Research Article

 

Assuring the Safety of Local and Imported Beef Meat from Different Slaughterhouses in Egypt

 

Hanan Korany Sayed1, Khalid Shawky Tolba2, Hassan Mohamed Sobhy3, Sahar Hussein Abdalla Hekal3*

1General Organization of Vet. Services – Ministry of Agriculture; 2Chief Researcher of Food Hygiene and Safety in Reference lab for Food Safety, Animal Health Research Institute, Dokki – ARC; 3Department of Natural Resources, Faculty of African Postgraduate Studies - Cairo University, Giza, Egypt.

 

Received | May 14, 2021; Accepted | June 12, 2021; Published | July 28, 2021

*Correspondence | Sahar Hussein Abdalla Hekal, Department of Natural Resources, Faculty of African Postgraduate Studies, Cairo University, Giza, Egypt; Email: [email protected]

Citation | Sayed HK, Tolba KS, Sobhy HM, Hekal SHA (2021). Assuring the safety of local and imported beef meat from different slaughterhouses in egypt. Adv. Anim. Vet. Sci. 9(9): 1472-1482.

DOI | http://dx.doi.org/10.17582/journal.aavs/2021/9.9.1472.1482

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2021 Hekal et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

INTRODUCTION

 

Meat has high nutritive value for human consumption. On the other hand, meat is considered as an ideal growth media for many microorganisms because of the high moisture content, high percentage of nitrogenous compounds, good supply of minerals, glycogen and a favorable pH for most microorganisms (Al-Metairie, 2011). As a result of inappropriate environmental conditions, unhygienic slaughtering processes, bad storage and transportation of meat as well as bad handling and retailing may be resulted in its contamination with different food spoilage and food poisoning microorganisms. (Ercolini et al., 2006).

 

Egypt imports different types of meat to fill the gaps in the requirements of animal protein. (USDA, 2016). While the importation of beef meat in Egypt is crucial to close the gap in animal protein requirements, monitoring the frequency of antimicrobial resistance in imported meat must assure that quality and safety standards are met. The extent of microbial contamination and composition of microbial flora reflect the standard hygienic measures adopted during meat processing (Ko et al., 2013; Kim et al., 2016). Meat may be contaminated with various pathogenic microorganisms as E. coli, Salmonellae and Staph. aureus which renders meat constitute a hazard to human health (Nørrung et al., 2009). Moreover, some strains of E. coli could be able to causes several human foodborne illnesses ranging from gastrointestinal symptoms to sever bloody diarrhea and dysentery, also it considered the main cause of urinary tract complication represented by hemolytic uremic syndrome (HUS), pneumonia and meningitis (Johnson et al., 2006). Pathogenic E. coli strains have been broadly classified into two major categories; extraintestinal pathogenic and diarrheagenic E. coli which classified into six categories including Enteropathogenic E. coli (EPEC), Enterotoxigenic E. coli (ETEC), Entero-invasive E. coli (EIEC), Enteroaggregative E. coli (EAEC), diffusively adherent E. coli (DAEC) and Entero-hemorrhagic E. coli (EHEC)/Shiga toxin-producing E. coli (STEC) (Monaghan et al., 2011; Clements et al., 2012).Salmonella has been considered as a significant foodborne disease and could be isolated from raw meat, poultry and their products. Cross contamination and unhygienic measures during food processing are considered a predisposing factor for contamination with Salmonella (Gorman et al., 2002). Staphylococcal foodborne intoxication occurs all over the world and caused by ingestion of already preformed Staph. aureus enterotoxins in food causing clinical signs as vomiting, diarrhea and even death in older people and children (Baumgartner et al., 2014).

 

The main sources of meat contamination occurred during slaughtering processes are hides and gastrointestinal contents of the slaughtered animals, the work environment. Also, carcasses can be contaminated during the slaughtering process through the contact with the animal’s skin, blood, hair, limbs, bile, equipment’s, water, air pollution and worker’s hands and clothes (Koffi-Nevry et al., 2011).

 

The circumstances at which the animal breed up, its health condition, slaughtered and carcass preparation are mostly affect the microbial load of the carcass in the abattoir. Firstly, carcass contamination takes place at the point of skinning and the following contamination occurs due to dust arises during removal of hide, workers hands or by contact between dirty hide and subcutaneous connective tissue (Zweifel et al., 2008). The degree of bacterial contamination of animal carcass differs according to plant sanitation. It is also affected by numerous factors as plant layout, rapidity of slaughtering processes and applying of good manufacturing and processing practices (GMP & GHP) as well as the skillfulness of the slaughtering plant workers and the presence of both un-skinned and skinned carcasses in the same area might be a source of meat contamination by many pathogenic agents (Alegre and Buncic, 2004; Hemmat et al., 2014).

 

Microbial examinations of slaughtered carcasses were not included through the routine of meat inspection in the slaughterhouses. (Muhammad et al., 2011; Bogere and Baluka, 2014).Therefore, the current study was applied to investigate E. coli and Staph. aureus counts as well as serodiagnosis of E. coli, Salmonellae isolates and determination of enterotoxin production by Staph. aureus in local and imported meat. Public health of isolated bacteria was discussed.

 

MATERIALS AND METHODS

 

Collection of samples

A total of 100 random fresh beef samples (locally produced and imported; 50 samples of each), were collected from different slaughterhouses in different Governorates; the local meat samples were from slaughter houses of El- Moneeb, El- Waraq and El- Basateen in Cairo and Giza governorates, while the imported meat samples were collected from El- Swiss slaughter house in Swiss canal governorate and Abu- Simble slaughter house in Aswan governorate. The collected samples were kept in its sailing bags and aseptically transferred without delay, in an insulated ice box to the laboratory without delay.

 

Preparation of sample homogenate

Twenty-five grams of the examined samples were aseptically transferred to a sterile stomacher bag and homogenized with 225 ml sterile buffered peptone water (0.1%) for 30-60 seconds to give an initial dilution of 1/10. Serial dilutions up to 106 was carried out according to APHA (2001). Prepared homogenate was used to carry out the following bacteriological examinations.

 

Bacteriological examination

Enumeration and Isolation of Staphylococcus aureus were done according to the technique recommended by FDA (2001).

 

Enumeration, Isolation and identification of B-glucuronidase-positive Escherichia coli according to (ISO 16649-2:2001).

 

Isolation of and identification of Salmonellae enterica according to (ISO 6579-1:2017).

 

Serological identification of Salmonellae according to Kauffman–White Scheme (Kauffman, 1974 for the determination of Somatic (O) and flagellar (H) antigens using Salmonella antiserum (DENKA SEIKEN Co., Japan).

 

Isolated Staphylococcus aureus strains were examined for their ability to produce different types of enterotoxins using Sac culture method and staphylococcal enterotoxin-Reversed Passive Latex Agglutination (SET-RPLA) test kit according to (Donnelly et al., 1967).

