Global Journal of Education and Allied Research (GJEAR) Volume.13, Number 10; October-2022; ISSN: 2837-3707 | Impact Factor: 6.79 https://zapjournals.com/Journals/index.php/gjear Published By: Zendo Academic Publishing pg. 11 EXAMINING MICROBIAL QUALITY IN READY-TO-EAT FOODS OF MAKKAH'S CAFETERIAS 1Ahmed Khalid Al-Faisal and 2Aisha Abdullah Al-Mansoori Article Info Abstract Keywords: Ready-to-eat foods, RTE, contamination, microorganisms, food safety. The consumption of ready-to-eat foods (RTEs) has witnessed a surge in the Kingdom of Saudi Arabia, particularly in the city of Makkah, owing to shifting demographics and lifestyle changes. This trend is influenced by the influx of itinerant workers, pilgrims, and visitors, leading to an increased preference for convenient RTE options, especially for breakfast. Cafeterias offering RTE foods have gained popularity due to their affordability, accessibility, and convenience. However, certain RTE food items, including those containing animal-derived ingredients like eggs, fish, meat, and poultry, are susceptible to contamination by various microorganisms such as bacteria and fungi. The contamination of RTE foods during processing and sandwich preparation has been reported, potentially resulting in cross-contamination and the presence of pathogenic microorganisms like Staphylococcus aureus, Salmonella species, Bacillus species, and Escherichia coli. Consequently, the quality of RTE foods can be significantly compromised. In this context, understanding the factors contributing to the contamination and deterioration of RTE foods is crucial for ensuring food safety and public health. This study aims to investigate the prevalence and implications of microorganism contamination in RTE foods in Makkah, Saudi Arabia, and proposes strategies to enhance the safety and quality of RTE meals. Introduction Ready-to-eat foods (RTEs) are items prepared in advance and ready for consumption only after heating without further processing or preparations. It could be raw or cooked meals. RTE food items consumption has recently 1Environmental Health Department, Faculty of Public Health & Health Informatics, Umm Al-Qura University, Makkah, Saudi Arabia 2 Epidemiology Department, Faculty of Public Health & Health Informatics, Umm Al-Qura University, Makkah, Saudi Arabia https://zapjournals.com/Journals/index.php/gjear Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 12 increased in the Kingdom of Saudi Arabia, mainly in holly Makkah city, due to the rapid demographic change characterized by a change in lifestyle and a large number of itinerant workers, visitors, and pilgrims resulting in a large percentage of the population taking ready-to-eat food especially as breakfast’s meal. In addition, cafeterias that serve RTE foods provide cheap, economical, and easily accessed items. Some RTE foods items contain raw materials of animal origin, such as eggs, fish, meat, and poultry, which can easily get contaminated by different microorganisms, including bacteria and fungi (Ashenafi, 1995). The cross-contamination of RTE foods with pathogenic microorganisms could occur during the processing and preparation of fillings and sandwiches (Oranusi et al., 2013; Rahman et al., 2014; Sharma et al., 2014). Contamination of RTE food by pathogenic microorganisms like Staphylococcus aureus, Salmonella species, Bacillus species, and Escherichia coli leads to remarkable changes in food quality. Moreover, consequently causing food-borne illnesses and food poisoning are considered major public health issues that negatively affect the socioeconomic development and output of many fields such as tourism and trading (Newman et al., 2015). Food-borne diseases and food poisoning problems are becoming an important issue worldwide (Al-Mazrous, 2004). In the Kingdom of Saudi Arabia in general and holly Makkah city in particular, food-borne illness and food poisoning are emerging as significant public health threats that render a high burden of diseases and negatively affect the socioeconomic development and productivity of many sectors. Several studies have reported that foods