Abstract
Purpose
Fresh vegetables contain advantageous phytochemical components, making them one of the most significant sources of nutrition. The threat of harmful bacteria still exists because these vegetables are not heated in restaurants before being consumed. Therefore, this study aimed to evaluate the microbial quality of fresh vegetables in restaurants of different levels.
Design/methodology/approach
A total of 499 fresh vegetable samples (from sandwiches and fresh-cut vegetable salads) were collected from 3 different types of food service establishment: 201 from international restaurants (IRs), 210 from national restaurants (NRs), and 88 from cafeterias (CAs). The samples were prepared and inoculated on specific growth media. The aerobic mesophilic bacteria (AMB) Campylobacter spp., Staphylococcus aureus (S. aureus), Enterobacteriaceae, Escherichia coli (E. coli) and yeast and molds were counted, and Listeria monocytogenes, Salmonella spp. and Escherichia coli O157 were detected using specialized medium.
Findings
High counts of S. aureus, above 3 log cfu/g, suggested that 71.5% of samples collected from NRs and 77.3% from CA were not accepted, whereas 81.6% of samples collected from IRs were accepted. The low population of E. coli, less than 2 log cfu/g, suggested that 99.0, 97 and 92.0 % of samples collected from IRs, NRs and CA, respectively, were accepted. Listeria monocytogenes and Escherichia coli O157 were absent from every sample. One sample was positive for Salmonella spp. in each of the NR and CA sample groups.
Originality/value
RIs adhere to health and hygiene standards better than NRs and CAs, according to the findings of vegetable contamination tests.
Keywords
Citation
Saleh, F.A. and Al-Otaibi, M.M. (2024), "Evaluation of fresh vegetable microbiological contamination in fast-food restaurants", Arab Gulf Journal of Scientific Research, Vol. 42 No. 3, pp. 1209-1220. https://doi.org/10.1108/AGJSR-02-2023-0066
Publisher
:Emerald Publishing Limited
Copyright © 2023, Farag Ali Saleh and Mutlag Mohammad Al-Otaibi
License
Published in Arab Gulf Journal of Scientific Research. Published by Emerald Publishing Limited. This article is published under the Creative Commons Attribution (CC BY 4.0) licence. Anyone may reproduce, distribute, translate and create derivative works of this article (for both commercial and non-commercial purposes), subject to full attribution to the original publication and authors. The full terms of this licence may be seen at http://creativecommons.org/licences/by/4.0/legalcode
1. Introduction
The spread and growth of fast-food restaurants are steadily increasing in all parts of the world. According to public sector figures for 2020, Saudi Arabia now has 34,357 catering outlets, or a 70.8% rate, the majority of which are service-oriented restaurants. The market for restaurants was worth 22.4bnUS$ in 2020, and it is anticipated that it will expand at a 12.2% annual pace from 2020 to 2025 (Anonymous, 2020). A crucial subset of ingredients for fast-food restaurants includes fresh vegetables like tomatoes, cucumbers, lettuce, watercress, parsley, carrots, rocca, broccoli and green peppers. Because they include vital substances including vitamins, minerals, plant sterols, natural antioxidants and dietary fibers, these fresh vegetables are regarded as one of the most significant food groups for human health.
As knowledge of obesity and cardiovascular disease patterns in the Gulf Cooperation Council (GCC) region grows, people are being encouraged to adopt healthy eating practices. The demand for high-quality fruits and vegetables is rising as a result of this healthy eating pattern (Mordor Intelligence, 2023).
Given the importance of eating vegetables, the World Health Organization (WHO) has recommended that a person eat 400 grams per day of fresh vegetables or fruits (WHO and FAO, 2003). Although vegetables are a source of important nutrient compounds, they can also be a source of microbial contamination and pathogens. It has been proven in a lot of research that fast-food restaurants are frequently linked to foodborne diseases that affect human health (Hazra, Collison, & Davis, 2022; U.S. Food & Drug Administration, 2023). In recent times, complaints about increases in foodborne diseases, especially those that are carried through vegetables and fruits, have increased in different regions of the world (Esmael et al., 2023). Oliveira et al. (2010) and (Zhang et al., 2018) reported an increase in the number of foodborne illnesses linked to vegetables and fruits in the United States of America (USA) and European Union (EU) countries. Leafy vegetables are the second-largest vector of foodborne bacteria in the USA (Kyle, Parker, Goudeau, & Brandl, 2010). A multi-state Listeria monocytogenes outbreak in the USA in 2022 was linked to bagged leafy greens from Dole. There have been reports of an epidemic of Listeria monocytogenes in 18 individuals from 13 different states (U.S. Food & Drug Administration, 2023). Despite the fact that everyone can contract a foodborne illness, sometimes known as food poisoning, some populations are more susceptible to it and to a serious sickness. These groups comprise people over the age of 65, children under the age of 5, individuals with compromised immune systems and pregnant individuals (Hazra et al., 2022). Vegetables are a common way for many infections to spread (Rahman et al., 2022), causing 2,191 disease cases and 11 deaths as a result of eating food loaded with foodborne bacteria in 2018 in Saudi Arabia (Ministry of Health, 2019). There is a close correlation between the type of foodborne bacteria and the type of food; fresh lettuce leaves and also a green salad containing lettuce carry many pathogenic bacteria, such as Listeria monocytogenes, Escherichia coli O157:H7, Salmonella typhimurium, Shigella sonnei, Campylobacter jejuni and Salmonella newport. Fresh green parsley may be a carrier of bacteria such as Shigella sonnei, while green basil leaves may be carriers of microbes such as Salmonella senftenberg and Cyclospora cayetanensis (Mercanoglu Taban & Halkman, 2011).
