Determinants of Food Safety Knowledge among University Students in Pakistan: A Cross-Sectional Study

Background Foodborne diseases are among the most serious public health problems and young adults are an important target group as they often engage in risky food handling practices. The purpose of this study was to assess the level of food safety knowledge and its determinants among Pakistani university students. Method A cross-sectional study was conducted among university students during the academic year 2018-2019. A convenient sample of 1417 students completed a structured questionnaire containing forty-four questions on food safety and hygiene. Results Overall, participants showed a moderate level of food safety knowledge with a mean percentage score of 62.5±8.4. Students had a good level of knowledge about causes of foodborne diseases (66.3±16.9). However, the lowest level of knowledge was identied in foodborne diseases' symptoms (55.2±14.3). In general, females and participants from health-related degree program scored signicantly higher (p<0.01) in all knowledge sections than their counterparts. A signicant association was found between the causes of foodborne diseases and postgraduate students being more knowledgeable (p<0.001). Multivariate logistic regression analysis showed that age, gender, academic degree program, level of education, and father's education were signicant predictors of overall food safety knowledge. Conclusion The results of this study showed that university students have a moderate knowledge in food safety. Educational interventions and awareness programs are needed to strengthen the existing knowledge.


Background
Food safety is one of the leading concerns being challenged not only in developed countries but is equally a threat to developing countries (1). Besides, food safety holds to be an important aspect in public health and epidemiology as it is directly related to worldwide foodborne illness and diseases (2).
Additionally, as per Global Burden of Disease, it is envisaged that millions of humans are subject to foodborne illness largely governed by poor hygiene and food handling practices (3).
It has been learned that foodborne diseases from contaminated food is responsible for millions of deaths globally with billions of dollars being spent on health care costs and hospitalization annually (4).
Nevertheless, the World Health Organization [WHO] routinely identi es upsurges foodborne disease outbreaks and epidemics that are point of interest for public health specialists, epidemiologists and health professionals. Even in the most developed food supply chain regions as European Union and United States, still there are reports of product recall, associated disease and illness issues (5). According to United States FDA statistics 2017, nearly 23% of the processed foods in United States had been recalled due to potential risk linked to public health epidemic and food safety concerns. However, for developing countries there is no such reliable data exists even that can portray a glooming snapshot of food safety (6).
Ingested food can become a source of disease if ingredients storage, handling, preparation, processing and product storage are not followed properly. In this context, consumer knowledge, awareness and attitude are perhaps the pillars predicting the overall food safety stratum as consumer behavior is largely governed by the existing food handling procedures, food safety knowledge and general hygiene following the postulates of Theory of Planned Behaviour (7).
According to World Health Organization, "food safety is a scienti c discipline describing handling, preparation and storage of food in order to avoid foodborne illness. That food safety procedure includes variety of practices needed to be followed to prevent the entry of potential health hazard responsible for the diseases". Furthermore, microorganisms are reported as major food safety hazard as they compete for nutrients with humans for their growth and survival (8). Hence, the signi cance of food safety and hygiene is of paramount importance as being a vital component of food supply chain, thereby assuring consumer con dence and safety (8). In this milieu, contaminated raw food, inadequate cooking, and consumption of food from an unsafe source are principal factors often associated with foodborne diseases in homes, restaurants and vendor foods (9). Accordingly, public health and its signi cance cannot be ignored and is totally concerned with food safety attitudes, knowledge and handling practices of food processors. As far as the global statistics are concerned, knowledge and awareness rankings for both the developed and developing countries are not so encouraging. Furthermore, developing countries are much behind others when it comes to food safety knowledge and awareness (10).
Lahore, the capital of the Punjab province, is the second largest metropolitan city of Pakistan with a population above 15 million individuals. In such a populated city, the signi cance of food safety becomes manifold when survival, well-being and health of individuals cannot be held at stake. Besides, health of school/college and university going students is at risk due to the consumption of unsafe/unhygienic food being supplied, processed and sold in school or university canteens and eateries.
Furthermore, general food safety is quite blissful reasoned to lack of awareness, education and rather weak legislation. More recently, dedicated efforts have been made on strengthening existing food safety legislation that includes revision of pure food rules and extending additional powers to o cials related to food inspection and regulation. Nevertheless, still a lot more work needs to be done.
Keeping the severity of existing food safety issue, the present research was conducted to relate the level of knowledge, attitude as well as practices regarding food safety among university students/youth in Lahore. Purposely, 1500 students from various universities of Lahore were asked to respond to a purposely designed questionnaire to evaluate their food safety knowledge, attitude and practice.