 

Serological identification of E. coli according to (Kok et al., 1996) using rapid diagnostic E. coli antisera sets (DENKA SEIKEN Co., Japan) for diagnosis of the Enteropathogenic types.

 

Statistical analysis

Was carried out using Statistical Package for the Social Sciences (SPSS). One Way ANOVA, Ver. 20.

 

Ethical statement

Ethical approval was not needed in this study as the samples were collected from slaughtered cattle from the abattoir. However, consent from the abattoir authorities was taken prior collection of samples.

 

RESULTS AND DISCUSSION

 

Beef meat have been considered as highly desirable, nutritious and good quality protein rich food, meanwhile, meat is highly perishable because they provide a nutrient required for growth and multiplication of different types of microorganisms. The hygienic practices applied during slaughtering and processing of animals is controlling the quality attribute of meat and its shelf life as the increase in microbial load and its content of food poisoning and food intoxication organisms shall constitute a public health hazard (Kalalou et al., 2004)

 

Staph. aureus and E. coli counts (log10cfu/g) in examined local and imported meat samples

It is evident from the results recorded in Table (1) that Staph. aureus mean value was 2.31±0.1 log10cfu/g and 2.07±0.09 log10cfu/g in examined samples of local and imported beef meat with 22(44%) and 20(40%) positive samples, respectively. Results achieved in Table (1) also showed that E. coli mean count was 3.15±0.13 log10cfu/g with incidence rate (40/80%) in local beef meat and 2.98±0.11 (34/68%) in examined imported beef meat. There were no significance differences (P>0.05) between both local and imported meat regarding Staph. aureus and E. coli. Nearly similar results were recorded by (Abdalrahman et al., 2015) who could isolate staph. aureus by 50% (23/46) of examined retailed beef cuts, they added that Staph. aureus is one of the top five pathogens contributing to acquired foodborne illnesses causing an estimated quarter million cases every year in the US. Many investigators recorded incidence of Staph. aureus in fresh meat (Wu et al., 2018) 63 samples/43.3%), (Ge et al., 2017) (27.9%) in the USA, (Tang et al., 2017)  (68%) in Denmark. In addition, (Bakr et al., 2004; Kitai et al., 2005; Van Loo et al., 2007; Buyukcangaz et al., 2013; Jackson et al., 2013; Bunnoeng et al., 2014; Dhup et al., 2015) found that 4 – 76.47% of raw meat samples were contaminated with Staph. aureus. Such differences in prevalence of Staph. aureus may be attributed to the sample sizes, sample types, hygienic status and geographic locations and collection period of investigation (Ge et al., 2017).

 

In this respect, (Elsharawy et al,. 2018) examined 40 fresh meat samples from Elkharja municipal slaughterhouse, New Valley Governorate, Egypt and it was found that mean E. coli count recorded (2.47x103±15.54x10) which is nearly identical to the results of the current study, while the mean Staph aureus count (9.94x102±15.7x10) was slightly higher, they concluded that applied hygienic measures in Elkharja slaughterhouse were low and more governmental efforts are still needed to control the microbial contamination and improve the environmental quality and infrastructure of Elkharga slaughterhouse in New Valley, Egypt. Also, similar results for Staph. aureus count was recorded by (Saad et al., 2019) (4.03 x 102 ± 0.75x102 cfu/g). The incidence of E. coli in imported fresh beef meat came in accordance with (Salman et al., 2015) (72%) from 150 samples collected from Alkadaro slaughterhouse, Khartoum-Sudan. Lower prevalence of Staph. aureus (8 isolates/16%) and E. coli (4/8%) obtained by (Abd El tawab et al. 2020). (Abdalla et al. (2009) found that Staph. aureus and E. coli were isolated by 10.54% and 8.86%, respectively from bovine carcasses in Khartoum – Sudan during 2008. Higher Staph. aureus count was recorded by Hemmat et al. (2014) (28×103±5×103 cfu/g) of shoulder beef meat collected from two traditional abattoirs of Elbehira province, while the incidence of Staph. aureus (12 isolates /40%) came in accordance with the present study. In this issue, Higher prevalence of Staph. aureus in examined raw buffalo meat samples in Nepal were recorded by (Kamana et al., 2018) (80%) respectively, while lower results were recorded by the same authors for isolation rate of E. coli (40%). They concluded that no significant difference between the type of meat and the presence of Staph. aureus and E. coli (P > 0.05). This agreed with statistical analysis of the present study.

 

Also, (Bogere and Baluka, 2014) recorded higher E. coli and Staph. aureus counts (8.4×104 and 2.7×103 cfu/g) respectively, in fresh meat samples collected from some abattoirs in Uganda Also, higher results of mean E. coli and Staph. aureus counts in meat were also recorded by (Hughes et al., 2015) in Ghana (5.97 and 5.5 log10cfu/g), respectively.

 

Table 1: Statistical analytical results of Staph. aureus and E. coli counts (log10cfu/g) in examined local and imported meat samples

 

Types of meat	Statistical analysis
	Staph. aureus			E. coli
	Count	Positive samples		Count	Positive samples
		No	%		No	%
Local	2.31a±0.1	22	44	3.15b±0.13	40	80
Imported	2.07a±0.09	20	40	2.98b±0.11	34	68

Statistical analysis expressed for positive samples only.

No significance difference (P>0.05) between means having the same small superscripted litter in the same column.

 

(FANZA , 2016) recorded 95.24% of beef meat samples had quality unsatisfactory quality due the presence of E. coli. (Philips et al., 2007) in Austria found that 17.8% of retailed beef meat contaminated with E. coli with mean count (1.49 log10cfu/g), while Staph. aureus contaminated samples were recorded 28.1%.

 

Staph. aureus enterotoxin production in local and imported meat

Fig. (1) Illustrated that Staph. aureus enterotoxins (SE) types “A” and “D” were successfully produced from two strains separately (20% for each) out of five tested strains obtained from local beef meat. In contrary, all random five Staph. aureus strains isolated from imported meat samples were negative for production of any type of enterotoxins.

 

 

These results go hand to hand with those recorded by (El-Shater-Nahla, 2010) (20% SEA and 26.8% SED) using SET-RPLA test kit, (Normanno et al., 2005) (26.5% SEA and 20.5% for SEA+SED) and (Normanno et al., 2007) (SEA, 18.4%). Furthermore, (Mathieu et al., 1991) found that SEA is the most common enterotoxin recovered from food-poisoning of all recorded outbreaks in the US (77.8%) followed by SED (37.5%) and SEB (10%). In addition to, Zagar et al. (2014) isolated 7 strains (14.8%) of Staph. aureus from examined beef meat samples, two samples (28.5%) found to contain enterotoxin type “A”. In Slovak republic, out of the 43 staphylococcal strains isolated from different foods, 15 strains (34.88%) were found to be enterotoxigenic and out of these 15 strains, seven (16.28%) contained enterotoxin “A” (Holeckova et al., 2002). Moreover, in 2011 in Marmara, Turkey, (Aydin et al., 2011) found that 13.8% of beef meat samples were contaminated with Staph. aureus out of which, 8.6% contained SEA. In Tehran, (Eshraghi, 2009) stated that Staph. aureus isolated from raw meat was able to produce SEA and SEA+SEC by 8% and 9%, respectively. These results, proved that the rates of presence of enterotoxin types A and D are the most common enterotoxins in meat which are identical to the results of the current research.