The sources of contamination of fresh vegetables in fast-food restaurants have been studied by previous researchers (Soriano et al., 2001a, b; Sospedra, Rubert, Soriano, & Mañes, 2013; Darwish, 2018), who have found that many different sources can cause contamination of vegetables in restaurants, including a lack of hygienic practices. A study by Sospedra et al. (2013) analyzed 555 samples of vegetables taken from restaurants and found that 13% of them were unsatisfactory and contained high levels of mesophilic aerobic bacteria. The samples most contaminated with Enterobacteriaceae were tomatoes and lettuce. Pathogenic bacteria have also been evaluated in fast-food establishments, which were found to have Staphylococcus aureus in 97.3% of cases, followed by Salmonella spp. in 86.7% of cases (Usman, Oladimeji, & Oluwasogbo, 2018). Soriano et al., (2001a) also studied the microbial contamination of fresh green salad and fresh lettuce, finding contamination with Staphylococcus aureus. Shahbaz (2022) found that out of 82 samples of fresh vegetables, 7% were found to be unsatisfactory or exceeded acceptable limits. The researchers attributed this contamination to unclean practices for dealing with fresh vegetables or to insufficient health standards in restaurants. Soriano et al., (2001b) also isolated different genera of Listeria from ready-to-eat salad. Moreover, cutting boards and knives may be considered important sources of vegetable contamination. Bukhari et al. (2021) found food contact surface materials contaminated with nine food-borne bacteria in some restaurants in Makkah city. Even the water used for irrigation can be a source of contamination for fresh vegetables before they reach restaurants (Weldezgina & Muleta, 2016; Saab et al., 2022).
In the Al-Ahsa region of Saudi Arabia, all sorts of fast-food restaurants use fresh vegetables; however, no research on the detection of microbial contamination of these vegetables has been found after analyzing the documentation of previous studies. The present work was a survey study to determine the extent of contamination of fresh vegetables in fast-food restaurants in the Al-Ahsa region of Saudi Arabia. We identified the types of microbes transported through the fresh vegetables, documented useful information for consumers to maintain their health and take care of necessary meals and informed the regulatory authorities and bodies concerned with food safety and human health about the actual reality of the extent of contamination of those meals. This information is for those restaurants to encourage them to follow health conditions to provide a clean and healthy product.
2. Materials and methods
2.1 Samples collection
Three different types of fast-food restaurants (food service establishments) provided a total of 499 samples (sandwiches and fresh-cut vegetable salads): 201 from international restaurants (IRs), 210 from national restaurants (NRs) and 88 from cafeterias (CAs) in the Al-Ahsa area of Saudi Arabia. The samples were taken at random from several locations in Saudi Arabia's Al-Ahsa Governorate, including Hofuf, Al-Mubarraz, Al-Uyoun, Al-Tarf, Al-Omran and Al-Jafr. The number of samples, the kind of samples and the vegetable ingredients are illustrated in Table 1. IRs: It is a regular entity that prepares and provides meals for its customers to be eaten inside the dining hall attached and prepared for this purpose or outside (it has multiple branches in different parts of the world). NRs: It is like IRs, but there are no other branches outside the country, and it also serves traditional meals. CA: It is a regular entity whose customers serve themselves from a counter, in which they prepare sandwiches and light meals and serve hot and cold drinks, and payment is made before eating. The samples were collected in May and June 2018, June 2019 and August 2020. The samples were kept in an icebox until they reached the lab. Three to five restaurant samples were collected daily, and samples were analyzed on the same day.