served by catering services were the primary source of many food-borne outbreaks (Osimani and Clementi, 2016). In Makkah city, increasing food poisoning cases were reported, especially during the Hajj and Umrah seasons. It was mainly due to the high consumption of RTE meals, especially those from cafeterias (Shirah et al., 2017). We think minimizing fungal and bacterial loads in RTE foods served in cafeterias within Makkah city by following good hygiene practices and continuous microbiological assessment programs is necessary. Moreover, using microbiological testing results of RTE foods in Makkah city will provide an example for other cities in Saudi Arabia for dealing with ready food. However, very little research has been carried out on assessing microbial quality and safety of RTE foods in Saudi Arabia, especially those distributed within Makkah city. Therefore, this study aimed to determine the microbial safety of RTE food items that are served in some cafeterias in Makkah city, Saudi Arabia. Materials and Methods Sample Collection Ready-to-eat food samples were collected randomly from different cafeterias located in different sites of Makkah City during the period March-April, 2021. A total of 108 samples represented six different types of ready-to-eat food (foul, falafel, boiled egg, fried egg, shakshuka, and sheep liver slices) collected from six different cafeterias and replicated three times. Collected samples were handled in sterile plastic bags and directly transferred to the microbiology lab for investigation. Microbiological Analysis Isolation and enumeration of bacteria. Ten grams of each experimental sample was mixed with 90 mL Nutrient Broth (Biotech, UK), and serial dilutions of each food sample homogenate were prepared to reach 10-3 dilutions. A 1 mL aliquot portions of the prepared dilutions were precisely distributed onto duplicate sterile plates of Nutrient Agar (Himedia, India), Eosin Methylene Blue (EMB) Agar (Titan Biotech, India), and Mannitol Salt Agar (MSA) (India mart, India) for total microbial load, Escherichia coli, and Staphylococcus aureus, respectively. Counting of bacterial colonies was performed after incubation of agar plates at 37 °C for 24 to 48 h, Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 13 by using the colony counter (Gallenkamp, England). Bacterial colonies were expressed as colony-forming units per mL of sample homogenate (CFU/mL). Isolation and enumeration of fungi. For fungal isolation, 10 grams of each sample were mixed in Sabouraud broth (India mart, India), and the same dilutions were prepared. A 1 mL portion of the dilution (10-3) was poured onto Sabouraud agar (India mart, India) medium supplemented with 0.005 gram/liter of rose Bengal (Sigma Aldrich, USA) for suppressing bacterial growth. The agar plates were incubated at 28 °C for 5-7 days; then, the developed colonies were counted and identified. Identification of Microbial Isolates. The developed bacterial colonies were counted using colony counter, purified, and stored on nutrient agar slants at 4 °C for identification. Identification based on cultural morphology and biochemical tests, including carbohydrate utilization on Tri-sugar Iron (TSI) medium, IMViC test, starch hydrolysis, gelatin liquefaction, nitrate reduction, oxidase urease activity, and motility test were employed to confirm the purity of the isolates. The fungal morphology was studied macroscopically by observing the colony features (color, shape, size, and hyphae) and microscopically by a compound microscope according to the following references Gaddeyya et al. (2012), Domsch et al. (1980), and Barnett & Hunte (1972). Results and Discussion Bacterial species isolated from ready-to-eat foods samples A total of 108 food samples, including 6 types (foul, falafel, boiled eggs, fried eggs, shakshuka, and sheep liver slices), were evaluated. The results showed in Table 1 that the highest aerobic plate counts were found in sheep liver slices sold by Cafeteria No 5 with the value of 8.4 × 103 CFU/mL, while the lowest value was detected in foul sold by Cafeteria No.2 with a value of 0.5 × 103 