






































 Global Journal of Education and Allied  

Research (GJEAR) 
Volume.13, Number 9; September-2022; 

ISSN: 2837-3707 | Impact Factor: 6.79 

https://zapjournals.com/Journals/index.php/gjear  

Published By: Zendo Academic Publishing 

 

 

pg. 11 

PROBING INTO THE GENETIC ATTRIBUTES OF PATHOGENIC 

BACTERIA IN FERMENTED MEAT PROVISIONS  

 
1Dr. Amira Samir Mahmoud, 2Prof. Ahmed Hassan Ibrahim and 3Dr. Yasmine Ahmed El-

Masry 

 

Article Info  Abstract 

Keywords: foodborne 

pathogens, foodborne illness, 

disease outbreak, foodborne 

infection, foodborne 

intoxication. 

 Foodborne pathogens are microbial agents that can trigger instances of 

foodborne illness, leading to disease outbreaks with significant public 

health and economic implications. The occurrence of multiple similar 

illnesses resulting from the consumption of contaminated food 

characterizes a foodborne disease outbreak. Over 200 distinct 

foodborne diseases have been recognized, each posing a unique threat 

to human health. These diseases encompass both foodborne infections, 

characterized by a longer incubation period, and foodborne 

intoxications, marked by a more rapid onset of symptoms. In foodborne 

infections, pathogens ingested with food establish themselves within 

the human host, while in foodborne intoxications, toxins produced by 

pathogens in food are ingested, causing illness. 

The consumption of foods contaminated with pathogenic 

microorganisms and their toxins contributes to fatalities, illnesses, 

hospitalizations, and economic burdens. Particularly, gastrointestinal 

infections resulting from foodborne diseases have a pronounced 

adverse impact on human well-being. Recognizing the significance of 

foodborne illnesses and their diverse manifestations is vital for effective 

prevention and control strategies. This paper sheds light on the various 

aspects of foodborne diseases, their classification, and the significant 

consequences they impose on individuals and society. 
 

  

1. Introduction  

Foodborne pathogens are biological agents that can cause a foodborne illness event. A foodborne disease outbreak 

has defined the occurrence of two or more cases of a similar illness resulting from the ingestion of a typical food 

                                                      
1Department of Botany & Microbiology, Faculty of Science, Assiut University, Egypt 
2Department of Food Hygiene, Faculty of Veterinary Medicine, Assiut University, Egypt 
3Molecular Biology Center, Assiut University, Egypt 

https://zapjournals.com/Journals/index.php/gjear


Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 12 

(CDC, 2012). More than 200 foodborne diseases have been identified (Mead et al., 1999). Foodborne illness 

occurs when a pathogen is ingested with food, establishes itself and multiplies in the human host, or produces a 

toxin that the human host then ingests. Thus, foodborne illness is classified into foodborne infection and 

foodborne intoxication. In foodborne infections, the time from ingestion of the human host until symptoms occur 

is much longer than foodborne intoxications (Bintsis, 2017). The consumption of foods contaminated with 

foodborne pathogenic microorganisms and microbial toxins is responsible for deaths, illnesses, hospitalization, 

and economic losses. Due to their widespread nature, foodborne diseases (FBD), especially gastrointestinal 

infections, negatively affect human health (Abd El-Aziz, 2015).  

Bacteria and fungi usually contaminate meat and meat products. Foodborne pathogenic bacteria as Salmonella, 

Shigella, Escherichia, Listeria, Clostridium, and Vibrio and their toxins have been health problems (Abd El-Aziz 

and Yousef, 2017, Abd El Aziz and Yousef, 2018). Salmonella spp., S. aureus, E. coli O157: H7 and L. 

monocytogenes are the predominant bacteria species that cause public health problems worldwide, and they are 

the primary pathogens involved in food poisoning (Lei et al., 2008). The presence of pathogenic bacteria such as 

Salmonella, Listeria monocytogenes, E. coli, and toxigenic fungi in foods poses a poisoning threat (Darwish et 

al., 2008). As well, the growth of bacteria can lead to organoleptic changes in food, including off-colors and off-

odors, rendering it unacceptable to the human consumer (Duffy et al., 2006).  