2.2 Microbiological analyses
For all samples, 25 g of the vegetable part of a sandwich or fresh-cut vegetable salad was mixed with 225 mL of 0.1% buffered peptone water (BPW) into a sterile stomacher bag (Difco, Becton Dickinson). The samples were blended in a stomacher blender (Lab Blender 400\UK) for 5 minutes. The serial dilution was made up to 10−5 in 0.1% BPW. Samples of 1.0-0.1 mL of each dilution were plated in duplicate on the appropriate media. Plate count agar medium (CM0107, Oxoid) was used to determine the aerobic mesophilic bacteria (AMB) according to Atlas (2004). The plates were incubated at 30 °C for 72 h. For the enumeration of Campylobacter species, a blood-free selective agar base plate medium (CM0739, Oxoid) was used. The plates were incubated under microaerophilic conditions at 37 °C for 48 h using a gas generating kit (Oxoid, BR0060) in conjunction with an anaerobic jar. Staphylococcus medium no. 110 (CM0145, Oxoid) was used for the enumeration of Staphylococcus aureus. The plates were incubated at 37 °C for 24-48 h (producing yellow-orange pigment colonies and clearing zones around them) and identified using the staphylase test (DR0595, Oxoid). The Enterobacteriaceae were counted using a violet-red bile glucose agar (VRBGA) medium (CM1082, Oxoid). The plates were incubated at 37 °C for 24 h (Atlas, 2004). The Escherichia coli were enumerated in RAPID E. coli 2 agar medium (3564024, BIO-RAD). The plates were incubated for 24 h at 44 °C, and colonies colored violet to pink were considered to be E. coli. Among the E. coli detected on RAPID E. coli 2 agar medium, the presence of E. coli O157 was tested using the Escherichia coli O157 Latex Test (DR0620, Oxoid) (Goncuoglu, Erol, Ayaz, Ormanci, & Kaspar, 2010). For enumeration of yeasts and molds, potato dextrose agar medium (CM0139, Oxoid) was used and the plates were incubated at 30 °C for 72 h. The counts of tested microorganisms were expressed as logarithm colony-forming units (log CFU) per gram (Atlas, 2004). The method of Rhodes and Quesnel (1986) was used for isolation and identification of Salmonella spp., 0.1 and 1 mL measures of BPW were placed into the Rappaport–Vassiliadis broth (RV), (CM0669B, Oxoid) and Muller–Kauffmann tetrathionate broth (MTTn), (CM0343, Oxoid), respectively. The enrichment broths were incubated at 37°C (for MTTn broth) and 42 °C (for RV broth) for 24 h. Confirmation of the positive cultures was performed using the API (analytical profile index)20E identification system (BioMerex, Marcy I’Etoile, France). After incubation, the streaked xylose–lysine–desoxycholate (XLD) agar plates (CM0469 Oxoid) were incubated at 37 °C for 24 h. For isolation and identification of Listeria monocytogenes, 1 mL quantities of BPW were inoculated into a Fraser broth (CM0895 Oxoid). The enrichment broth was incubated for 48 h at 37 °C. The turbid tubes were streaked onto Palcam agar (CM0877 Oxoid) and incubated at 37 °C for 24 h. The gram-positive, motile, catalase-positive and oxidase-negative colonies were identified by API Listeria (BioMérieux, Mancy l’Etoile, France).
2.3 Statistical analysis
The minimum, maximum, mean and standard deviation values of the microbial counts and simple mathematical operations such as the percentage of samples contaminated with numbers of microorganisms were calculated by one-way analysis of variance (ANOVA) using Minitab 17 software.
3. Results and discussion
3.1 Contaminated microorganisms
3.1.1 Aerobic mesophilic bacteria (AMB)
As shown in Table 2, the AMB count ranged from <102 to 103 cfu/g in IR samples, from <102 to >105 cfu/g in NR samples and from <102 to 105 cfu/g in CA samples. The highest sample percentages (91%, 92.9% and 77.3% from IRs, NRs and CA, respectively) were found in 2, between 3 and >5 and in 5 log cfu/g for IR, NRs and CA, respectively. In IRs, 91% of the samples had an AMB count >2 log cfu/g, while only 4.7% and 9.12% of NRs and CA had the same count, respectively. According to the technical guidelines of hazard analysis critical control point and total quality management (HACCP-TQM) (Anonymous, 1998), if the count of AMB (at 21.1°C) in raw foods ˂ 4 log cfu/g considered “good”, 4-6.7 log cfu/g “average”, 6.7-7.7 log cfu/g “poor” and ˃7.7 log cfu/g “spoiled”. In our results, no samples from either IRs or CA contained AMB above 3 and 5 log cfu/g. However, 21.4% of NR samples had a population above 5 log cfu/g. The mean counts of AMB were 0.25, 4.16 and 3.82 log cfu/g for IR, NR and CA samples, respectively, with the lowest count in IR samples (Figure 1).
Many results from the literature confirmed that fresh vegetables are the samples most contaminated with AMB (Oliveira et al., 2010; Sospedra et al., 2013; Shahbaz, 2022). Sospedra et al. (2013) and Shahbaz (2022) found that aerobic bacteria counts in 13% and 22% of samples were not satisfactory, respectively. Moreover, Oliveira et al. (2010) reported that the AMB count in conventional and organic lettuce ranged from 2.85 to 7.04 and 5.19 to 7.81 log cfu/g, respectively. Additionally, in ready-to-eat salad samples, Ssemanda et al. (2017) found that the mean count of aerobic plate count bacteria was 4.9 log cfu/g. Faour-Klingbeil, Todd and Kuri (2016) explained that the mean AMB count in 17% of ready-to-eat fresh vegetable samples provided in restaurants was above 107 cfu/g. The population of AMB was considered evidence for microbial quality of food and the shelf-life duration but was not related to food safety hazards (Pianetti et al., 2008).