Study design and population
A cross-sectional study was conducted from September 2019 to December 2019 to assess food safety knowledge and its determinants among students enrolled in different universities of Lahore. The purpose and details of the study were explained in detail to participants in simple and clear language and voluntary written consent obtained. A total of 1500 students were randomly approached in four different universities and invited to participate in the study. Of those approached, 1417 (94.5%) consented and completed the survey. Participant were strati ed into two elds of studies; health-related disciplines and non-health related disciplines. Where possible we followed the STROBE (Strengthening the Reporting of Observational studies in Epidemiology) guidelines (11).

Instrumentation
In order to assess the food safety knowledge of students, a 44-item structured questionnaire was designed by reviewing relevant literature and previously used standardized, validated questionnaires (12)(13)(14)(15)(16). Where necessary, modi cations were made in the questionnaire to meet the local needs. Before data collection, the questionnaire was pilot tested with 50 students for clarity and acceptability. These respondents were not included in the study. This pilot study resulted in minor modi cations in the questionnaire, including rephrasing of a few questions and terminology. The nal questionnaire was divided into ve sections; demographic pro le (5 questions), personal hygiene practices (9 questions), symptoms of foodborne diseases (12 items), and food handling practices (12 items). The questions regarding food safety knowledge were graded as true and false. For each question, "1" was given to the correct answer and "0" was given to the incorrect answer. After taking the ethical approval initially from the Ethical Review Board of the University of Veterinary and Animal Sciences, a questionnaire was approved by respective institutional review boards of participant universities.

Statistical Analysis
The data collected were analyzed using Statistical Package for the Social Sciences (SPSS version 20.0).
The response was entered as a categorical variable, right answer was assigned the score of 1 point whereas, 0 point was assigned to all wrong answers. Higher knowledge scores indicate greater knowledge. For each knowledge section, the mean score was calculated and converted into percentage. Descriptive statistics were carried out to summarize demographic characteristics and data regarding food safety knowledge. Comparison of food safety knowledge between different demographic variables was performed using t-test and analysis of variance (ANOVA). For logistic regression model, food safety knowledge score was dichotomized into high and low scoring groups according to the median of each subsection. For all statistical comparisons, a p-value of ≤ 0.05 was considered signi cant.