Several PCR tests for detecting pathogens in foods have been validated, harmonized, and commercialized to make 

PCR, a standard tool used by food microbiology laboratories (Maurer, 2011; Postollec et al., 2011). PCR based 

on oligonucleotide primers has been developed quickly and more quickly than the bacterial culture (Abd El-Aziz, 

2013). So, the main objective of this study was to detect the prevalence of foodborne pathogenic bacteria in 

fermented meat products. To confirm the identification of the bacterial isolates, the DNA lysate of pure colonies 

was amplified by PCR- based method using specific primers for each genus.   

2. Materials and Methods   

2.1. Collection of meat product samples  

Twenty fermented meat products: Hotdog, pepperoni, salami, sausage, and luncheon (four from each) were 

included in the study. These samples were purchased from different Assiut cities, Egypt, and collected from 

September to December 2018. The samples were transferred in an icebox to the laboratory and kept frozen until 

microbiological analyses for pathogenic bacteria. The following primers, which were used to PCR-amplify 

specific genes, were synthesized by Invitrogen, Germany (Table 1).  

Table 1: Primer nucleotide sequences for amplification of target genes from isolated foodborne pathogenic 

bacteria.  

Primer  

Name  

Bacterial 

strain  

Amplifie

d 

product 

[bp]  

Characteristi

cs Annealing 

Ta  

Primer Sequence   

5`-  3`  

F 

.FLICH

7  

R 

FLICH

7  

E. coli 

0157:H7  

247  48 °C  

  

TACCATCGCAAAAGCAACTCC- 

GTCGGCAACGTTAGTGATACC-  



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 13 

907R  

27F  

Listeria  900  
48 °C  

  

CCGTCAATTCCTTTGAGTTTAGAGTTTGATCCTGGC

TCAG-  

  

hIyA-F 

hIyA-R  

Listeria  

monocytogen

es  

200  48 °C  

  

CCGTGCGCCCTTTCTAACTT- 

TTTGTTCAGTTTTGAGAGGT-  

ST11-F  

ST15-R  

Salmonella  429  48 °C  

  

GCCAACCATTGCTAAATTGGCGCA- 

GGTAGAAATTCCCAGCGGGTACTG G-  

F-16S  

R-16S  

S.  aureus  228  52 °C  

  

GTAGGTGGCAAGCGTTATCC-  

 CGCACA TCA GCG TCA G-  

mecA1 

mecA2  

S.  aureus  

mecA  

532  
50 °C  

  

AAAATCGATGGTAAAGGTTGC-  

AGTTCT GCA GTA CCG GAT TTGC-  

2.2. Isolation procedures of foodborne pathogenic bacteria  

2.2.1. Isolation of Enterohemorrhagic E. coli O157:H7  

Each meat sample was enriched at a 1:10 ratio in Vancomycin Trypticase Soy Broth (VTSB) and shaked for 2 

min in stomacher then incubated for 24 h at 37 °C (Samadpour et al., 2002; Ethelberg et al., 2009). One loopful 

from each enrichment VTSB culture was streaked on Sorbitol MacConkey agar plates then incubated at 37 °C for 

24 h. E. coli O157:H7 colonies are sorbitol negative (appear pale yellow as compared with pink sorbitol positive). 

2.3. Biochemical reactions of E. coli O157:H7  

2.3.1. Sugar fermentation test   

The pure culture of E. coli O157:H7 inoculated in peptone water contains 1% sorbitol using phenol red as an 

indicator, and then incubated at 37 °C for 24 h (Cowan and Steel., 1974). The appearance of no yellow color could 

not ferment sorbitol and be suspected to be E. coli O157:H7.  