3.1.2 Campylobacter spp
Campylobacter spp. was not detected in any sample from IRs, NRs or CAs (Table 2). These results are in agreement with the results obtained by Santarelli et al. (2018) and Zhang, Yamamoto, Murphy, and Locas (2020), who confirmed that the Campylobacter spp. was not detected in ready-to-eat fresh and raw vegetables. Campylobacter spp. is commonly found in many types of food animals other than chicken (Humphrey, O’Brien, & Madsen, 2007). Some fresh vegetable samples were adjacent to animal source foods, such as beef and chicken (Table 1); nevertheless, the samples were free from Campylobacter spp. Campylobacter spp. is known to be the leading cause of bacterial foodborne diarrhea worldwide (Silva et al., 2011).
3.1.3 Staphylococcus aureus (S. aureus)
S. aureus is widespread and is one of the main pathogens that cause infection in humans and animals (Sergelidis & Angelidis, 2017). The counts of S. aureus ranged from <102 to 104, from <102 to 105 and from <102 to 105 cfu/g in IRs, NRs and CA, respectively (Table 2). The highest sample percentages (72.6%, 57.1% and 77.3% from IRs, NRs and CA, respectively) were found in 3, 4 and between 3 and 5 log cfu/g for IRs, NRs and CA, respectively. The IR and CA samples (14.3 and 44.3%) had S. aureus counts above 4 log cfu/g. No IR samples contained S. aureus above 4 log cfu/g. The average counts of S. aureus in IR, NR and CA, samples were 2.43, 2.81 and 3.03 log cfu/g, respectively, with the lowest count in IR samples (Figure 1). According to GCC standardization organization GSO (2015), the count of S. aureus should not be more than 103 cfu/g. As a result, our findings show that the IRs, NRs and CA samples, respectively, 81.6, 28.5 and 22.7%, are regarded as acceptable because they were below the maximum allowed (Table 2). S. aureus is a common commensal of the skin and mucosal membranes of humans (Kluytmans & Wertheim, 2005). Thus, food handlers carrying S. aureus in their noses or on their hands are regarded as the main source of food contamination, via manual contact or through respiratory secretions. Santarelli et al. (2018) found that 0.33% of tested precut or uncut vegetable samples contained S. aureus. Ssemanda et al. (2017) found that the mean coagulase-positive S. aureus count was 3 log cfu/g in ready-to-eat salad samples. Faour-Klingbeil et al. (2016) and Shahbaz (2022) stated that more than 41.5% and 48% of the ready-to-eat fresh vegetable and salad samples provided in restaurants were found to contain S. aureus, respectively.
3.1.4 Enterobacteriaceae
Enterobacteriaceae microorganism counts were similar to those of S. aureus, with ranges between <102 to 104 cfu/g in both IR and CA samples and from <102 to >105 cfu/g in NR samples (Table 2). The highest sample percentages (81.6, 70.9 and 100% from IRs, NRs and CA, respectively) were found between 2 and 4, 3 and 5 and <2 and 4 log cfu/g for IRs, NRs and CA, respectively. The NR samples (35.7%) had Enterobacteriaceae counts above 5 log cfu/g. There were no samples that contained more than 4 log cfu/g in IR or CA samples. The average counts of Enterobacteriaceae in IR, NR and CA, samples were 2.01, 3.48 and 2.55 log cfu/g, respectively, with the lowest count in IR samples (Figure 1). Oliveira et al. (2010) found that the average count of Enterobacteriaceae in conventional lettuce and organic lettuce was 5.61 and 3.80 log cfu/g, respectively. Sospedra et al. (2013) found that 23% of samples collected from restaurants had unsatisfactory levels of Enterobacteriaceae. They pointed out that lettuce and tomato are the most contaminated vegetables. Enterobacteriaceae are generally intestinal bacteria that live in animal guts and do not cause disease. However, there are genera/species of Enterobacteriaceae that cause a range of diseases in humans and animals (Octavia & Lan, 2014). The presence of Enterobacteriaceae in fresh vegetables is considered normal, but these numbers must be reduced or absent after washing and before serving vegetables for consumption.
3.1.5 Escherichia coli (E. coli)
E. coli is a member of the fecal coliform group and is a more specific indicator of fecal contamination than other fecal coliforms (Odonkor & Ampofo, 2013). Therefore, its presence is considered evidence of inadequate hygiene conditions in food service establishments. E. coli was present in low numbers compared to other bacteria, with averages between <102 to 103 cfu/g in IR samples and from <102 to >104 cfu/g in the samples of NRs and CA (Table 2). The highest sample percentages (99.0, 97.1 and 92% from IR, NR and CA samples, respectively) were found in 2 log cfu/g for all food service establishments. There were no samples that contained >3 log cfu/g (only 1% of samples had 2 log cfu/g) in IRs. Some NR and CA samples (only 1% and 2.3%) had counts of E. coli above 3 log cfu/g. The E. coli average counts in IR, NR and CA samples were 0.03, 0.11, and 0.31 log cfu/g, respectively, with the lowest counts in IR samples (Figure 1). This means that food service establishments follow hygiene requirements, especially IRs. GSO (2015) reported that the number of E. coli should be not more than 102 cfu/g. Accordingly, 99.0, 97 and 92.0 % from samples collected from IRs, NRs and CA, were accepted, respectively, (Table 2). Some previous microbiological studies that were conducted on fresh vegetables served in restaurants found that 6.6% of lettuce samples and 27% of salad samples were contaminated with E. coli (Sospedra et al., 2013; Shahbaz, 2022;respectively). E. coli was isolated from 31.3% ready-to-eat salad samples in a previous study, with bacterial counts between 1.00 and 7.15 log cfu/g (Sospedra et al., 2013).