Backgrounds data
A total of 1417 questionnaire forms were lled by university students. Distribution of demographic characteristics of the study population is presented in Table 1. Of the participants, 68% were female participants and 32% male with a mean age of 22 years (± standard deviation (SD) ± 2.9). The data shows that the majority of the participants (62.8%) were in the age group of 20-24 years and 79.8% of them were undergraduate students. The students comprised of two educational groups; 41.8% from health-related and 58.2% from non-health related majors. Majority of the respondents' fathers had university education and mothers had college education.
Overall food safety knowledge score Table 2 presents the mean scores of knowledge sections and overall food safety knowledge. Results showed that the respondents had a moderate knowledge about overall food safety with a mean score of 62.48%. Participants achieved the highest score for the knowledge on causes of foodborne diseases (66.25%) and the lowest score for the knowledge on food handling practices (63.77%). Table 3 showed the percentages of correct responses for the questions about personal hygiene practices.
Majority of the respondents answered correctly for all questions except the question 6, 9 and 10 for which students had poor knowledge. Only 35.3% gave the correct answer for question "It is not safe to store chicken, sh and raw meat together in a fridge or freezer", 88% wrongly believed that "To avoid food poisoning, you should clean the kitchen sink drain every week" and 16.2% did know the correct answer for the question "The best way to avoid food poisoning from fruits and vegetables is to wash them under a running tap".
Descriptive results of knowledge questionnaire in the area of foodborne diseases are presented in Table  4. Respondents had poor knowledge (28.8%) about the consumption of canned vegetable and they believe that its consummation without prior heating will increase one's risk of suffering food poisoning. About 30.8% of the students gave wrong answer to the question about the "Leftover chicken eaten cold can cause foodborne diseases".
This study found that students have a very poor knowledge about the symptoms of foodborne diseases. Majority of the respondents didn't know that body temperature rises quickly (79%), low blood pressure (64.7%), sweats (66.8%), pain in the bone (52.7%), coughing or sneezing (64%) are not the symptoms of foodborne diseases. Only 45.9% students correctly know that stiff neck is also a symptom of the foodborne diseases (Table 5) Improper food handling practices are thought to contribute to a high number of foodborne illness outbreaks. Data presented in table 6 show the respondents knowledge on food handling practices. Most of the participants (86%) failed to select the correct answer for the question about "Thorough washing of vegetables and fruits in tap water is necessary to prevent food poisoning". Likewise, only 17.1% and 38.4% of the correspondents knew that the food handler should be medically examined every six months and they cannot clean their hands by wiping them on a piece of cloth, respectively. Over half of the respondents (53.7%) believed that it is unnecessary to reheat the previously cooked food.
Impact of socio-demographic characteristics on students' food safety knowledge Students aged above 30-year had signi cantly lower knowledge on all the types of knowledge scores except "symptoms of foodborne diseases" where the score was lower, but the result was non-signi cant.
There was a statistically signi cant difference between the gender and the knowledge on personal hygiene practices, causes of foodborne diseases, symptoms of foodborne diseases, food handling practice and overall knowledge. Female students showed signi cantly higher score on all the types of knowledge (Table 7).
Current levels of education of students had no effect on all the types of knowledge scores except the causes of foodborne diseases. Postgraduate students had signi cantly higher scores for causes of foodborne diseases than undergraduate students. The mean score of all knowledge types of health science students was higher than non-health related students and the difference between means was statistically signi cant (Table 7).
According to this study, students whose fathers were educated had signi cantly higher mean knowledge of all groups except personal hygienic practices. Participants whose mother was educated had signi cantly higher mean score on overall knowledge and knowledge on symptoms of foodborne diseases.

Predictors of food safety knowledge
Multivariate logistic regression analysis was used to explore the signi cant predictors among the sociodemographic variables for food safety knowledge. As shown in Table 8, regression analysis showed that age, gender, education level, academic discipline and father's education are signi cantly (P < 0.05) associated with overall food safety knowledge. In the full model, being female (OR = 1.88, P = 0.001), postgraduate students (OR = 1.28, P = 0.001), students from health-related majors (OR = 3.84, P = 0.001) and students who had educated father (OR = 3.87, P = 0.001) were positively associated with adequate food safety knowledge. A negative association was also found between age groups higher than 30 years and overall food safety knowledge (OR = 0.09, P = 0.001). For personal hygiene practices knowledge, age group 20-24 (OR = 1.82, P = 0.001), 25-29 years (OR = 2.05, P = 0.017), health-related majors (OR = 3.16, P = 0.001) and father's education (OR = 2.21, P = 0.029) were positively associated with adequate knowledge. In addition, female gender (OR = 0.67, P = 0.004), being in age group of >30 years (OR = 0.34, P = 0.040) and having higher education (OR = 0.62, P = 0.004) were negatively associated to the personal hygiene practices knowledge. As for the knowledge on causes of foodborne diseases, being in age group 20-24 (OR = 1.31, P = 0.037) and 25-29 years (OR = 2.07, P = 0.021), female gender (OR = 10.268, P = 0.064), having higher education (OR = 1.421, P = 0.035), health-related majors (OR = 2.057, P = 0.001) and father's education (OR = 3.340, P = 0.001) were positively associated with adequate knowledge. In addition, being in age 25-29 years (OR = 2.07, P = 0.021), female gender (OR = 10.268, P = 0.064), healthrelated majors (OR = 2.057, P = 0.001) and educated father (OR = 3.340, P = 0.001) were positively associated with adequate knowledge on symptoms of foodborne diseases. The subjects in age groups above 30 years with a high education level were more likely to have inadequate knowledge on symptoms of foodborne diseases. Age group 20-24 (OR = 0.72, P = 0.010) and mother's education (OR = 039, P = 0.001) revealed a negative relationship with knowledge on of foodborne diseases.

