FOOD POISONING ABILITY OF STAPHYLOCOCCUS AUREUS ISOLATED FROM MEAT PRODUCTS AND POULTRY MEAT

Assiut University web-site: www.aun.edu.eg

FOOD POISONING ABILITY OF STAPHYLOCOCCUS AUREUS ISOLATED FROM MEAT PRODUCTS AND POULTRY MEAT

MOHAMED KARMI

Department of Food Hygiene, Faculty of Veterinary Medicine, Aswan University, 81528 Aswan, Egypt

Received: 27 May 2019;     Accepted: 20 June 2019

INTRODUCTION

Staphylococcus aureus (Staph aureus) is a gram positive bacterium secret enterotoxins which responsible for food poisoning in human through consumption of meat and poultry (Genigeorgis, 1989, Wieneke et al., 1993), which containing enough dose of pre-prepared toxins (Dinges et al., 2000, Le Loir  et al., 2003). The most characteristic feature of staphylococcal food poisoning (SFP) is the rapid onset through 3-8 hours as well as nausea, vomiting, abdominal cramps and rarely diarrhea and lasts for 1-2 days. Sever course can occur in children and elderly who get infection through consumption of processed meat and dairy products. The implicated foods are prepared and handled in unhygienic manner and stored in higher temperatures. Degree of contamination and the environmental conditions may favor the growth and multiplication of the microorganism and subsequently the formation of large amounts of enterotoxins (Downs and Ito, 2001). Staph aureus is the second food borne pathogen causing food poisoning in the world after Salmonella (Atanassova et al., 2001). S. aureus conforms a large proportions of nosocomial infections especially methicillin – resistant Staph aureus (MRSA) which

Corresponding author: Dr. Mohamed Karmi

E-mail address: karmy99@ yahoo.com

Present address: Department of Food Hygiene, Faculty of Veterinary Medicine, Aswan University, 81528 Aswan, Egypt

resistant to several antibiotics such as quinolones (Ortega et al., 2010). Staph aureus normally inhabit about 20% of people and 60% are carriers (Kluytmans et al., 1997). It is found normally in the nasal cavity of most people which causing infection in people with lowered immunity especially in carrier persons while non-carrier persons can get infection through consumption of contaminated foods (Von Eiff et al., 2001). Enterotoxin type A is the most common cause of food poisoning everywhere beside other types (Argudin et al., 2010). Staphylococcal enterotoxins are resistant to heat, acidity and proteolytic enzymes and preserve activity after processing and digestion, it is active in low micrograms (Schantz et al., 1965). Staph aureus is a very serious pathogen in food poisoning and in hospital infections and characterized by production of virulent heat stable toxins which are responsible for toxic shock like syndrome and food poisoning as well as induction of T cells proliferation as superantigen (Harris et al., 1993, Martin et al., 2003, Kérouanton et al., 2007). Hemolysin, thermonuclease, lipases and hyaluronidase are virulence factors responsible for the pathogensis of Staph aureus (Sandel and McKillip, 2004, Normanno et al., 2007, Kuroda et al., 2007). Enterotoxins type A, D and B are the most risky and notable ones in food poisoning. Type A is more common then type B which used as inhalational bioweopon (Ler et al., 2006). Type D is the second common cause of food poisoning and in a very small dose (Bergdoll et al., 1981). Type E has the ability to cause food poisoning while type F causes toxic shock syndrome (Morris et al., 1972). Type G, H and I are not common in food poisoning although they implicated in outbreak in Taiwan (Chen et al., 2004). Type H also was isolated as a causative agent of massive food poisoning from reconstituted milk in Osaka, Japan in 2000 (Ikeda et al., 2005). Therefore, this work was planned to study the prevalence of Staph aureus in meat products and poultry meat samples as well as PCR detection of staphylococcal enterotoxins (SEs)-forming genes in isolated bacteria,

MATERIALS AND METHODS

Samples

A total of 200 samples including 100 samples from chicken meat; 50 fresh and 50 frozen (breast and thigh muscles) and 100 samples from meat products (minced meat, burger, luncheon and sausages) were collected from Aswan markets. Sampling box containing ice pads was used for carrying the samples from market to laboratory maintaining low temperature. Samples were preserved in sterile polyethylene bags in the refrigerator. Twenty five grams of each chicken meat or meat product sample were aseptically transferred to sterile stomacher bag, homogenized by using Stomacher® 400 Circulator (Seward Ltd., UK) and mixed in 225 ml Buffered Peptone Water (BPW).

Isolation and Identification

The mixture samples were incubated at 37 °C for 18-24 hours. Pre-incubated samples (0.1 ml) in BPW were spread on the surface of Baird-Parker agar (BPA) medium supplemented with Egg-Yolk Tellurite Emulsion and Mannitol salt Agar (MSA) (Oxoid Limited, Hampshire, England), a selective media for Staph aureus and incubated at 37 °C for 24-48 hours. Black colonies surrounded by whitish halo zone formation on BPA and yellow colonies on MSA were considered presumptive Staph aureus, confirmed with the help of Gram's staining, coagulase, catalase and other biochemical tests (Szabo, 2000, Bennett and Lancette, 2001).