 

(Shawish and Al-Humam, 2016) find a considerable diversity of Staph. aureus and its enterotoxin production where they isolated 19 Staph. aureus strains from minced meat (38%) out of which, 8(16%) were enterotoxin producers; 6(75%) were SEA producers, 4(50%) SEB, 5(62.5%) SEC and 4(50%) SED producer. For beef burger, out 11(22%) Staph. aureus isolates, 4(8%) were enterotoxigenic; 4(100%) were SEA producers, 2(50%) SEB and 2(50%) SEC producers. The aforementioned incidences of enterotoxin considered higher than that obtained in the present study. In addition, the majority of reported Staphylococcal Food Poisoning (SFP) outbreaks are associated with the classical enterotoxins, SEA-SEE and staphylococcal enterotoxin A (SEA) being considered the most common cause of SFP (Wieneke et al., 1993; Cha et al., 2006). Such variation in enterotoxin production may be due to the variation in the implemented traditional hygienic practices and food safety measures (Hussain and Dawson, 2013). Moreover, (Fisher et al., 2018) explained that Staph. aureus enterotoxins are a superfamily of secreted virulence factors that share structural and functional similarities and possess potent adverse effect on immunity. The classical (SEA-SEE) enterotoxin groups resulted in several serious human diseases, including toxic shock syndrome, pneumonia, and sepsis-related infections. Additionally, some of these enterotoxins are responsible for emetic activity and are frequently responsible for food poisoning outbreaks. Due to their robust tolerance to denaturing, the enterotoxins retain activity in food contaminated previously with Staph. aureus. The genes encoding the enterotoxins are found mostly on a variety of different mobile genetic elements. Therefore, the presence of enterotoxins can vary widely among different Staph. aureus isolates. Additionally, the enterotoxins are regulated by multiple, and often overlapping, regulatory pathways, which are influenced by environmental factors.

 

Isolation and identification of B-glucuronidase-positive Escherichia coli and Serological identification of E. coli

The results recorded in Fig (2,3 & Photo 1) indicated that among the five strains of E. coli that were randomly selected from 40 E. coli strains isolated from fresh local meat, one strain (20%) was classified as Enteropathogenic (EPEC) and its serodiagnosis was O146:H21 which harbored stx2 gene, while two strains (40%) were Enterohaemorrhagic (EHEC) “O111:H2” and both found to harbor (stx1, stx2 and eaeA) genes and finally, one strain (20%) was Enterotoxigenic (ETEC) “O15:H4” and found to contain stx1 only, while the 5th strain was non-pathogenic and subsequently not subjected to serodiagnosis.

 

 

 

On the other hand, the results of serodiagnosis and virulence gens of the five randomly selected strains of E. coli out of 34 E. coli isolates from imported meat which registered in Fig (4,5 & Photo 1) showed that, one strain (20%) was classified as Enteropathogenic (EPEC) and its serodiagnosis was O128:H2 which harbored stx1 gene, while one strains (20%) was Enterohaemorrhagic (EHEC) “O26:H11” which harbored both (stx1 and stx2) genes and finally, the 3rd strain (20%) was Enteroinvasive (EIEC) “O159” and found to contain stx1 only, while the 4th and the 5th strains were non-pathogenic and subsequently not subjected to serodiagnosis. From the obtained results it could be concluded that local meat contained more pathogenic E. coli and virulence gens as compared with imported meat.

 

Lane M: 100 bp ladder as molecular size DNA marker.

Lane C+: Control positive E. coli for stx1, stx2 and eaeA genes.

Lane C-: Control negative.

Lanes 2 & 3 (O111): Positive E. coli for stx1, stx2 and eaeA genes.

Lane 5 (O26): Positive E. coli for stx1 and stx2 genes.

Lane 1 (O15), 6 (O128) & 7 (O159): Positive E. coli for stx1 gene.

 

 

Table 2: Incidence and serodiagnosis of Salmonella enterica in examined locally and imported meat samples (50 samples each)

 

Type of meat / No. of positive isolates	Incidence of positive samples	Identified strains	Group	Antigenic structure
				O	H
Local meat: 1	4%	Salmonella Montevideo	C1	6,7,14	g,m,s: 1,2,7
1		Salmonella Enteritidis	D1	1,9,12	g,m : -
Imported meat: 1	2%	Salmonella Typhimurium	B	1,4,5,12	i: 1,2

 

 

The obtained results are compatible with (Hussein, 2007) isolated members of O26 which successfully detected in the present study. Furthermore, the results are in line with that recorded by (Berger et al., 2010; Qardi et al., 2005; Steffen et al., 2005) mentioned that ETEC and EPEC are most common in developing world and appear to be the major causes of infantile diarrhea with potentially fatal consequences when untreated, while EHEC considered the main E. coli pathotypes associated with food poisoning outbreaks in the developed world. Nearly similar results were obtained by (Zweifel, 2003) detected stx1 and stx2 of non O157 E. coli isolated from sheep carcasses obtained from three Swiss abattoirs. (Monaghan et al., 2011); Datta et al., 2012; Hamed et al., 2015) stated that E. coli commonly considered non-virulent, but some strains have adopted pathogenic or toxigenic virulence factors that make them virulent to human and animals. Pathogenic E. coli strains have been broadly classified into two major categories; extraintestinal pathogenic and diarrheagenic E. coli which classified into six categories including Enteropathogenic E. coli (EPEC), Enterotoxigenic E. coli (ETEC), Entero-invasive E. coli (EIEC), Enterohemorrhagic E. coli (EHEC)/Shiga toxin-producing E. coli (STEC), Enteroaggregative E. coli (EAEC) and diffusively adherent E. coli (DAEC).