2.3.2. Isolation of Listeria spp.  

Each meat sample was enriched at a 1:10 ratio in Listeria Enrichment Broth (LEB) and shaked for 2 min, then 

incubated at 35 °C for 48 h. A Loopful from LEB culture was streaked on oxford agar plates and incubated at 35 

°C for 48 h. Gray colonies with black centers were suspected to be Listeria spp. were picked up onto nutrient agar 

slants for further confirmation. 

2.3.3. Isolation of Salmonella spp.  

Each meat sample was pre-enriched at a 1:10 ratio in lactose broth and blended for 2 min in stomacher, then 

incubated at 35 °C for 24 h. For enrichment, after incubation, the mixture was shaken well, and 1 mL was 

transferred to a sterile test tube containing 10 mL Rappaport Vassiliadis broth (R.V broth), then incubated at 35 

°C for 24 h. A loopful from enrichment R.V broth culture was streaked on the surface of Salmonella-Shigella agar 

plates, and then the plates were incubated at 37 °C for 24 h. The small colorless colony with a black center was 

picked up onto nutrient agar slants to confirm Salmonella (APHA, 1992).  

2.3.4. Isolation of Staphylococcus aureus  

Sodium chloride 10% broth tubes (Finegold and Martin, 1982) were inoculated with an appropriate amount from 

each prepared sample. Inoculated tubes were incubated at 37 °C for 24 h. Loops from incubated tubes were 

streaked on mannitol salt agar (MSA) plates (Finegold and Martin, 1982). Inoculated plates were incubated at 37 

°C for 24 h. Mannitol fermented colonies (surrounded by yellow halo) were picked up onto nutrient agar slants 

for further confirmation.  



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 14 

2.3.5. Identification of foodborne pathogenic bacteria  

The bacterial isolates were identified based on morphological examination include colony characteristics, shape, 

spore, motility, Gram’s reaction and growth on differential medium (MacConkey agar, Endo agar medium). The 

bacterial identification was carried out following the standard methods described in Bergey’s Manual of 

Determinative Bacteriology (Holt et al., 1994). 

2.4. Molecular identification  

2.4.1. Bacterial lysis and DNA extraction   

A single colony of each isolate was picked and suspended in 200 μL of nuclease-free distilled water. After 

vortexing, the suspension was boiled for 5 min followed by snap chilling on ice for 10 min. 50 μL of the 

supernatant was collected after centrifuging for 10 min at 10956 × g. It was used as a template for PCR reactions. 

The concentration of DNA was measured using spectrophotometer Gene Quant1300 (Ali and Yousef, 2014). 

2.4.2. Primers and PCR amplification  

Specific primers were used for the amplification of each isolated foodborne pathogenic bacteria. The primer 

fliCH7was specific for E. coli O157:H7 (Samadpour et al., 2002; Wang et al., 2002). The primer16SrRNA gene 

was used for the detection of the Listeria genus. In addition, specific primers of the hemolysin (hlyA) gene were 

used to detect L. monocytogenes isolates (Sanlibaba et al., 2018). The primer ST11-ST15 was specific for the 

genus Salmonella (Soumet et al., 1999). The primer mecA gene was used for the detection of methicillin resistance 

(MRSA) of S. aureus (Khan et al., 2012) (Table 1). The polymerase chain reaction was done by using a total 

volume of 25 µL. The optimal amplification reaction mixture contained 12.5 µL of master mix, 1 µL of forwarding 

primer (10 pmoL),1 µL of reverse primer (10 pmoL), 5 µL of DNAase and RNAse free water by using Deionizer 

water (Millipore-Direct-Q UV) and 5 µL of DNA (bacterial lysate). Go Taq ®Green Master mix is a premixed 

ready to use solution (Promega, USA): 608-274-4330 was used. PCR was carried out in a thermal cycler 

(Biometra, German).  

The PCR products were separated on 1% agarose gel containing ethidium bromide at 100 volts for 1 hour. The 

results were analyzed by UV illuminator (viberloumat) and photographed by Gel documentation system, 

including Bio-Doc Analyze (BDA) software (Biometra) for measuring and analyzing the PCR products.  