Genetic Detection

DNA extraction was carried out by using boiling method; DNA was prepared by the whole-cell procedure. Each DNA template was prepared by using approximately half a loopful of culture transferred to 1 ml of TE buffer (pH 8) and mixed in suspension. The resulting suspension was heated at 100°C for 10 minutes and centrifuged at 13000 rpm for 5 minutes. A five µl aliquot was directly used as a template for PCR amplification (Lawrynowicz-Paciorek et al., 2007). Primer sequences were used as forward and reverse for sea, seb and sec genes used for identification of toxin genes (Table 1). Multiplex PCR amplification of toxigenic genes was carried out, each reaction consists of 2.5 µl of 10x buffer, 10 µl master mix, 0.5 µl each primer, 3 µl DNA template and nuclease free water till 25 µl volume (Rahimi, 2013). Thermacycler (Eppendorf, Germany) was used with initial denaturation step at 94°C for 5 minutes followed by 30 cycles (denaturation at 94°C for 0.5 minute, annealing at 59°C for 0.5 minute and extension at 72°C for 0.5 minute for toxin genes) (Akbar and Anal, 2013), ending with final extension at 72°C for 10 minutes. Amplified products were analyzed by 1.5% agarose gel electrophoresis stained with ethidium bromide and visualized on UV transilluminator (Martineau et al., 1998, Rall et al., 2008, Zouharova and Rysanek, 2008).

RESULTS

Overall prevalence of pathogenic coagulase-positive Staph aureus was 70%, 46% and 11% in fresh chicken meat, frozen chicken meat and meat products samples, respectively. Prevalence of Staph aureus in breast and thigh muscles of fresh chicken was 72% and 68% while in breast and thigh muscles of frozen chicken was 52% and 40%, respectively (Table 2). In meat products, prevalence of Staph aureus were 20% and 24% in minced meat and luncheon, respectively, while burger and sausage were free from contamination by Staph aureus. Genetic investigation of toxigenic genes showed presence of sea gene in 51% of fresh chicken meat, 35% of frozen chicken meat, 100% of minced meat and luncheon positive - Staph aureus isolates while seb gene was failed to be detected in examined samples while sec gene was found in 37% of fresh chicken meat, 17% of frozen chicken meat and 100% of minced meat and luncheon positive Staph aureus isolated (Table 3).  

Table 1: Primer sequences and expected size of PCR amplified gene targets of   Staph aureus (Gayathri and Prakash, 2014).  

Table 2: Prevalence of pathogenic Staph aureus in fresh chicken meat, frozen chicken meat and meat products.

Table 3: Prevalence of toxigenic genes (sea, seb, sec) in Staph aureus isolated from fresh chicken meat, frozen chicken meat and meat products.           

DISCUSSION

In this study, the overall prevalence of pathogenic coagulase-positive Staph aureus was 70%, 46% and 11% in fresh chicken meat, frozen chicken meat and meat products samples, respectively. It is noticed that highest rate of contamination was in fresh chicken meat (70%) then in frozen meat chicken (46%) and lower rates in meat products (20% in minced meat and 24% in luncheon). Comparison of these results with results of other authors revealed that overall prevalence of Staph aureus in chicken meat (70%, 46%) was in agreement with results such as: 85.71% (Capita et al., 2001), 68.53% (Islam et al., 2014), 67.5% (Gundogan et al., 2005), 57.1% (Kitai et al., 2005), 50.98% (Rasheed, 2011), 41% (Waters et al., 2011) and higher than other results of 25% (Bhargava et al., 2011), 18.18% (Akbar and Anal, 2013), 17.8% (Hanson et al., 2011), 12.8% (Heo et al., 2008), 7.8% (Lin et al., 2009). Prevalence of Staph aureus in meat products (20% in minced meat and 24% in luncheon) was in agreement with results such as: 20.5% (Bhargava et al., 2011), lower than results such as: 63% (Jackson et al., 2013), 45.6% (van Loo et al., 2007), 50% (Abdalrahman et al., 2015), 37% (Waters et al., 2011) and higher than results such as: 10% (Heo et al., 2008), 6.9% (Hanson et al., 2011), 6.1% (Gutierrez et al., 2012). Results revealed that 51% of fresh chicken meat, 35% of frozen chicken meat, 100% of minced meat and luncheon having enterotoxin A-producing gene (sea) which is responsible for occurrence of staphylococcal food poisoning in consumers and considered the main cause of emetic symptoms. About 37% of fresh chicken, 17% of frozen chicken and 100% of minced meat and luncheon  having enterotoxin C - producing gene (sec) while enterotoxin B-producing gene (seb) was absent in all samples. These results indicated that isolated strains of Staph aureus having ability to produce one or more than one enterotoxins which responsible for food poisoning in consumers and appearance of their symptoms.