 

E. coli of different serotypes and virulence factors was isolated from fresh meat and meat products with different diversities by many investigators; (Aidar-Ugrinovich et al., 2007) could isolate members of STEC represented by O7:H10, O22:H16, O111:H(-), O119:H(-) and O174:H21,  whereas O26:H11, O123:H11 and O177:H11 were the most prevalent among EPEC strains in Brazil, The eaeA gene was detected in 25% of the STEC and 100% of EPEC strains. (Abd El-Tawab et al., 2015b) (O55:H7 (3/27.3%), O78 (2/18.2%), O111:H4 (1/9.1%), O26:H11 (2/18.2%), O119:H4 (1/9.1%) and O128:H18 (1/9.1%), (Binsy et al., 2016) (O3, O19, O22, O25, O29, O34, O36, O42, O50, O51, O53, O55, O65, O66, O73, O79, O105, O109, O115, O139, O140, O147, O152, O163, O164 and O173), (Shaltout et al., 2016) (O55:H7 EPEC (2/5.71), O125:H18 EPEC (1/2.86), O111:H4 EHEC (1(2.86) and O26:H11 EPEC (1/2.86%), (El-Sayed, 2019) (O55:H7 and O26:H11 and eaeA gene was detected in the tested strains. Furthermore, (Gyles, 2007) and (Aidar-Ugrinovich et al., 2007) mentioned that healthy dairy and beef cattle are a major reservoir of a diverse group of STEC that infects humans through contamination of food and water, as well as through direct contact. These results were compliant with the present research.

 

Incidence and serodiagnosis of Salmonella enterica in examined locally and imported meat : Results in Table (2) indicated that Salmonella spp. was isolated from two samples (4%) of examined local meat out of which one strain was identified as S. Montevideo of Group “C1” with antigenic structure (O6,7,14:H g,m,s:1,2,7) and the 2nd strain was S. Enteritidis of group “D1” (O: 1,9,12:H g,m). While, imported meat recorded 1 strain (2%) of S. Typhimurium of group “B” (O:1,4,5,12 H: i:1,2). In this regard, Food safety standards set by international organizations concerned with food safety parameters (EC No. 2073l2005; ICMSF, 2011; FDA, 2018 and FNANZ, 2018) that food should be free of salmonella spp. Therefore, the obtained results in the present study revealed that two samples (4%) of examined local meat and 2% of imported meat were rejected as they contained salmonella spp. and considered unfit for human consumption Nearly similar results were recorded by (Duffy et al., 2001) isolated Salmonella by (1.5%) from lamb carcasses. (Fegan et al., 2005) who could isolate Salmonella by 3% from both pre and post chilled beef carcasses. (Reid et al., 2002) found that the hides of the rump area of beef carcasses was less contaminated (2.2%) with Salmonella spp. as compared with brisket area (10%). This may be attributed to the contact of brisket with the slaughterhouse floor which is the main source of contamination or may be due to the live animal itself and the environment which serve as sources for pathogenic bacteria which contaminate the meat during slaughtering, dressing and evisceration processes. (Tassew et al., 2010) isolated two Salmonella strains (1.2%) from meat samples collected from hotels, butcher shops and abattoir (Hemmat et al., 2014) (2.2%) of rump beef meat. Furthermore, the obtained results coincide with Hendriksen et al. (2007) who concluded that S. enteritidis and S. typhimurium are the most dominated serovar isolated from meat and meat products and are considered the most common cause of human infection. In addition, (Sibhat et al., 2011) (2%) in Ethiopia with serotypes of S. Eastbourne and S. urbana. (Narvaez-Bravo et al., 2013) (6%) in Mexico, (Moaward et al., 2017) (3.3%) S. enteritidis from examined fresh beef meat in Egypt, while the incidence of S. typhimurium was 3 strains (10%) which considered higher than the results in the present study. Also, (Ead-Hoiam and Abdelgadir, 2019) could isolate Salmonella from 4 rump samples (3.3%), 2(1.7%) from shoulder, 9(7.5%) from flank and 1(0.8%) from neck beef meat in in karay slaughterhouse, Khartoum state, Sudan.

 

Lowe incidence of salmonella in fresh beef meat were recorded by (Vugia et al., 2004) (0.09 cases annual incidence among 100000 population and 7.8 cases among infants), the authors could isolate Typhimurium, Typhi, Enteritidis, Heidelberg, Dublin, Para typhi A, Choleraesuis, and Schwarzengrund, (Greig et al., 2001) (0.07%) of human salmonellosis in Australia, (Crim et al., 2015) (0.015%) in USA. While, many investigators; (Venkateswaran et al., 1988; Kalyapure et al., 1994, Binsy et al., 2016; Elsharawy and Mahran, 2018) failed to isolate Salmonella spp. from examined beef meat samples (0%).

 

In this issue, Higher results were reported by (Mc Evoy et al., 2003) 6 isolates (7.6%) from bovine carcasses in Ireland. (Aftab et al., 2012) concluded that 100% of fresh beef meat was contaminated with Salmonella in Peshawar, Pakistan. (Ahmad et al., 2013) 4(20%) and 7(35%) of examined beef meat samples from abattoir and R. outlets, (Abd El- Tawab et al., 2015 b) who isolated 3 strains of salmonella spp. (12%) out of which; 2 strains of S. typhimurium (66.7%) and one strain S. enteritidis (33.3%) from beef meat, (Muluneh and Kibret, 2015) could isolate Salmonella from hind limb, abdomen and Neck of beef meat samples with 6%, 10% and 7%, respectively in slaughterhouse of Bahir Dar town, Ethiopia. The serovars identified as 11(47.8) as Salmonella group A., 9(39.1%) as S. Arizona and 3 isolates (13.1) identified as S. typhi. (Birhanu and Menda, 2017) (4/19%), (Saad et al., 2019) (28%), (Kamana et al., 2018) (20% and 33.3%) from buffalo and goat meat respectively. (Abou El Nour-Mona and Sakr-Ebtehag In Nepal, 2020) (38%).

 

The presence of Salmonella on the cattle hides indicated that contamination could be potentially transferred to the carcass during slaughtering and dressing process (Bacon et al., 2002; Ruby et al., 2007). or during unhygienic slaughtering process (Li et al., 2004; Rhoades et al., 2009). In addition to, variation in analytical methods, environmental condition, samples and sampling procedure would be able to assess the levels of contamination (Fegan et al., 2005). Also, the variation which observed between different research data related to the prevalence rate of Salmonella and its detected serovars around the world may be attributed to several factors including cleaning and sanitation within the slaughterhouse, possible contamination of meat during processing and difference among the applied reference methods for detection of Salmonella (Rahimi, 2012). Moreover, workers hands and clothes, and the work environment act as additional sources for carcasses contamination through the contact with the blood, hair, limbs, bile, facilities, equipment, water supplies and air pollution (Koffi-Nevry et al., 2011; Muhammad et al., 2012).

 

COnCLUSION AND RECOMMENDATIONS

 

The present study concluded that local and imported beef meat are contaminated with E. coli of different serovars and some of them was able to possess different virulence genes. (stx1, stx2 and eaeA). Also, Staph. aureus was present in both local and imported meat with some strains were able to produce enterotoxins A and D. Moreover, Salmonella was present with different percentages. This may be due to neglected sanitary measures adopted during slaughtering, dressing, evisceration, storage, transportation and distribution of cattle carcasses. Therefore, a concerted effort should be made to improve sanitary condition in all carcasses processes to mitigate bacterial contamination in slaughterhouses. In addition, Hazard Analysis and Critical Control Points (HACCP) should be applied to improve carcass hygiene as well as to eliminate or reduce the presence of pathogenic bacteria of beef carcasses well as application of control measures for pathogenic bacteria through the food chain including slaughterhouses and retail outlets.