3.1.6 Yeast and molds
The presence of molds in vegetables can cause potential health problems, as some of them may produce dangerous mycotoxins, and it is known that some types produce large numbers of conidia, causing an allergic reaction (Tournas, 2005; Tournas & Katsoudas, 2005). Food spoilage from mold can also be a food safety issue due to the production of mycotoxins by these molds (Marchetti, Casadei, & Guerzoni, 1992). Yeasts and molds were present in small numbers compared to bacteria, except for E. coli, with ranges between <102 and 104 cfu/g in all of the samples of studied food service establishments (Table 2). The highest sample percentage (81.6, 85.7 and 77.3% from IRs, NRs and CA, respectively) was found between <2 and 3 in all food service establishments. The largest percentage of samples that contained 104 cfu/g was found in the CA samples (22.7%). The average count of yeast and molds in IR, NR and CA samples were 1.48, 2.06 and 1.56 log cfu/g, respectively (Figure 1). Tournas (2005) reported that the count of fungi in ready-to-eat salads ranged between 3.8 × 104 and 1.1 × 105 cfu/g. Oliveira et al. (2010) found the count of yeast and molds was 4.21 log cfu/g in conventional lettuce and 4.74 log cfu/g in organic lettuce. Marchetti et al. (1992) and Liao and Fett (2001) also found a high concentration of yeast counts in salads, peeled carrots and Romaine lettuce.
3.1.7 Positive samples for detection of pathogenic bacteria
The detection of pathogenic bacteria in food service establishment samples is tabulated in Table 3. L. monocytogenes and E. coli O157 were not identified in any tested food service establishment samples. The GSO (2015) requires that vegetables and fruits must be free of L. monocytogenes, E. coli O157 and Salmonella spp. Salmonella spp. was detected in only one sample collected from each of NRs and CA (sample percentage of 0.5 and 1.1%, respectively). Therefore, all the samples collected from IRs were accepted, whereas 99.5 and 98.9% samples from NRs and CA were accepted, respectively (Table 3).
The spread of pathogenic bacteria, inclusive of Salmonella spp., L. monocytogenes and Escherichia coli O157, was limited or absent in fresh vegetables related to the results of previous research. Zhang et al. (2020) reported that E. coli O157:H7 and Salmonella spp. were unidentified in 5,379 fresh-cut vegetable samples, while 13 samples were contaminated by Listeria monocytogenes. Moreover, Santarelli et al. (2018) noted that 0.33% of precut and uncut vegetables were contaminated by Salmonella spp., while L. monocytogenes was unidentified in the same samples. In a study of vegetable dishes from food service establishments, Sospedra et al. (2013) found that only 0.7% of samples were contaminated by Salmonella spp. and E coli, while L. monocytogenes was not detected. It is easy for L. monocytogenes to spread in vegetables because environmental microorganisms normally live in soil and water. The presence of Salmonella spp. in some samples may be due to the transition from the surfaces of knives and cutting boards to fresh vegetables. Faour-Klingbeil et al. (2016) isolated groups of bacteria from the surfaces of knives and cutting boards used to chop fresh vegetables. In general, contamination of vegetables with microbes can be caused by many reasons, such as irrigation with untreated water, organic fertilization or during harvesting, transportation, handling and other practices (Liao & Fett, 2001; Mercanoglu Taban & Halkman, 2011; Oliveira et al., 2010).
4. Conclusions
Our results showed that the IR samples showed the smallest counts of tested microorganisms (AMB, S. aureus, Enterobacteriaceae, E. coli, yeasts and molds). The samples most contaminated by AMB, yeasts and molds were obtained from NRs, while the samples obtained from the CA retained the highest counts of S. aureus and E. coli. All vegetable samples collected from all food service establishments were free of L. monocytogenes and E. coli O157, while 0.5 and 1.1% from the samples collected from NRs and CA were contaminated with Salmonella spp., respectively. In general, especially samples taken from IRs, the majority of vegetable samples taken from three food service outlets were below the upper limit for contamination. According to the guidelines of GSO (2015), the accepted samples collected from IRs, NRs and CA were 81.6, 28.5 and 22.7% from the total for S. aurous, 99.0, 97 and 92.0 % for E. coli and 100, 99.5 and 98.9% for Salmonella spp., respectively. These results reflect the fact that IRs are more compliant with health and hygiene requirements compared to NRs and CAs.