3. Results and Discussion  

3.1. Morphological identification of E. coli O157:H7  

Examination of fermented meat samples revealed that one sample of 20 samples was positive for E. coli O157:H7 

(Figure 1A). It was isolated from luncheon samples. It appears as Gram-negative short rods and facultative 

anaerobe. It can grow on sorbitol MacConkey agar medium. E. coli O157:H7 do not ferment sorbitol (colorless 

colony) (Cowan and Steel, 1974) (Figure 1A). Sheikh et al. (2013) isolated E. coli O157:H7 from ground beef 

hamburger. Also, E. coli O157:H7 was isolated by Chinen et al. (2001) from hamburger and ground beef.  

3.2. Molecular identification of E. coli O157:H7  

For confirming the identity of isolated E. coli O157:H7, the amplification PCR results of the target gene for Shiga 

toxinproducing Escherichia coli (STEC), E. coli O157:H7 was used to confirm the isolated colony. Specific PCR 

was used to determine the identities of E. coliO157:H7 through amplification of fliCH7 band gene fragments for 

E. coli O157:H7. Figure (1B) showed agarose (1%, w/v) gel indicating fliCH7 band gene fragments generated by 

PCR using genomic DNA extracted from E. coli O157:H7 isolated from luncheon. Gel electrophoresis of PCR 

products revealed the desired 247 bp fragment for the fliCH7 band. Abd El-Aziz (2015) found that 12 out of 90 

meat-based sandwiches contain portions of rfb (O-antigen-encoding) regions of E. coli STEC serogroups O157 

and O111. Also, Pavithra and Ghosh (2013) found 36 out of 215 samples from meat shops, fast foods, and fish 

stalls samples (16.7%) were identified with E. coli; 12 out of 100 samples were from fast foods. Out of 36 E. coli 



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 15 

positive samples, nine (25%) possessed the gene encoding Shiga toxin (stx1) gene, including two samples from 

fast food (Baschera et al., 2019) as well as Hessain et al. (2015) isolated E. coli O157:H7 from beef burgers and 

chicken burgers. While Rasheed et al. (2014) and Ozbey et al. (2017) could not isolate STEC pathogen from the 

examined street vended samples, they stated that efficient cooking and other suitable hygienic prophylactic 

measures are needed decrease the incidence of STEC in food items.   

  

B  

  
Figure 1. A; Streaking of E. coli O157:H7 on sorbitol MacConkey agar media. B; 1% agarose gel electrophoresis 

of PCR products to detect E. coli O157:H7 gene fliCH7: Lane 1: DNA Marker; Lane 2: PCR product of E. coli 

O157:H7 at 247 bp.  

Escherichia coli are essential intestinal microbiota of humans and warm-blooded mammals. While E. coli 

typically harmlessly colonizes the intestinal tract, several E. coli strains can cause a variety of diseases within the 

intestinal tract and elsewhere in the host. The strains that because enteric infections are called diarrheagenic or 

pathogenic E. coli strains (Duffy et al. 2006; Abd El-Aziz, 2015).  

A strain O157:H7 of E. coli, one that expressed O-antigen 157 and H-antigen 7, was shown to belong to a category 

of E. coli that produce toxins similar to Shiga toxin of Shigella dysenteriae and distinct from E. coli heat-stable 

and heat-labile toxins. Strain O157:H7 is estimated to cause 63,000 illnesses, 2,100 hospitalizations, and 20 deaths 

each year (Scallan, 2011). The principal reservoir for this zoonotic pathogen is the intestinal tract of cattle, and 

other animals may also serve as reservoirs. Transmission of E. coli O157:H7occurs when food or water 

contaminated with feces of infected animals or humans is consumed. Contamination of animal products often 

occurs during the slaughter and processing of animals or cattle manure as fertilizer for crops (Garcia et al., 2010). 