CFU/mL. S. aureus appeared in all food samples collected from all cafeterias. The highest count (9.8 × 103 CFU/mL) for S. aureus was detected in shakshuka sold by Cafeteria No.6, while the lowest count (1.2 × 103 CFU/mL) was observed in falafel sold by Cafeteria 1. Generally, it could be reported that all the tested samples were highly contaminated with S. aureus, and 42% of the samples were contaminated with E. coli. The total counts for S. aureus and E. coli (in shakshuka and sheep’s liver slices) exceeded the recommended levels by the International Commission on Microbiological Specifications for Foods (ICMSF, 1996). The ICMSF (1996) recommends that ready-to-eat foods between 0-103 CFU are acceptable, 104- 105 CFU is tolerable, and 106 CFU and above are unacceptable. Table 1. Mean total counts (CFU/mL) of each bacterial species isolated from ready-to-eat foods samples sold in Makkah city. Vendors samples station Food types Bacteria Aerobic plate count S. aureus count E. coli count Cafeteria 1 Foul 2.4 ×103 3.6 ×103 ND Falafel 3.5 ×103 1.2 ×103 ND Boiled egg 1.2 ×103 4.6 ×103 ND Fried egg 2.5 ×103 1.3 ×103 ND Shakshuka 5.7 ×103 4.3 ×103 0.4 ×103 Sheep liver slices 6.3 ×103 3.1 ×103 0.5 ×103 Cafeteria 2 Foul 0.5 ×103 3.4 ×103 1.2 ×103 Falafel 3.4 ×103 5.2 ×103 ND Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 14 Boiled egg 3.2 ×103 2.5 ×103 ND Fried egg 1.5 ×103 3.3 ×103 ND Shakshuka 4.3 ×103 6.4 ×103 2.3 ×103 Sheep liver slices 5.9 ×103 3.6 ×103 0.6 ×103 Cafeteria 3 Foul 1.5 ×103 3.5 ×103 ND Falafel 3.2 ×103 4.1 ×103 ND Boiled egg 1.1 ×103 3.2 ×103 ND Fried egg 0.9 ×103 3.7 ×103 1.1 ×103 Shakshuka 5.9 ×103 7.5 ×103 2.4 ×103 Sheep liver slices 4.5 ×103 7.5 ×103 1.6 ×103 Cafeteria 4 Foul 4.2 ×103 8.7 ×103 ND Falafel 3.4 ×103 4.3 ×103 ND Boiled egg 2.8 ×103 4.9 ×103 ND Fried egg 2.1 ×103 3.5 ×103 ND Shakshuka 4.8 ×103 6.7 ×103 ND Sheep liver slices 5.6 ×103 6.8 ×103 2.3 ×103 Cafeteria 5 Foul 5.2 ×103 5.2 ×103 ND Falafel 2.8 ×103 5.5 ×103 ND Boiled egg 2.1 ×103 4.3 ×103 0.3 ×103 Fried egg 1.1 ×103 4.2 ×103 ND Shakshuka 4.7 ×103 6.4 ×103 4.2 ×103 Sheep liver slices 8.4 ×103 7.9 ×103 2.3 ×103 Cafeteria 6 Foul 2.8 ×103 4.2 ×103 ND Falafel 4.4 ×103 9.1 ×103 ND Boiled egg 1.4 ×103 4.2 ×103 0.2 ×103 Fried egg 0.9 ×103 2.2 ×103 ND Shakshuka 5.9 ×103 9.8 ×103 1.7 ×103 Sheep liver slices 4.8 ×103 7.5 ×103 0.7 ×103 % of contaminated samples 100% 42% Note. ND - Not detected, APC - Aerobic plate count. The consumption of cooked RTE foods analyzed herein might increase the risk of food-borne illness caused by various microorganisms, especially S. aureus and E. coli. The highest aerobic plate counts recorded in this study might be caused by different environmental factors, such as contaminated air, water, and utensils used in the meal Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 15 preparation. Poor personal hygiene practices in the cafeterias could have also led to the contamination of these pathogens. Bezirtzoglou et al. (2000) reported that RTE food exposure to air or dust at the vending point is likely to increase loads of the bacteria as it appears that most bacteria are carried in aerosols by dust and wind. Contamination by the food producer or handlers is also the most common means of transmitting this germ. S. aureus could be transmitted through the dirty hands and mouths of the producers and customers. Similarly, Burt et al. (2003) stated that food contamination by S. aureus originates from man’s respiratory passages, skin, and uncovered wounds. Thus, its persistence in cooked RTE foods might cause many health risks to consumers. Several reports indicate that most strains of S. aureus are known to be pathogenic due to their excreted heat-stable enterotoxins in direct relationship to their inoculum level (Adebayo-Tayo et al., 2012). S. aureus produces enzymes incorporated with staphylococcal invasiveness and many extracellular substances, which are enterotoxins that are stable at high temperatures and turn the food riskier even though it appears normal (Prescott et al., 2019). The appearance of the symptoms may differ with the quantity of the contaminated food