Figures
Descriptions of fresh vegetable samples collected from IRs, NRs and CAs
Food service establishments | Number of samples | Kind of samples | Fresh vegetable ingredients |
---|---|---|---|
IRs | 31 | Beef burger | Tomato, cucumber and lettuce |
43 | Chicken sandwich | Lettuce | |
32 | Chicken burger | Tomato and lettuce | |
95 | Beef burger | Tomato and lettuce | |
NRs | 15 | Chicken sandwich | Lettuce |
19 | Chicken sandwich | Tomato and lettuce | |
91 | Fresh-cut vegetable salad | Tomato, cucumber, lettuce and carrot | |
29 | Fresh-cut vegetable salad | Tomato, cucumber and lettuce | |
13 | Fresh-cut vegetable salad | Cucumber, cabbage and carrot | |
17 | Fresh-cut vegetable salad | Tomato, cucumber, lettuce, cabbage and carrot | |
11 | Fresh-cut vegetable salad | Tomato, cucumber and lemon slices | |
15 | Fresh-cut vegetable salad | Tomato, cucumber, lettuce and lemon slices | |
CA | 13 | Sandwich of falafel* and French-fried potato | Tomato and cucumber |
18 | Falafel sandwich | Tomato, lettuce, onion and rocca | |
11 | Sandwich of falafel and French-fried potato | Tomato and lettuce | |
27 | Beef burger | Lettuce | |
19 | Sandwich of falafel, French-fried potato and eggplant | Tomato and cabbage | |
18 | Falafel sandwich | Tomato, cucumber and lettuce | |
17 | Sandwich of falafel and French-fried potato | Tomato, cucumber and lettuce | |
12 | Sandwich of falafel, French-fried potato and eggplant | Tomato, cucumber and cabbage |
Note(s): 1. *Falafel is a deep-fried patty or ball prepared from ground chickpeas or fava beans with garlic, leek and coriander
Source(s): Table by authors
Contaminated microorganism counts in fresh vegetable samples collected from IRs, NRs and CA in each interval
Microorganisms | Food service establishments | Percentage of samples in the indicated interval | ||||
---|---|---|---|---|---|---|
<102a | 102-103 | 103-104 | 104-105 | >105 | ||
Aerobic mesophilic bacteria | IRs | 91.0 | 9.0 | 0 | 0 | 0 |
NRs | 4.7 | 2.4 | 28.6 | 42.9 | 21.4 | |
CA | 9.12 | 2.3 | 11.4 | 77.3 | 0 | |
Campylobacter spp. | IRs | 0 | 0 | 0 | 0 | 0 |
NRs | 0 | 0 | 0 | 0 | 0 | |
CA | 0 | 0 | 0 | 0 | 0 | |
Staphylococcus aureus | IRs | 9.0 | 72.6 | 18.4 | 0 | 0 |
NRs | 21.4 | 7.1 | 57.1 | 14.3 | 0 | |
CA | 17.0 | 5.7 | 33.0 | 44.3 | 0 | |
Enterobacteriaceae | IRs | 27.4 | 54.2 | 18.4 | 0 | 0 |
NRs | 14.3 | 7.1 | 35.2 | 35.7 | 7.6 | |
CA | 22.7 | 21.6 | 55.7 | 0 | 0 | |
Escherichia coli | IRs | 99.0 | 1.0 | 0 | 0 | 0 |
NRs | 97.1 | 1.9 | 1.0 | 0 | 0 | |
CA | 92.0 | 5.7 | 2.3 | 0 | 0 | |
Yeast and molds | IRs | 45.3 | 36.3 | 18.4 | 0 | 0 |
NRs | 43.3 | 42.4 | 14.3 | 0 | 0 | |
CA | 44.3 | 33.0 | 22.7 | 0 | 0 |
Note(s): ain cfu/g
Source(s): Table by authors
Percentages of samples contaminated with pathogenic bacteria of fresh vegetable collected from IRs, NRs and CA
Pathogenic bacteria | IRs (n = 201) | NRs (n = 210) | CA (n = 88) |
---|---|---|---|
Escherichia coli O157 | nd | nd | nd |
Salmonella spp. | nd | 0.5% | 1.1% |
Listeria monocytogenes | nd | nd | nd |
Note(s): nd: not detected
Source(s): Table by authors
References
Anonymous. (1998). HACCP-TQM Technical guidelines. Section IV Contamination levels and microbiological control. Available from: http://www.hi-tm.com/PDG/Tech-Sect-4.html
Anonymous. (2020). Monshaat, small medium enterprises general authority, Accommodation and food sector report. Saudi Arabia. Available from: https://monshaat.gov.sa/
Atlas, R. M. (2004). Handbook of microbiological media (3rd Edition). Boca Raton: CRC Press. 2051. doi: 10.1201/9781420039726.
Bukhari, M. M. Banasser, T., El-Bali, M. A. Bulkhi, R. A. Qamash, R., Trenganno, A., … & Bahewareth, F. (2021). Assessment of microbiological quality of food preparation process in some restaurants of Makkah city. Saudi Journal of Biological Sciences, 28(10), 5993–5997. doi: 10.1016/j.sjbs.2021.06.050.
Darwish, A. M. (2018). Foodborne pathogens of fast food and ready-to-eat Foods in Tabuk city and evaluating hazard for food quality. International Journal of Healthcare and Biomedical Research, 6, 149–158.
Esmael, A., Al-Hindi, R. R., Albiheyri, R. S., Alharbi, M. G., Filimban, A. A. R., Alseghayer, M. S., … Teklemariam, A. D. (2023). Fresh produce as a potential vector and reservoir for human bacterial pathogens: Revealing the ambiguity of interaction and transmission. Microorganisms, 11, 753. doi: 10.3390/microorganisms11030753.