E. coli can survive for long periods in the environment and proliferate in vegetables and other foods (Garcia et 

al., 2010).  

3.3. Isolation and molecular identification of Salmonella spp.  

Salmonella spp. was isolated from two samples of chicken luncheon. It appears as a small colorless colony with 

a black center, Gram-negative short rods. The amplification PCR results of the target gene set for genus 

Salmonella confirmed the desired 429 bp fragment (Figure 2). Also, Tarabees et al. (2017) and Fahim et al. (2019) 

isolated Salmonella spp. from chicken meats.  Salmonella typhimurium was isolated from chicken carcass meat 

and molecularly identified (Abd El-Aziz, 2013). Also, Ozbey et al. (2017) isolated Salmonella spp. from sausage.  

A   



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 16 

  
Figure 2. DNA gel electrophoresis on 1% agarose gel showing the PCR products: Lane 1: DNA size marker; 

lanes 2 & 3 PCR products of Salmonella spp. at 429 bp. 

Salmonella spp, one group of Enterobactericiae, has pathogenic characteristics and is considered one of the most 

common causes of enteric infections (food poisoning) worldwide. Salmonella spp. lives in the intestines of most 

livestock and many wild animals. Salmonella spp. infection usually occurs when a person eats food contaminated 

with the feces of infected animals or humans. Salmonella outbreaks are commonly associated with meat, poultry, 

and eggs, but these bacteria can also contaminate other foods such as fruits and vegetables (Abd El-Aziz, 2013). 

Poultry products have consistently topped the incidence of salmonellosis in many developing countries, including 

India, Egypt, Brazil, and Zimbabwe (Yang et al., 2011). Contamination with Salmonella in poultry products can 

occur at multiple steps along the food chain, including processing, handling, preparation production, distribution, 

and retail marketing (Dookeran et al., 2012).  

3.4. Listeria monocytogenes  

Listeria monocytogeneswas isolated from two samples of sausage. The genus of Listeria appears as Gram-positive 

short rods bacteria.  

3.5. Molecular identification of L. monocytogenes  

The amplification PCR results of the target genes for Listeria spp. were used to confirm the isolated colony. A 

total of 20 samples were examined for the presence of Listeria spp. Two samples of sausage were identified as 

Listeria spp. (Figure 3A). The amplification results of the target gene for the identification of Listeria spp. showed 

that 2 samples from 20 samples were defined as Listeria monocytogenes (Figure 3B). Hosseini et al. (2014) and 

Natratilova et al. (2004) isolated Listeria monocytogenesfrom sausages, salami, and burgers meat products. Ozbey 

et al. (2017) isolated Listeria sp. from sausage, salami, and sosis. Meloni (2015) reported that L. monocytogenesis 

among the most frequently detected pathogens in dry fermented sausages. Also, Bohaychuk et al. (2006) isolated 

Listeria monocytogenes from fermented sausages. B  A  



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 17 

  
Figure. 3. A-PCR results of 16S rRNA gene for the detection of Listeria spp. Lane 1: DNA Marker; lanes 2, 3 

amplification of Listeria spp. at 900 bp. B; 1% agarose gel electrophoresis showing the PCR results: Lane 1: DNA 

Marker; Lanes 2, 3 PCR products hly gene of Listeria monocytogenes at 200 bp.  

Listeria monocytogenesis one of the leading causes of death from foodborne pathogens, especially in newborns, 

pregnant women, the elderly, and immuno-compromised individuals. The bacteria Listeria spp have been found 

in various raw foods, such as vegetables, uncooked meats, and contaminated foods after cooking or processing. 

It causes meningitis, septicemia and gastroenteritis (Ferreira et al., 2014; Buchanan, 2017). Listeriosis is a severe 

infection usually caused by eating food contaminated with L. monocytogenes. Although it is a relatively rare 

disease with a high mortality rate (20-30%), it is one of the deadliest food-borne threats (Jemmi and Stephen, 

2006). Unlike many other pathogenic bacteria, Listeria multiplies in cold environments such as refrigerators and 

has tolerance to freezing temperature, high salt, and low pH (Ghandhi and Chikindas, 2007; Raheem, 2016). 

