Awareness of Foodborne Pathogens among Students: A Cross-Sectional Study in the Kingdom of Saudi Arabia

Food poisoning associated with microbial pathogens causes millions of foodborne disease cases in the Kingdom of Saudi Arabia. Awareness about foodborne pathogens may play a positive role in the reduction of foodborne illnesses. The present cross-sectional study investigates awareness about five major microbial pathogens (Salmonella, Campylobacter, Staphylococcus, Listeria, and Escherichia coli) among university students (n = 399) from four major cities in the Kingdom of Saudi Arabia. Multiple logistic regression models were used to predict the determinants of inadequate knowledge. Of the 399 study participants, only 34.5% of students knew the above-mentioned foodborne pathogens. Awareness varied by pathogen, and the variations appeared to be related to age, sex, education, and field of study. In comparison to students in health sciences, students in computer sciences were found to be less knowledgeable about foodborne pathogens (OR: 2.85; 95% CI: 1.36-5.99). Our findings suggest that awareness about microbial pathogens is low among students and is associated with their field of study. Effective education programs about foodborne hazards could help improve students' awareness of microbial pathogens.


Introduction
Microbial contamination of food is a major public health concern due to the emergence of foodborne pathogens [1,2]. More than 250 sources of foodborne diseases have been identified globally [3]. Numerous studies indicate that foodborne outbreaks are becoming more frequent globally and have urged public health interventions [4][5][6][7]. Each year, microbial pathogens cause millions of foodborne disease cases, resulting in many hospitalizations and deaths in Saudi Arabia [8]. The highest proportion of outbreaks was in adults (68.1%), and Salmonella species (81%) was the most common causative agent, followed by Staphylococcus aureus (19%) [9]. In the United States, 31 major pathogens caused 9.4 million foodborne illnesses [10]. Most (58%) illnesses were caused by norovirus, followed by nontyphoidal Salmonella spp. (11%), Clostridium perfringens (10%), and Campylobacter spp. (9%). Between 1964 and 2010, listeriosis cases occurred in 28 (90%) provinces in China, and the overall case-fatality rate was 26% [11]. Due to the increase in foodborne infectious diseases, several food quality regula-tions have been implemented in various countries [11][12][13][14][15][16]. Foodborne pathogens reduce human health productivity and pose a substantial economic cost to the health system [17,18]. However, there is a knowledge gap on awareness of microbial pathogens in food, as reported by a recent systematic review and meta-analysis [19]. Food safety efforts generally focus on laboratory examination and physical investigation of the end product, while interventions to improve knowledge on the causes of foodborne illness have received limited attention.
A study in the United States reported low awareness of four major microbial pathogens (Salmonella, Campylobacter, Listeria, and E. coli) among consumers and reported associations with demographics and food safety behaviors [20]. In Jordan, only 65.1% of the study participants knew about foodborne disease. Only 23.1% knew that the presence of Shigella in food can cause illness, and 50.1% have heard of salmonellosis [21]. In the Kingdom of Saudi Arabia, only 49% of consumers have information about Salmonella as a foodborne pathogen. In comparison, only 16% mentioned Campylobacter as a foodborne pathogen [22]. Foodborne illnesses are prevalent in Saudi Arabia, but the number of infection and associated deaths has not been accurately reported. Previous studies have suggested that awareness of foodborne pathogens is related to a better knowledge of safe food handling and preparation principles [23]. A recent study highlighted that consumers with more awareness of foodborne pathogens were more likely to adopt food safety practices [24]. Therefore, evaluating foodborne pathogen knowledge among young individuals is important, as interventions can be implemented to help them develop proper attitudes and skills to understand contemporary food issues to improve public health. The study was aimed at assessing students' knowledge about five major foodborne pathogens and to predict their knowledge with their sociodemographic profile in Saudi Arabia.

Study Design and Participants.
A cross-sectional study was designed among registered students at Saudi Electronic University in four significant cities (Abha, Dammam, Jeddah, and Riyadh) in the Kingdom of Saudi Arabia. Five hundred random students were contacted to participate in the study; however, only 399 students participated in the survey (79.8% response rate).

Data Collection.
After obtaining informed consent, students were asked to complete the survey. The questionnaire of each respondent was coded to ensure anonymity. Data were collected through interviews by trained enumerators using a validated questionnaire. The questionnaires were completed directly by the respondents. Each questionnaire took approximately 10 to 20 minutes to complete.

Data
Analysis. Statistical analysis of the data was performed using STATA software (version 13.0). Descriptive statistics were used to generate summary statistics. Pearson's chi-squared test was used to investigate the association between sociodemographic differences in foodborne pathogen knowledge among students. Logistic regression models were constructed to predict the association between students' knowledge and their sociodemographic profile. Statistical significance was identified at the 95% confidence level (p < 0:05).

Ethical Considerations.
The study protocol was reviewed and approved by the Institutional Review Board of Saudi Electronic University. Study participants were asked to participate voluntarily and allowed to withdraw from the study if they so desired. Survey results were anonymized and analyzed for interpretation.