Faour-Klingbeil, D., Todd, E. C. D., & Kuri, V. (2016). Microbiological quality of ready-to-eat fresh vegetables and their link to food safety environment and handling practices in restaurants. LWT - Food Science and Technology, 74, 224–233. doi: 10.1016/j.lwt.2016.07.051.
Goncuoglu, M., Erol, I., Ayaz, N. D., Ormanci, F. S. B., & Kaspar, C. W. (2010). Isolation and genomic characterization of Escherichia coli O157:H7 in bile of cattle. Annals of Microbiology, 60(2), 293–297. doi: 10.1007/s13213-010-0040-5.
GSO (2015). GCC standardization organization 1016/2015, Microbiological criteria for foodstuffs. Available from: https://www.gso.org.sa/store/standards/GSO:693280/GSO%201016:2015?lang=en
Hazra, A., Collison, M. W., & Davis, A. M. (2022). CDC sexually transmitted infections treatment guidelines, 2021. JAMA, 327(9), 870–871. doi: 10.1001/jama.2022.1246.
Humphrey, T., O’Brien, S., & Madsen, M. (2007). Campylobacters as zoonotic pathogens: A food production perspective. International Journal of Food Microbiology, 117, 237–257. doi: 10.1016/j.ijfoodmicro.2007.01.006.
Kluytmans, J. A. J. W., & Wertheim, H. F. L. (2005). Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections. Infection, 33(1), 3–8. doi: 10.1007/s15010-005-4012-9.
Kyle, J. L., Parker, C. T., Goudeau, D., & Brandl, M. T. (2010). Transcriptome analysis of escherichia coli O157:H7 exposed to lysates of lettuce leaves. Applied and Environmental Microbiology, 76, 1375–1387. doi: 10.1128/AEM.02461-09.
Liao, C. H., & Fett, W. F. (2001). Analysis of native microflora and selection of strains antagonistic to human pathogens on fresh produce. Journal of Food Protection, 64, 1110–1115. doi: 10.4315/0362-028X-64.8.1110.
Marchetti, R., Casadei, M. A., & Guerzoni, M. E. (1992). Microbial population dynamics in ready-to-use vegetable salads. Italian Journal of Food Science, 4, 97–108.
Mercanoglu Taban, B., & Halkman, A. K. (2011). Do leafy green vegetables and their ready-to-eat [RTE] salads carry a risk of foodborne pathogens?. Anaerobe, 17, 286–287. doi: 10.1016/j.anaerobe.2011.04.004.
Ministry of Health, S. A. (2019). Foodborn diseases statistics (2018). Ministry of Health. Available from: https://www.moh.gov.sa/en/Ministry/MediaCenter/Publications/Pages/Publications-2019-11-12-001.aspx
Mordor Intelligence (2023). Fruits and vegetables market in Saudi Arabia size & share analysis- growth Trends & Forecasts (2023 – 2028). Available from: https://www.mordorintelligence.com/industry-reports/fruits-and-vegetables-in-the-kingdom-of-saudi-arabia-industry
Octavia, S., & Lan, R. (2014). The family enterobacteriaceae. In The Prokaryotes: Gammaproteobacteria. doi: 10.1007/978-3-642-38922-1_167.
Odonkor, S. T., & Ampofo, J. K. (2013). Escherichia coli as an indicator of bacteriological quality of water: An overview. Microbiological Research (Pavia), 4, 2. doi: 10.4081/mr.2013.e2.
Oliveira, M., Usall, J., Viñas, I., Anguera, M., Gatius, F., & Abadias, M. (2010). Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiology, 27(5), 679–684. doi: 10.1016/j.fm.2010.03.008. 20510788.
Pianetti, A., Sabatini, L., Citterio, B., Pierfelici, L., Ninfali, P., & Bruscolini, F. (2008). Changes in microbial populations in ready-to-eat vegetable salads during shelf-life. Italian Journal of Food Science, 20, 245–254.
Rahman, M., Alam, M. U., Luies, S. K., Kamal, A., Ferdous, S., Lin, A., … Ercumen, A. (2022). Contamination of fresh produce with antibiotic-resistant bacteria and associated risks to human health: A scoping review. International Journal of Environmental Research and Public Health, 19, 1–15. doi: 10.3390/ijerph19010360.
Rhodes, P., & Quesnel, L. B. (1986). Comparison of Muller-Kauffmann tetrathionate broth with Rappaport-Vassiliadis (RV) medium for the isolation of salmonellas from sewage sludge. Journal of Applied Bacteriology, 60(2), 161–167. doi: 10.1111/j.1365-2672.1986.tb03374.x.
Saab, M. T. A., Jomaa, I., El Hage, R., Skaf, S., Fahed, S., Rizk, Z., … Mateo-Sagasta, J. (2022). Are fresh water and reclaimed water safe for vegetable irrigation? Empirical evidence from Lebanon (Vol. 14). Switzerland: Water. doi: 10.3390/w14091437.