 

Acknowledgments

 

The authors are thankful to General Organization for Veterinary Services, Egypt for providing necessary facilities for this study. The authors did not receive any funds for this study.

 

CONFLICT OF INTEREST

 

None of the author has any conflict of interest to declare.

 

Authors’ Contributions

 

HKS collected the samples, and performed the laboratory work and data analysis. KST, HMS and planned the research and experimental design, supervised the work, checked the data analysis. SHAH prepare the manuscript

 

REFERENCES

 

• Abd El-Tawab AA, Maarouf AA, El-Hofy-Fatma I, El-Said, Aya A (2015b). Bacteriological studies on some food borne bacteria isolated from chicken meat and meat products in Kaliobia Governorate. Benha Vet. Med. J. 29(2): 47-59. https://doi.org/10.21608/bvmj.2015.31545

• Abd El-Tawab A A, Maarouf AA, El-Hofy-Fatma I, Ahmed-Nesma MG (2020). Phenotypic characterization of some food poisoning bacteria isolated from meat and meat products in Kaliobia, Egypt. Benha Vet. Med. J., 38(2): 146-151. https://doi.org/10.21608/bvmj.2020.25678.1186

• Abdalla M A, Suliman S E, Ahmed D E, Bakhiet A O (2009). Estimation of bacterial contamination of indigenous bovine carcasses in Khartoum (Sudan). African J. of Microbiol. Res., 3(12): 882-886. https://doi.org/10.5897/AJMR.9000292

• Abdalrahman LS, Wells H, Fakhr MK (2015). Staphylococcus aureus is More Prevalent in Retail Beef Livers than in Pork and other Beef Cuts. J. Pathogens., 4(2): 182-198. https://doi.org/10.3390/pathogens4020182

• Abou El Nour-Mona M, Sakr-Ebtehag AE (2020). Isolation and Molecular Identification of Some Food Borne Pathogens from Raw and Processed Meats: In vitro Synergistic Probability of Lactobacillus CFS and Antibiotic. Egypt. J. Bot., 60(2): 405-421. https://doi.org/10.21608/EJBO.2019.19837.1395

• Aftab M. Rahman A, Qureshi M, Akhter S, Sadique U, Sajid A, Zaman S (2012). Level of Salmonella in beef of slaughtered cattle at Peshawar. Canadian J. Plant Sci., 22(2): 24-27.

• Ahmad MU, Sarwar A, Najeeb MI, Nawaz M, Anjum AA, Ali MA (2013). Assessment of microbial load of raw meat at abattoir and retail outlets. J. Amin. Plant Sci., 23(3): 745-748

• Aider-Ugrinovichm L, Blanco B M, Blanco J E, Leomil L, Dahbi G, Mora A, Onuma D L, Silveira W D, de Castro AFP (2007), Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in São Paulo, Brazil. Int. J. Food Microbiol., 115(3): 297-306. https://doi.org/10.1016/j.ijfoodmicro.2006.10.046

• AI-Metairie MF (2011). The Incidence of Enterobacteriaceae Causing food Poisoning in some meat products. J. of food Sci. and Technol., 3 (2): 116-121.

• Alegre L, Buncic S (2004). Potential for use of hide-carcass microbial counts relationship as an indicator of process hygiene performance of cattle abattoirs. Food Prot. Tren., 24: 814-820.

• APHA “American Public Health Association” (2001). Compendium of Methods for Microbiological Examination of food. 4th Ed., Washington, DC, USA. https://doi.org/10.2105/MBEF.0222

• Aydin A, Sudagidan M, Muratoglu K (2011). Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of food-borne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. Int. J. Food Microbiol., 148(2): 99-106. https://doi.org/10.1016/j.ijfoodmicro.2011.05.007

• Bacon RT, Sofos JN, Belk KE, Hyatt DR, Smith GC (2002). Prevalence and antibiotic susceptibility of Salmonella isolated from beef animal hides and carcasses. J Food Prot. Feb;65(2):284-90. https://doi.org/10.4315/0362-028x-65.2.284. PMID: 11848559.

• Bakr W M, Fawzia M, Hashish MH (2004). Detection of coagulase positive staphylococci in meat products sold in Alexandria using two different media. J. Egypt Public Health Assoc., 79, 31–42

• Baumgartner A, Niederhauser I, Johler S (2014). “Virulence and Resistance Gene Profiles of Staphylococcus aureus Strains Isolated from Ready-to-Eat Foods”. J- Food Protect., 7:1232-1236. https://doi.org/10.4315/0362-028X.JFP-14-027

• Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink DH, Frankel PG (2010). Fresh fruit and vegetables as vehicles for the transmission of human pathogens Environ. Microbiol.,12(9): 2385-97. https://doi.org/10.1111/j.1462-2920.2010.02297.x

• Binsy M, Nanu E, Sunil B (2016). Isolation of bacteria of public health significance from market beef. Int. J. Adv. Res. Biol. Sci., 3(4): 160-164.

• Birhanu S, Menda S (2017). Hygienic Handling and Processing of Raw Beef Meat at Slaughter Houses and Meat Stalls in Gojjam Area, Ethiopia International J. of Vet. Health. Sci. & Res. (IJVHSR), 5(8): 213-216. https://doi.org/10.19070/2332-2748-1700042

• Bogere P, Baluka S (2014). Microbiological quality of meat at the abattoir and butchery levels in Kampala City, Uganda. Internet J. Food Safe. 16: 29-35

• Bunnoeng N, Themphachana M, Pewleang T, Kongpheng S, Singkhamanan K Saengsuwan P (2014). High prevalence and molecular characterization of methicillin-resistant Staphylococcus aureus isolated from retailed meats, south Thailand. Int. Food Res. J., 21, 569–576.

• Buyukcangaz E, Velasco V, Sherwood JS, Stepan RM, Koslofsky RJ, Logue CM (2013). Molecular typing of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) isolated from animals and retail meat in North Dakota, United States. Foodborne Pathog. Dis. 10, 608–617. https://doi.org/10.1089/fpd.2012.1427

• C Narvaez-Bravo MFM, T Jackson S Jackson, A Rodas-Gonzalez, K Pond, A Echeverry, M M. Brashears (. Salmonella and Escherichia coli O157:H7 prevalence in cattle and on carcasses in a vertically integrated feedlot and harvest plant in Mexico. J. Food Protec. 2013; 76(5):786-795. https://doi.org/10.4315/0362-028X.JFP-12-079

• Cha JO, Lee JK, Jung YH, Yoo JI, Park YK, Kim BS, Lee YS (2006). Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J Appl Microbiol., 101(4):864–871. https://doi.org/10.1111/j.1365-2672.2006.02957.x

• Clements A, Young JC, Constantinou N, Frankel G (2012). Infection strategies of enteric pathogenic Escherichia coli. Gut Microbes. Mar-Apr. 3(2):71-87. https://doi.org/10.4161/gmic.19182.