Contamination of meat by Staph aureus, which may due to unsanitary conditions during processing and preparation, conform a high risk to the consumers (Gundogan et al., 2005). Certain steps in poultry slaughter such as scalding, defeathering, washing and chilling may increase the incidence of contamination of poultry meat by S. aureus (Hansson, 2001, Spescha et al., 2006). Large proportions of meat and poultry get contaminated by Staph aureus which reached 37-77% and about 52% of the isolates are resistant to multiple antibiotics (Waters et al., 2011). Staph aureus produce several exotoxins such as toxic shock syndrome toxins, coagulase, hemolysin, exfoliative toxin and about fifteen types of enterotoxins (Mehrotra et al., 2000). Shock syndrome toxin and enterotoxins type A and B are more dangerous toxins and superantigens (Gunaydin et al., 2011). The higher contamination of retail meat by Staph aureus is the higher potential of MRSA transfer to the consumers (Shukla et al., 2010). It is found that incidence of Staph aureus in poultry meat (65.8%) was higher than that of beef (20-25%) or pork (26-29%) (Shimizu     et al., 1991, Jiang et al., 2001). Poultry meat get contaminated by Staph aureus through two main sources; the first one is by poultry types which found in the nasal cavity and intestines of the birds and contaminate the meat during slaughter steps and the second one is the human types which found on the skin and hands of workers who handle and prepare the poultry meat (Shimizu et al., 1986, Saitoh et al., 1994, Arai et al., 2004). The food poisoning ability and the pathogenicity of Staph aureus are attributed mainly to formation of exo- and endotoxins (Sandel and McKillip, 2004).

About fifteen enterotoxins produced by Staph aureus (Atichou et al., 2004), types A, B, C, D and E are the more common and considered the main cause of food poisoning while the other types such as G and O may play minor role in food poisoning (Jay et al., 2005). The role of the novel discovered types of enterotoxins in the food poisoning or other affections is still not clear enough and need more research. The use of innovative genetic characterization of enterotoxin forming genes may be useful in the study of these toxins. The majority of Staph aureus strains isolated from food produce enterotoxins type A, C and D (Rahimi, 2013). The enterotoxins are heat stable and resist denaturation to still intact in the food and subsequently induce food poisoning.  Also, the major problem is the occurrence of multidrug resistant strains of Staph aureus which causing antibiotic-associated diarrhea in the hospitals (Pinchuk, et al., 2010).

CONCLUSION

Meat products and poultry meat products are considered important sources for pathogenic Staph aureus which get contaminated either from animal origin or from human during processing and preparation. All Staph aureus isolates contained one or more enterotoxin-forming genes which give the bacteria the ability to cause food poisoning to the consumers. Enterotoxin type A and type C were considered the main enterotoxins and may be responsible for occurrence of food poisoning outbreaks.

AUTHORS’ CONTRIBUTIONS

Author performs collection, preparation, processing, and analysis of samples, isolation of bacteria, data acquisition, writing, preparation and revision of manuscript.

ACKNOWLEDGEMENTS

I thank Faculty of Veterinary Medicine, Aswan University for technical support.

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قدرة ميکروب المکور العنقودى الذهبى المعزول من اللحوم و الدواجن على  إحداث التسمم الغذائى

محمـد کرمـى

E-mail: karmy99@yahoo.com       Assiut Univers ity web-site: www.aun.edu.eg

تم إجراء هذا البحث لدراسة معدل انتشار ميکروب المکور العنقودى الذهبى فى منتجات اللحوم ولحوم الدواجن وللکشف على الجينات المکونة للسموم البکتيرية فى ميکروب المکور العنقودى الذهبى. تم تجميع عدد 200 عينة منها 100 عينة من الدواجن الطازجة والمجمدة من الصدور والأوراک و100 عينة من منتجات اللحوم الحمراء بواقع 25 عينة من کل من اللحوم المفرومة واللانشون والبرجر والسجق لإجراء هذا البحث. تم إجراء الفحص البکتريولوجى و البيوکيميائى والجينى باستخدام تفاعل إنزيم البلمرة المتسلسل. دلت النتائج على أن معدل إنتشار ميکروب المکور العنقودى الذهبى کان 72% و 67% و 52% و 40% فى صدور وأوراک الدواجن الطازجة والمجمدة على التوالى و 20% و 24% فى اللحوم المفرومة واللانشون بينما کانت عينات البرجر والسجق خالية من هذا الميکروب. معدل تواجد الجين أ کان 51% فى الدواجن الطازجة و 35% فى الدواجن المجمدة و 100% فى اللحوم الحمراء المفرومة واللانشون ومعدل تواجد الجين ج کان 37% فى الدواجن الطازجة و 17% فى الدواجن المجمدة و 100% فى اللحوم الحمراء المفرومة واللانشون بينماخلت جميع العينات من الجين ب. خلصنا من هذا البحث أن قدرة ميکروب المکور العنقودى الذهبى على إحداث التسمم الغذائى للإنسان تعتمد أساسا على مدى إحتوائه على الجينات المکونة للسموم البکتيرية وأن الجين أ هو الجين الأشهر والرئيسى لإحداث هذا التسمم الغذائى فى الإنسان من خلال إستهلاک اللحوم والدواجن.