dambrosio A, Quaglia NC, Corrente M, Parisi A, Santagada G, Firinu A, Crisetti E, Celano GV. Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol 2007; 115: 290–6.

Kitai S, Shimizu A, Kawano J, Sato E, Nakano C, Uji T, Kitagawa H. Characterization of methicillin-resistant isolated from retail raw chicken meat in Japan. J Vet Med Sci 2005; 67: 107–10.

Kwon NH, Park KT, Jung WK, Youn HY, Lee Y, Kim SH, Bae W, Lim JY, Kim JY, Kim JM, Hong SK, Park YH. Characteristics of methicillin- resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Vet Microbiol 2006; 117: 304–12.

Van Loo IHM, Diederen BMW, Savelkoul PHM, Woudenberg JHC, Roosendaal R, van Belkum A, Lemmens-den Toom N, Verhulst C, van Keulen PHJ, Kluytmans JAJW. Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg Infect Dis 2007;13:

–5.

Sergelidis D, Angelidis AS. Methicillin‐resistant Staphylococcus aureus: a con-troversial food‐borne pathogen. Lett applied microbiol 2017; 64: 409–18.‏

De Boer E, Zwartkruis-Nahuis JT, Wit B, Huijsdens XW, de Neeling AJ, Bosch T, van Oosterom RA, Vila A, Heuvelink AE. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol 2009; 134:52–6.

Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, Foster JT, Bowers J, Driebe EM, Engelthaler DM, Keim PS, Price LB . Multidrug-Resistant Staphylo-coccus aureus in US Meat and Poultry. Clin Infect Dis 2011; 52: 1227–30.

Yurdakul NE, Erginkaya Z, Unal E. Antibiotic resistance of enterococci, coagulase-negative Staphylococci and Staphylococcus aureus isolated from chicken meat. Czech J Food Sci 2013; 1: 14–9.

Robert-Pillot A, Copin S, Himber C, Gay M, Quilici ML. Occurrence of the three major Vibrio species pathogenic for human in seafood products consumed in France using real-time PCR. Int J Food Microbiol 2014; 189: 75–81.

Tanil GB, Radu S, Nishibuchi M, Rahim RA, Napis S, Maurice L, et al. Characterization of Vibrio parahaemolyticus isolated from coastal seawater in peninsular Malaysia. Southeast Asian Journal of Trop Med Public Health 2005; 36:

–5.

Nygård K, Lassen J, Vold L, Andersson Y, Fisher I, Löfdahl S, Threlfall J, Luzzi I, Peters T, Hampton M, Torpdahl M, Kapperud G, Aavitsland P. Outbreak of Salmonella Thompson infections linked to imported rucola lettuce. Foodborne Pathog Dis 2008; 5: 165–73.

Gundogan N, Citak S, Turan E. Slime pro-duction, DNase activity and antibiotic resistance of Staphylococcus aureus isolated from raw milk, pasteurized milk and ice cream samples. F Cont 2006;17: 389–92.

Neihart RE, Fried JS, Hodges GR. Coagulase-Positive Staphylococci. South Med J 1988; 81: 491–500.


Refbacks

  • There are currently no refbacks.