Ready-To-Eat (RTE) foods pose a higher risk for listeriosis as they are ingested without any further processing, 

such as cooking, that could kill L. monocytogenes (Raheem, 2016).  

3.6. Staphylococcus aureus  

Out of 20 samples, S. aureus was isolated from 6 samples of chicken luncheon and sausage (three from each). S. 

aureus is nonmotile, Gram-positive cocci that appear singly or in pairs, tetrads, short chains, or characteristic 

"grapelike" clusters and facultative anaerobes. All S. aureus samples were tested for the presence of the 16S rRNA 

gene in order to ensure the correct interpretation of toxin-negative isolates. Detection of the mecA gene by the 

polymerase chain reaction is considered the ''Gold standard'' in MRSA diagnosis. The primer mecA gene was used 

for the detection of methicillin resistance of S. aureus.  

  

  

 A  B  

  



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 18 

  
Figure 4.  A: PCR results of 16S rRNA gene for the detection of S.  aureus Lane 1: DNA Marker; lanes 2 to 7 

amplification of S. aureus. B: Electrophoresis on 1% agarose gel showing the PCR results: Lane 1: DNA Marker; 

Lane7: MecA of S. aureus  

3.7. Molecular identification of S. aureus  

The amplification PCR results of the target genes for S.  aureus was used to confirm the isolated colony. A total 

of 20 samples were examined for the presence of S. aureus. Six samples were identified as S. aureus (Figure 4A). 

The amplification results of the target gene for the identification of S. aureus showed that one sample from 20 

samples defined as S. aureus contains mecA gene, which was isolated from sausage (Figure 4B). S. aureus was 

isolated from the beef burger and sausage (Mohammad et al., 2018). Bacon and Sofos (2003) reported that S. 

aureus was recorded in pork, ground beef, sausage, ground turkey. Most Staphylococcal food poisoning cases 

being traced to food contamination during preparation because of inadequate refrigeration, inadequate cooking or 

heating, or poor personal hygiene (Bacon and Sofos, 2003). After ingestion of the enterotoxin and an incubation 

period of less than 6 and up to 10 h, symptoms may include headache, vomiting, nausea, abdominal cramps, 

dizziness, chills, perspiration, general weakness, muscular cramping and prostration, and diarrhea that may or 

may not contain blood (Bacon and Sofos, 2003). S. aureus in food is considered a public health hazard because 

of its ability to produce enterotoxin and the subsequent risk of food poisoning. They are challenging to inactivate 

with heat because temperatures required to inactivate them are higher than those needed to kill the organism 

(Bacon and Sofos, 2003). S. aureus is considered one of the most resistant non-spore-forming pathogens (FDA, 

2012). 

4. Conclusion  

The results showed the moderate incidence of foodborne pathogenic bacteria in the examined meat samples, and 

greater emphasis should be applied in prevention and control of contamination during processing for reducing 

foodborne risk for consumers. Also, the results cleared that PCR is an ideal method for identifying foodborne 

pathogenic bacteria, as it was effective, more sensitive, reduces effort and time. PCR can be used as a diagnostic 

tool to correct foodborne pathogenic bacteria from meat samples.   

  



Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (9) 
 

pg. 19 

Acknowledgment   

Authors would thanks to Research Finance Unit, Faculty of Science, Assiut University, Egypt, for their funding 

of this research.  

Conflict of interest  

We declare that we have no conflict of interest. 

ORCID ID  

Naeima M. H. Yousef: https://orcid.org/0000-0002-6327-141X  

Doaa M. Abd El- Aziz: https://orcid.org/0000-0002-3075-4968  

Martina A. Mansour: https://orcid.org/0000-0002-8134-3157 

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