Results
The sociodemographic characteristics of the study participants are presented in Table 1. Of the 399 study participants, approximately 29.5% resided in the city of Abha, followed by Riyadh (29.0%), Dammam (24.3%), and Jeddah (17.0%). More than half (55.14%) of the respondents were female. Approximately 25.0% of the students were younger than 20 years, with the majority falling in the 20-30-year range. A majority of the respondents (78.70%) studied at the bachelor's level of a university program, and more than half (58.7%) of the respondents were enrolled in the health sciences program. Table 2 represents the association between students' knowledge of foodborne pathogens and their sociodemographic characteristics. The overall knowledge of foodborne pathogens among students was found to be poor. Only 34.5% of students recognized all five major foodborne pathogens listed in this study. Of the 399 students, only 88 (22%), 43 (10.7%), and 60 (15%) were aware of E. coli, Campylobacter, Staphylococcus, and Listeria, respectively. Approximately 60% of students were aware of Salmonella as a foodborne pathogen. Knowledge of Salmonella was found to be associated with sex (p = 0:020), education (p ≤ 0:001), field of study (p ≤ 0:001), and place of residency (p = 0:002).
The multiple logistic regression model results suggest that age, sex, and field of study are significant determinants in explaining the pathogen knowledge variables in the study (Table 3). Female students were found to be more knowledgeable (OR: 0.46; 95% CI: 0.21-0.99). In comparison to students in the health sciences, students in the fields of computer sciences (OR: 2.85; 95% CI: 1.36-5.99), administration and business (OR: 1.98; 95% CI: 0.93-4.24), and languages

Discussion
This study revealed that the majority (65%) of student respondents were not aware of foodborne pathogens. Only 34.5% of students recognized all the major foodborne pathogens listed in this study: only 88 (22%), 43 (10.7%), 60 (15%), and 39 (9.8%) were aware of E. coli, Campylobacter, Staphylococcus, and Listeria, respectively. Salmonella was a wellknown pathogen among our study participants, and similar findings were reported in other studies [25]. Our study shows that there is a need for health education programs for students, especially those emphasizing foodborne pathogens. A similar study conducted in Taif, Kingdom of Saudi Arabia, revealed the lack of knowledge among people on foodborne pathogens. In that study, only half of the participants knew about salmonellosis, the most commonly known cause of food poisoning, 27% had information about hepatitis, and 22% had knowledge of E. coli [22]. Similarly, a study from Jordan showed that 76.9% (three-fourths) of the respondents had not heard of Shigellosis and did not know that it could be transmitted to humans through food [21]. A review study from Saudi Arabia highlights the magnitude and determinants of food poisoning internationally and in the Kingdom [8]. Another review pointed out that older adults' awareness of Listeria varies between 33 and 58%, with a median understanding of only 40% [19]. Compared to previous studies, our study findings indicate the following important points about pathogen awareness among students in the Kingdom of Saudi Arabia.

International Journal of Food Science
First, more students said they had heard of Salmonella (60.15%) than the other foodborne pathogens. Second, students' with a health science background were significantly more informed about Salmonella (70%) than students with other backgrounds. Third, male students (40.42%) were less informed about foodborne pathogens than female students. Our study findings suggest that awareness of different pathogens (Salmonella, Campylobacter, Staphylococcus, Listeria, and Escherichia coli) among students is related to their field of study. As reported, health science students are more aware than their peers in other programs of study. This may also suggest that health science students have better access to microbial food safety information. Female students are more knowledgeable about pathogens than their male counterparts. This may be because of their food handling behavior and access to food safety information.
Furthermore, students are a known high-risk population for foodborne illness due to their high-risk eating behavior [21,[26][27][28]; imparting to them the knowledge of pathogenspecific unsafe food sources and prevention practices may help in changing their behaviors. As suggested by numerous studies, our findings also highlight that promoting under-standing of microbial pathogens in food to students is necessary. It could be an essential intervention in reducing the burden of foodborne disease in Saudi Arabia.

Limitations
Our study cannot rule out other confounding variables in predicting students' awareness levels. One of the study's limitations is that it measured self-reported knowledge on foodborne pathogens, and respondents could over/underreport their understanding of pathogens. Moreover, the study is focused on students in university settings and cannot be generalized.

Conclusions
Considering the results, it is concluded that the study participants in Saudi Arabia were poorly informed about major foodborne pathogens (Salmonella, Campylobacter, Staphylococcus, Listeria, and Escherichia coli). Among the five pathogens, students were more informed about Salmonella and showed a lower level of awareness of other pathogens in food. Note: Independent variables for the multiple logistic regression model analysis included age, sex, education, field of study, and place of residence. + Students not able to recognize any one of the foodborne pathogens listed in this study. * Statistically significant (p < 0:05).

International Journal of Food Science
There is a need to conduct food safety education programs for university students to improve their level of awareness about foodborne pathogens.

Data Availability
The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Ethical Approval
This study was approved by the Institutional Research Ethics Committee, Saudi Electronic University, Riyadh, Kingdom of Saudi Arabia.

Consent
Written consent was obtained from all the study participants before participation.

Conflicts of Interest
The author declares that there are no competing interests.

Authors' Contributions
MAM made substantial contributions to the conception and design and oversaw data collection and curation and the writing of the manuscript. MAM performed the statistical analysis and approved the submitted version of the manuscript.