consumed and the susceptibility of the people to the toxin. Some symptoms of staphylococcal food poisoning include vomiting, nausea, diarrhea, and abdominal pain (Amusan et al., 2010). E. coli was not detected in most tested food samples, but it appeared in shakshuka and sheep’s liver slices from most cafeterias. The highest count was 4.2 × 103 recorded in shakshuka samples vended in cafeteria No. 5—a report by Idowu and Rowland (2006) showed that the highest aerobic plate numbers were found in a fang soup sold by street Vendors with a count of 2.80 × 106 CFU/mL while the lowest count was observed in stew sold by stationary food vendors with shade (SVWS) with several 1.20 × 106 CFU/mL. Moreover, the highest value of S. aureus was obtained in moimoi sold by a street vendor with the count of 4.30 × 106 CFU/mL, and the lowest count was observed in stew sold by SVWS with the count of 1.20 × 103 CFU/mL. E. coli counts were detected most in moimoi sold by MV with the value of 2.20 × 106 CFU/mL. The presence of E. coli in cooked RTE foods indicates secondary contamination, as E. coli is known to be correlated with the gastrointestinal tract of warm-blooded animals and not found in the environment as a natural flora (Amusan et al., 2010). However, contamination can take place by the use of contaminated water. E. coli has been detected in foods sold at fast foods in a report by Fowoyo and Baba-Ali (2015). In this study, direct or indirect fecal contamination may be the leading cause of E. coli., and E. coli belong to the Enterobacteriaceae genus, the leading causal agent for diarrhea, gastroenteritis, urinary tract infections, meningitis, nosocomial pneumonia, and dysentery. The strain of E. coli named Enterohaemorrhagic E. coli can cause food-borne diseases similar to the E. coli O157H7 strain, which causes a severe and potentially fatal illness called Hemorrhagic colitis which is characterized by bloody diarrhea and severe abdominal pain (Evans & Evans, 1996). Following the Public Health Laboratory Service (UK) criteria, the count of E. coli in RTE food was defined as <20 CFU/mL (satisfactory), 20– <100 CFU/ML (acceptable), ≥100 CFU/mL (Health Protection Agency, 2009). In our findings, the counts of E. coli in the samples of shakshuka and sheep’s liver slices can be considered unacceptable. Fungal species isolated from ready-to-eat foods samples Data shown in Table 2 indicated that 21 fungal species belonging to 7 genera were identified. The number of isolated fungi varied according to different meals. The least fungal number (9 species) appeared in fried egg sandwiches followed by 12, 14, 15, 18, and 20 species in shakshuka, boiled egg, falafel, sheep's liver slices, and foul samples, respectively. Aspergillus appeared in most samples collected from cafeterias, represented by six species. Among Aspergillus, A. flavus was the highest, and its occurrence ranged between 50-83% of samples. Also, A. niger and A. parasiticus were among the common Aspergillus species found in the samples. Among Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 16 samples analyzed herein, shakshuka samples were highly contaminated by Aspergillus species (50% by A. flavus, 83% by A. niger, 100% by A. ochraceus, and 50% by A. parasiticus). Mucor racemosus emerged in remarkable count in falafel samples (50%) and did not emerge in Shakshuka. Four species of Penicillium were isolated, and among them, P. aurantiogresum was the most commonly isolated. It encountered 72%, 50%, 67%, and 83% in foul, falafel, boiled egg, and sheep’s liver slices, respectively. P. cyclopium appeared in 5 types of samples with remarkable accounts. Rhizopus nigricans were found in high occurrence in foul (72%) and falafel (52%). About 100% of foul and 89% of falafel samples were contaminated by Stachybotrys chartarum. Trichoderma sp. was found in five samples, mostly foul (83%) and fried egg (50%). Uzeh et al. (2009) revealed that microorganisms found in salad constitute raw vegetables include Mucor sp., Aspergillus fumigatus, Trichoderma, Neurospora crassa, and Aspergillus niger. Barnett et al. (2000) reported several mycotoxins