• Crim SM, Griffin PM, Tauxe R, Marder EP, Gilliss D, Cronquist AB, Cartter M, Tobin-D’Angelo M, Blythe D, Smith K, et al. (2015). Preliminary incidence and trends of infection with pathogens transmitted commonly through food—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2006–2014. Morb. Mortal. Wkly. Rep. 64: 495-498. https://doi.org/10.15585/mmwr.mm6711a3

• Datta S A, Akter A, Shah IG, Fatema K, Islam TH, Bandyopadhyay A, Khan ZUM, Biswas D (2012). Microbiological quality assessment of raw meat and meat products and antibiotic susceptibility of isolated Staphylococcus aureus. J. Agric. Food Anal. Bacteriol., 2: 187-195.

• Dhup V, Kearns AM, Pichon B, Foster HA (2015). First report of identification of livestock-associated MRSA ST9 in retail meat in England. Epidemiol. Infect., 143, 2989–2992. https://doi.org/10.1017/S0950268815000126

• Donnelly CB, Leslie JE, Black LA, Lewis KH (1967). Serological identification of enterotoxigenic Staphylococci from cheese. J. Appl. Microbial., 15, (6): 1382 – 1387.

• Duffy EA, Belk K, Sofos JN, Levalley SB (2001). Microbial contamination occurring on lamb carcasses processed in the United States. J. Food Protec., 64(4): 503-8. https://doi.org/10.4315/0362-028X-64.4.503

• Duc J Vugai, Michael Samuel, Monica M Farley, Ruthanne Marcus, Beletshachew Shiferaw, Sue Shallow, Kirk Smith, Frederick J Angulo. Invasive Salmonella infections in the United States, FoodNet, 1996-1999: incidence, serotype distribution, and outcome. Clin Infect. Dis.  2004; 38 Suppl 3: S149-56. https://doi.org/10.1086/381581

• Ead-Hoiam A, Abdelgadir A (2019). Detection of Salmonella in Cattle and their Carcasses at Karary Slaughterhouse, Khartoum State, Sudan. Preventive Medicine and Public Health, Fac. Vet. Med. Univ. of Khartoum, Sudan. 14(10): 952-960.

• EC “ Commission regulation” (2005). No. 2073/2005. Microbiological criteria for foodstuffs. Official J. of the European Union. Commission Regulation of the European Union

• Egyptian Standard Specification “ESS”, (2004). (No.4334/2004): Fresh meat. Egyptian Organization for Standardization and Quality Control.

• El Sayed AA (2019). Bacteriological and molecular studies on antibiotic resistant Escherichia coli isolated from meat and its products in Kaliobia Egypt. Benha Vet. Med. J., 36(2): 335-344. https://doi.org/10.21608/BVMJ.2019.15531.1058

• Elsharawy-Nagwa T, Mahran HA (2018). Determination of Hygienic Condition of Municipal Slaughterhouse and Its Microbial Effect on the Meat Quality. AJVS, 59(1): 11-18.

• El-Shater-Nahla S (2010). Evaluation of immunological and bacteriological patterns of some food poisoning micro-organisms (Staphylococcus aureus and Clostridium perfringens) Ph.D. Thesis, Zagazig University.

• Ercolini D, Russo F, Torrieri E, Masi P, Villani F (2006). Changes in the spoilage related microbiota of beef during refrigerated storage under different packaging conditions. Appl. Environ. Microbiol., 72 (7): 4663-4671. https://doi.org/10.1128/AEM.00468-06

• Eshraghi S (2009). Prevalence of tst, entC, entA and entA/C genes in Staphylococcus aureus strains isolated from different foods. Danishkadah Pezeshki. 2009; 67 :470–476.

• FDA “Food and Drug Administration” (2018). Center for Food Regulation and Research. CFRR ELECTRONIC REGISTRATION USER BOOKLET

• Fegan N, Vanderlinde P, Higgs G, Desmarchelier PA (2005). study of the prevalence and enumeration of Salmonella enterica in cattle and on carcasses during processing. J. Food Prot., 68:1147–1153. https://doi.org/10.4315/0362-028X-68.6.1147

• Fisher EL, Otto M, Cheung GYC (2018). Basis of Virulence in Enterotoxin-Mediated Staphylococcal Food Poisoning. Front Microbiol., 9: 436. https://doi.org/10.3389/fmicb.2018.00436

• Food and Drug Administration (FDA) (2001). Staphylococcus aureus. Bacteriological analytical manual. 8th Ed. Chapter 12. Gaithersburg, p.562

• FSANZ “Food safety Australian New Zealand” (2016). Compendium of microbiological criteria in food. www.foodstandards.gov.au

• Ge. B, Mukherjee S, Hsu CH, Davis JAl, Tran TTT, Yang Q, et al (2017). MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats, 2010–2011. Food Microbiol., 62: 289–297. https://doi.org/10.1016/j.fm.2016.10.029

• Gorman R, Bloomfield S, Adley – Catherine C (2002). A study of cross contamination of food-borne pathogens in the domestic kitchen in the Republic of Ireland. Int. J. Food Microbiol ., 76(1- 2):143-150. https://doi.org/10.1016/s0168-1605(02)00028-4

• Greig J, Lalor K, Ferreira C, McCormick E (2001). An outbreak of Salmonella typhimurium phage type 99 linked to a hotel buffet in Victoria. Commun. Dis. Intell. Q. Rep.,  25: 277–278. 

• Gyles CL (2007). Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci., 85(13): 45-62. https://doi.org/10.2527/jas.2006-508

• Hamed EA, Ahmed AS, Abd El-Aaty MF (2015). Bacteriological hazard associated with meat and meat products. Egypt. J. Agric. Res., 93, 4 (B): 385-393

• Hemmat M, Reham A, Omima A, El Shafay M (2014). Quality of beef and edible offal at abattoir level. Benha Vet. Med. J. 25(2): 254-263.

• Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DMA, Jensen AB, Wegener HC, Aarestrup FM (2007). Global monitoring of Salmonella serovar distribution from the World Health Organization global foodborne infections network country data bank: Results of quality assured laboratories from 2001 to 2007. Foodborne Pathog. Dis. 2011;8: 887–900. https://doi.org/10.1089/fpd.2010.0787

• Holeckova B, Holoda E, Fotta M, Kalinacova V, Gondol J, Grolmus J (2002). Occurrence of enterotoxigenic Staphylococcus aureus in food. Ann. Agric. Environ. Med., 9 (2):179–82

• Hughes F, Adu-Gyamfi A, Appiah V (2015). Microbiological and parasitological quality of local beef retailed in Accra and radiation sensitivity of Salmonella sp. Int. J. Current Microbiol. Appl. Sci. 4(4): 86-96.