Santarelli, G. A., Migliorati, G., Pomilio, F., Marfoglia, C., Centorame, P., D’Agostino, A., and … Iannetti, L. (2018). Assessment of pesticide residues and microbial contamination in raw leafy green vegetables marketed in Italy. Food Control, 85, 350–358. doi: 10.1016/j.foodcont.2017.09.035.
Sergelidis, D., & Angelidis, A. S. (2017). Methicillin-resistant Staphylococcus aureus: A controversial food-borne pathogen. Letters in Applied Microbiology, 64, 409–418. doi: 10.1111/lam.12735.
Shahbaz, M. (2022). Microbiological safety of fresh-cut produce and salads served at quick service restaurants. Biomedical Journal of Scientific and Technical Research, 47(4). doi: 10.26717/bjstr.2022.47.007536.
Silva, J., Leite, D., Fernandes, M., Mena, C., Gibbs, P. A., & Teixeira, P. (2011). Campylobacter spp. as a foodborne pathogen: A review. Frontiers in Microbiology, 2, 1–12. doi: 10.3389/fmicb.2011.00200.
Soriano, J. M., Rico, H., Moltó, J. C., & Mañes, J. (2001a). Incidence of microbial flora in lettuce, meat and Spanish potato omelette from restaurants. Food Microbiology, 18, 159–163. doi: 10.1006/fmic.2000.0386.
Soriano, J. M., Rico, H., Moltó, J. C., & Mañes, J. (2001b). Listeria species in raw and ready-to-eat foods from restaurants. Journal of Food Protection, 64(4), 551–553. doi: 10.4315/0362-028X-64.4.551.
Sospedra, I., Rubert, J., Soriano, J. M., & Mañes, J. (2013). Survey of microbial quality of plant-based foods served in restaurants. Food Control, 30, 418–422. doi: 10.1016/j.foodcont.2012.08.004.
Ssemanda, J. N., Reij, M., Bagabe, M. C., Muvunyi, C. M., Joosten, H., & Zwietering, M. H. (2017). Indicator microorganisms in fresh vegetables from “farm to fork” in Rwanda. Food Control, 75, 126–133. doi: 10.1016/j.foodcont.2016.12.031.
Tournas, V. H. (2005). Moulds and yeasts in fresh and minimally processed vegetables, and sprouts. International Journal of Food Microbiology, 99, 71–77. doi: 10.1016/j.ijfoodmicro.2004.08.009.
Tournas, V. H., & Katsoudas, E. (2005). Mould and yeast flora in fresh berries, grapes and citrus fruits. International Journal of Food Microbiology, 105, 11–17. doi: 10.1016/j.ijfoodmicro.2005.05.002.
U.S. Food & Drug Administration. (2023). Investigations of foodborne Illness Outbreaks, 1–14.
Usman, S., Oladimeji, A. A., & Oluwasogbo, O. A. (2018). Evaluation of hazard analysis and critical control point methods in fast food establishments in Kaduna metropolis, Kaduna state, Nigeria. Available at: https://www.proquest.com/openview/224ba317aa78bf1d8656a3eb35d8877a/1?pq-origsite=gscholar&cbl=2026366&diss=y
Weldezgina, D., & Muleta, D. (2016). Bacteriological contaminants of some fresh vegetables irrigated with awetu river in jimma town, southwestern Ethiopia. Advanced Biology 2016, (1), 1–11. doi: 10.1155/2016/1526764.
WHO and FAO (2003). Diet, Nutrition, and the Prevention of Chronic Diseases (Report of a joint WHO and FAO Expert Consulation). WHO Technical Report Series. 916, doi: 10.1093/ajcn/60.4.644a.
Zhang, G., Chen, Y., Hu, L., Melka, D., Wang, H., Laasri, A., … Hammack, T. S. (2018). Survey of foodborne pathogens, aerobic plate counts, total coliform counts, and Escherichia coli counts in leafy greens, sprouts, and melons marketed in the United States. Journal of Food Protection, 81, 400–411. doi: 10.4315/0362-028X.JFP-17-253.
Zhang, H., Yamamoto, E., Murphy, J., & Locas, A. (2020). Microbiological safety of ready-to-eat fresh-cut fruits and vegetables sold on the Canadian retail market. International Journal of Food Microbiology, 335, 108855. doi: 10.1016/j.ijfoodmicro.2020.108855.
Further reading
Annual Report on Foodborne Disease Outbreaks-2018 (2019).
Acknowledgements
The authors acknowledge the Deanship of Scientific Research at King Faisal University for funding this research (No: 160083).
Conflicts of interest: The authors declare that there is no conflict of interest related to this study.
Corrigendum: It has come to the attention of the publisher that the article: Saleh, F.A. and Al-Otaibi, M.M. (2023), “Evaluation of fresh vegetable microbiological contamination in fast-food restaurants”, Arab Gulf Journal of Scientific Research, Vol. ahead-of-print No. ahead-of-print. https://doi.org/10.1108/AGJSR-02-2023-0066 incorrectly listed the funding details in the acknowledgments as No: 22774.
Our guidelines make it clear that funding information is to be checked at proof stage.
The error has been corrected in the online version of the article to include the correct funding information.