isolated from various foods. For instance, Aspergillus and Penicillium produced aflatoxins. The aflatoxins have been found in legumes, grains, fruits, meats, spices, cheeses, milk, rice, corn, cotton seeds. Other toxins with carcinogenic, hemorrhagic, hepatotoxic, neurotic uterotrophic effects have been found in foodstuff and recorded as metabolites of fungi (Jeswal & Kumar, 2015). Ochratoxins are toxins excreted by Aspergillus ochraceus, A. sulphureus, A. malleus, and A. ochraceus can be found in soils and decaying vegetation, grains, wheat, corn, cotton seeds, legumes, peppers, onions, and pears (Adams & Moss, 2002). Table 2. Mean total count and occurrence remarks (O.R.) of each fungal species (CFU/mL) isolated from ready-to-eat food samples sold in Makkah city. Fungal genera & species CFU/mL O.R. out of 6 sites Foul Falafel Boiled egg Fried egg Shakshuka Sheep liver slices (% count of each isolate out of 18 samples) Alternaria alternata 11 H 00 00 3(17%) 3(17%) 3(17%) 2(11%) Aspergillus A. flavus 56 VH 9(50%) 4(22%) 7(39%) 15(83%) 9(50%) 12(67%) A. niger 42 VH 11(61%) 00 6 (33%) 9(50%) 15(83%) 1(5.6%) A. ochraceus 32 H 3(17%) 00 3(17%) 00 18(100%) 8 (44%) A. parasitus 27 VH 6 (33%) 3(17%) 14(78%) 00 9(50%) 4(22%) A. sydowi 26 H 10(56%) 00 7(39%) 00 4(22%) 5(28%) A. ustus 14 L 7(39%) 3(17%) 00 00 00 4(22%) Cladosporium sp. 12 L 6(33%) 00 00 00 10(56%) 6(33%) Mucor racemosus 36 VH 4(22%) 9(50%) 5(28%) 4(22%) 00 4(22%) Fusarium F. culmorum 16 M 2(11%) 5(28%) 6(33%) 00 00 3(17%) F. solani 3 R 3(17%) 00 00 00 7(39%) 00 Penicillium Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 17 P. aurantiogriseum 62 VH 13(72%) 9(50%) 12(67%) 6(33%) 00 15(83%) P. digitatum 29 H 5(28%) 8(44%) 7(39%) 00 5(28%) 9(50%) P. citrinum 21 H 8(44%) 4(22%) 4(22%) 00 00 00 P. cyclopium 33 VH 10(56%) 4 (22%) 7(39%) 7(39%) 00 9(50%) Rhizopus nigricans 38 VH 13(72%) 5(52%) 6(33%) 4(22%) 4(22%) 6(33%) Stachybotys chartarum 40 VH 18(100%) 16(89%) 7(39%) 6(33%) 00 5(28%) Trichothicium roseum 17 M 8(45%) 4(22%) 00 00 00 00 Phoma sp. 8 R 4(22%) 4(22%) 00 00 00 00 Trichoderma sp. 44 VH 15(83%) 6(33%) 00 9(50%) 5(28%) 2(11%) Verticillium sp. 7 L 2(11%) 4(22%) 00 00 00 1(0.06%) No. of isolated fungi 20 15 14 9 12 18 Note. Rare (R) = Appeared in 1 site, Low (L) = Appeared in 2 sites, Medium (M) = Appeared in 3 sites, High (H) = Appeared in 4 sites, and Very High (VH) = Appeared in 5 -6 sites. Patulin is the primary toxic metabolite produced by Penicillium (Bennett & Klich, 2003). Fusarium culmorum and Trichothecium roseum appeared moderately, and the least encountered fungal species were A. ustus, Cladosporium sp., and Verticillium sp. (Table 2). The isolation of S. aureus, Aspergillus niger, Aspergillus fumigatus, Mucor sp, and Penicillium sp, are consistent with the findings of Attiya et al. (2015), Taulo et al. (2008) and Oranusi, et al. (2013), in which these microorganisms were found in RTE foods. Molds like Mucor sp and Aspergillus sp. Contaminated food samples through dust and soil as they disperse in the form of spores abundant in the environment (Apinis, 2003). Molds in food samples are a severe health threat due to mycotoxin production (Makun et al., 2009). Global Research Journal of Management and Social Sciences (GRJMSS) Vol. 13 (10) pg. 18 Picture 1. Most common isolated fungi and bacteria. A). Aspergillus niger (black), A. fumigatus (olive colony), and A. ustus (brown colony); B). A. flavus (yellow-green) mixed with Stachybotrys chartarum (black); C). Curvularia lanata (black color) and A. ustus (grey colonies); D). Alternaria alternate (black) and Trichoderma SP. (green); E). Mixed cultures of S. aureus (golden) and E. coli (white); F). Pure culture of Stachybotrys chartarum. Conclusion Ready-to-eat foods (RTEs), especially of animal origin, could be considered as potential sources for microbial infections in humans. This study revealed that RTE foods served in cafeterias in Makkah city had unsatisfactory microbiological contamination; thus, it may increase the potential risk of food-borne poisoning and diseases among consumers. 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