• Hussain MA, Dawson CO (2013). Economic impact of food safety outbreaks on food businesses. Foods 2, 585–589. https://doi.org/10.3390/foods2040585

• Hussein HS (2007). Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their product. J. Anim. Sci., 85(13): 63-72. https://doi.org/10.2527/jas.2006-421

• ICMSF “International Commission on Microbiological Specifications for Foods” (2011). Microorganisms in Foods 8, Katherine MJ Swanson, editorial committee chair. Springer New York Dordrecht Heidelberg London.

• ISO “ International Organization for Standardization” 6579-1 (2017). Microbiology of food and animal feeding stuffs — Horizontal method for the detection of Salmonella spp. 4th ed., Geneva, Switzerland

• ISO “International Organization for Standardization” 16649-2 (2001). Microbiology of food and animal feeding stuffs -- Horizontal method for the enumeration of Beta-X-glucuronidase-positive Escherichia coli -- Part 2: Colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide.

• Jackson CR, Davis JA, Barrett JB (2013). Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J. Clin. Microbiol. 51: 1199–1207. https://doi.org/10.1128/JCM.03166-12

• Johnson J, Kuskowki M, Menard M, Gajewski A, Xercavins M, Garau J (2006). Similarity between human and chicken E. coli isolates in related to ciprofloxins resistance status. Infect. Dis., 194(1): 71- 78. https://doi.org/10.1086/504921

• Kalalou I, Faid M, Ahami AT (2004). Extending the shelf life of fresh minced camel meat at ambient temperature by Lactobacillus delbruekii subsp. delbruekii. Electronic J. Biotechnol., 7: 246-251. https://doi.org/10.4067/S0717-34582004000300005

• Kalyapure R.A, Sherikar AT, Paturkar AM, Waskar VS, Zende R.J (1994). Microbiological survey on buffalo meat sold at retail market in the city of Bombay XV Annual conference of Indian Association of Veterinary Microbiologist, Immunologist and specialist in infectious diseases. Dec 27-29 Bombay Abstr No.3:16.

• Kamana B, Kalyan R, Dhiren SL, Hemanta K (2018). Food-borne bacterial pathogens in marketed raw meat of Dharan, eastern Nepal. BMC Res. Notes, 11, 618. https://doi.org/10.1186/s13104-018-3722-x

• Kauffman G (1974). Kauffmann white scheme. J. Acta. Path. Microbiol. Sci., 61:385.

• Kim HJ, Kim D, Song SO, Goh YG, Jang A (2016). Microbial status and guideline for raw chicken distributed in Korea. Korean. J. Poult. Sci., 43:235–242. https://doi.org/10.5536/KJPS.2016.43.4.235

• Kitai S, Shimizu A, Kawano J, Sato E, Nakano C, Kitagawa H, et al (2005). Prevalence and characterization of Staphylococcus aureus and enterotoxigenic Staphylococcus aureus in retail raw chicken meat throughout Japan. J. Vet. Med. Sci. 67: 269–274. https://doi.org/10.1292/jvms.67.269

• Ko EK, Heo EJ, Kim YJ, Park HJ, Wee SH, Moon JS (2013). Evaluation of microbiological contamination level of raw beef from retail markets in Seoul, Korea. Korean J. Food Sci. Anim. Resour., 33:403–410. https://doi.org/10.5851/kosfa.2013.33.3.403

• Koffi-Nevry R, Koussemon M, Coulibaly S (2011). Bacteriological quality of beef offered for retail sale in Cote d’Ivoire. Am. J. Food Technol. 6(9): 835–842. https://doi.org/10.3923/ajft.2011.835.842

• 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.

• Li QZ, Sherwood JS, Logue CM (2004). The prevalence of Listeria, Salmonella, Escherichia coli and E. coli O157:H7 on bison carcasses during processing. Food Microbiol. 21 (6):791-799. https://doi.org/10.1016/j.fm.2003.12.006

• Mathieu AM, Isigidi BK, Devriese LA, Godard C, Vanhoof R (1991). Characterization of Staphylococcus aureus and Salmonella spp. strains isolated from bovine meat in Zaïre. Int. J. Food Microbiol., 14(2):119–125. https://doi.org/10.1016/0168-1605(91)90098-A

• Mc Evoy MC, et al (2003). The prevalence of Salmonella spp. in bovine fecal, rumen and carcass samples at a commercial abattoir. J. Appl. Microbiol. 94.4 (2003): 693-700. https://doi.org/10.1046/j.1365-2672.2003.01898.x

• Moawad AA, Hotzel H, Awad O, Tomaso H, Neubauer H, Hafiz HM, ElAdawy H. (2017). Occurrence of Salmonella enteric and Escherichia coli in raw chicken and beef meat in northern Egypt and dissemination of their antibiotic resistance markers. Gut Pathogens. 9(57): 2-13. https://doi.org/10.1186/s13099-017-0206-9

• Monaghan A, Byrne B, Fanning S, Sweeney T, McDowell D, Bolton DJ (2011). Serotypes and virulence profiles of non-O157 Shiga toxin-producing Escherichia coli isolates from bovine farms. Appl. Environ. Microbiol., 77: 8662–8668. https://doi.org/10.1128/AEM.06190-11

• Muhammad M, Fazline F, Jasbir S, Arshad M, Mohd Azam K, Al-Sultan I (2011). Isolation of bacteria from bovine meat obtained from backyard slaughter in Kelantan. J. Adv. Med. Res. 1:61-64.

• Muhammad S, Erkihun A, Arshad M, Al-Sultan I (2012). The penetrability of selected bacteria on the raw bovine meat. J. Adv. Med. Res. 212-217

• Muluneh G, Kibret M (2015). Salmonella spp. and risk factors for the contamination of slaughtered cattle carcass from a slaughterhouse of Bahir Dar Town, Ethiopia. Asian Pacific J. Trop. Dis. 5(2): 130-135. https://doi.org/10.1016/S2222-1808(14)60640-X

• Narvaez-Bravo C, Miller MF, Jackson T, Jackson S, Rodas-Gonzalez A, Pond K, Echeverry A, Brashears MM (2013). Salmonella and Escherichia coli O157:H7 prevalence in cattle and on carcasses in a vertically integrated feedlot and harvest plant in Mexico. J Food Prot. 76(5):786-95. https://doi.org/10.4315/0362-028X.JFP-12-079. PMID: 23643120.

• Nørrung B, Andersen JK, Buncic S (2009). Main Concerns of Pathogenic Microorganisms in Meat Safety of Meat and Processed Meat. F. Toldrá, ed. (Springer New York), 3-29.

• Normanno G, Al Salandra G, Dambrosio A, Quaglia NC (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. International J. Food Microbiol., 115(3): 290-6. https://doi.org/10.1016/j.ijfoodmicro.2006.10.049

• Normanno G, Firinu A, Virgilio S, Mula G, Dambrosio A, Poggiu A, Decastelli L, Mioni R, Sucuota S, Bolzoni G, Digiannatale E, Salinetti AP, Lasalandra G, Bartoli M, Zuccon F, Pirino T, Sias S, Parisi A, Quaglia NC, Celano GV (2005). Coagulase positive Staphylococci and Staphylococcus aureus in foods products marketed in Italy. Food. Microbiol. 2005; 98:73–79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008

• Philips D, Jordan D, Morris S, Jenson I, Sumner J (2007). A national survey of the microbiological quality of retail raw meats in Australia. J. Food. Protec., 71(6): 1232-1236. https://doi.org/10.4315/0362-028x-71.6.1232

• Qadri F, Svennerholm AM, Faruque AS, Sack RB (2005). Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clinic. Microbiol. Rev., 18(3):465-83. https://doi.org/ 10.1128/CMR.18.3.465-483.2005

• Rahimi E(2012). Prevalence and antimicrobial resistance of Salmonella spp. in Iran. Revue de Med. Vet. 163.6 (2012): 271-275.

• Reid CA, Small A, Avery SM, Buncic S (2002): Presence of foodborne pathogens on cattle hides. Department of Clinical Veterinary Science, Research reports Division of Food Anim. Sci. Univ. of Bristol. UK, 134-135. https://doi.org/10.1016/S0956-7135(01)00050-0

• Rhoades JR, Duffy G, Koutsoumanis K (2009). Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review. Food Microbiol., 26(4):357-76. https://doi.org/ 10.1016/j.fm.2008.10.012

• Ruby J, Zhu RJ, Ingham SC (2007). Using indicator bacteria and Salmonella test results from three large-scale beef abattoirs over an 18-month period to evaluate intervention system efficacy and plan carcass testing for Salmonella. Journal of Food Protection., 70 (12):2732-2740. https://doi.org/10.4315/0362-028x-70.12.2732

• Saad SM, Ali ME, Awadeen -Manal OA (2019). Prevalence of some pathogenic organisms in cattle carcasses. BENHA Vet. Med. J., 36(2): 252-255.

• Salman AM, Abdella HH, Mustafa EA (2015). Some Quality Aspects of Fresh and Refrigerated Beef Cuts in Alkadaro slaughterhouse, Khartoum-Sudan. J. Appl. Indust. Sci., 3(2): 52-57

• Shaltout FA, Maarouf AA, El-Kewaiey IA, Heweidy AY (2016).Prevalence of some foodborne microorganisms in meat and meat products. Benha Vet. Med. J., 31(2): 213-219.

• Shawish, R.R. and Al-Humam, N.A. (2016): Contamination of beef products with staphylococcal classical enterotoxins in Egypt and Saudi Arabia. GMS Hyg and Infec. Control J., 2016: 11. https://doi.org/10.3205/dgkh000268

• Sibhat B, Zewde BM, Zerihun A, Cole L, Boerlin P, Muckle-Anne C (2011). Salmonella serovars and antimicrobial resistance profiles in beef cattle, slaughterhouse personnel and slaughterhouse environment in Ethiopia. Zoonoses Public Heal., 58(2): 102-9. https://doi.org/10.1111/j.1863-2378.2009.01305.x

• Slements A,Young JC, Constantinou N, Frankel G (2012). Infection strategies of enteric pathogenic Escherichia coli. Gut Microbes J., 3(2): 71-78. https://doi.org/10.4161/gmic.19182

• Steffen R, Castelli F, Nothdurft DH, Rombo L, Jane Zuckerman JN (2005).Vaccination against enterotoxigenic Escherichia coli, a cause of travelers’ diarrhea. J. Travel Med., 12(2):102-7. https://doi.org/10.2310/7060.2005.12207

• Tang Y, Larsen J, Kjeldgaard J, Andersen PS, Skov R, Ingmer H (2017).Methicillin-resistant and -susceptible Staphylococcus aureus from retail meat in Denmark. Int. J. Food Microbiol. 249, 72–76.

• Tassew H, Abdissa A, Beyene G, Gebre-Selassie S (2010). Microbial flora and foodborne pathogens on minced meat and their susceptibility to antimicrobial agents. Ethiop J. Health Sci., 20(3): 137–143. https://doi.org/10.4314/ejhs.v20i3.69442

• USDA (2016). United States Department of Agriculture Foreign Agricultural Service Foreign Ag Service Verified account @USDAForeignAg.

• Van Loo IH, Diederen BM, Savelkoul PH, Woudenberg JH, Roosendaal R, Van BA, et al (2007). Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg. Infect. Dis., 13, 1753–1755. https://doi.org/10.3201/eid1311.070358

• Venkataraman K, Nakano H, Kawakami H, Hashimoto H (1988). Microbiological aspects and recovery of Salmonella in retailed foods. J. of the faculty of applied Biological Sci., Hiroshima University. 27(1): 33-39. http://doi.org/10.15027/23484

• Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S, Smith K, Angulo FJ (2004). Emerging Infections Program FoodNet Working Group. Invasive Salmonella infections in the United States, FoodNet, 1996-1999: incidence, serotype distribution, and outcome. Clin Infect Dis. 15;38 Suppl 3:S149-56. http://doi.org/10.1086/381581.

• Wieneke AA, Roberts D, Gilbert RJ (1993). Staphylococcal food poisoning in the United Kingdom, 1969-90. Epidemiol. Infect., 110(3): 519–531. https://doi.org/10.1017/s0950268800050949

• Wu S, Huang J, Wu Q, Zhang F, Zhang J, Lei T (2018). Prevalence and characterization of Staphylococcus aureus isolated from retail vegetables in China. Front. Microbiol., 9:1263. https://doi.org/10.3389/fmicb.2018.01263

• Zargar MHS, Doust RH, Mobarez AM (2014). Staphylococcus aureus enterotoxin a gene isolated from raw red meat and poultry in Tehran, Iran. Int. Enteric Pathog. J., 2(3): e16085. https://doi.org/10.17795/ijep16085

• Zweifel C (2003). Microbiological monitoring of sheep carcass contamination in three Swiss abattoirs. J. Food Protec., 66(6): 946-52. https://doi.org/10.4315/0362-028x-66.6.946

• Zweifel C, Fischer R, Stephen R (2008). Microbiological contamination of pig and cattle carcasses in different small-scale Swiss abattoir. J. Meat Sci., 78: 225-231. https://doi.org/10.1016/j.meatsci.2007.06.025