Discussion
It has been previously reported that poor hygiene knowledge and practices of consumers are associated with 87% of reported foodborne outbreaks linked to food prepared or consumed in private homes in the United Kingdom, Europe, Australia, New Zealand, the United States, and Canada (17). Therefore, it is important to educate the consumers about safe food handling and preparation (Gurudasani & Sheth, 2009). To date, there is no study documenting food safety knowledge status among the Pakistani consumers. This investigation provides valuable information about the self-reported food safety knowledge of young adults enrolled in different universities of Lahore city. In general, overall participants' responses revealed optimal levels of food safety knowledge with a mean score of 62.48%. The moderate level of food safety knowledge among the students was also a common nding in a previous similar study aimed at evaluating determinants of food hygiene knowledge among University students of Malaysia and Saudi Arabia, respectively. (18, 19). On the other hand, several studies identi ed a better food safety knowledge among participants as compared to our ndings, reasoned to better exposure, prior food safety knowledge and geographical location [as mostly such results have been attained in developed countries] (12,(19)(20)(21).
Four different sets of questions were designed to access food safety knowledge, the participants exhibited slightly low knowledge on symptoms of foodborne diseases (mean score of 55.18%) and high knowledge about the causes of foodborne diseases (66.25%), followed by personal hygiene practices (64.75%) and food handling practices (63.77%). Similarly, a previous study in Kuala Lumpur city observed that participants had the lowest knowledge score on symptoms of foodborne diseases (18).
Although some studies reported that food safety knowledge score signi cantly increases with age (12,18,19,22,23), might be due to extended exposure and education. Nevertheless, in our ndings, this pattern was not observed as some younger students depicted a rather higher level of food safety knowledge that may be linked to improved food safety knowledge. This nding is consistent with the results of (22), who suggested that the young population have more access to TV and social media and, therefore, higher opportunities of knowledge sharing. In all four types of food safety knowledge sections, female students obtained signi cantly higher scores than males. Female students signi cantly outperformed males on all four types of food safety knowledge. These ndings are comparable with the previous researches conducted in USA, Greece and Turkey, where females have higher food safety knowledge scores than males (12,20,22,24). In Pakistani culture, in any household, females are responsible for the food preparation and cooking; that could be the reason of their high food safety knowledge score.
Students in health-related disciplines reported signi cantly higher food safety knowledge scores than non-health related students since they are expected to learn basic food safety elements in the syllabi at the elementary and intermediate levels. The present nding is consistent with previous investigations conducted in Jordan, Saudi Arabia and USA (12,19,22,23,25) where the students from an academic discipline related to health sciences had more knowledge on food safety. According to this study, the father's education rather than the mother's education is positively associated with the level of healthrelated knowledge of college students. Fathers may play an important role in delivering food safety knowledge to their children. Our ndings agree with (18), who found that father's education in uenced the food safety score of their children. Furthermore, multivariate logistic regression models revealed signi cant relationships between all four types of food safety knowledge groups and all independent variables (age, educational level, academic discipline, father's education) except mother's education.

Conclusion
This study showed that the university students in Pakistan have a moderate knowledge of food safety (Mean score 62.5 ± 8.4). Results identi ed that students' reported food safety knowledge varies by sex, academic discipline and father education. These results suggest the need for educational strategies at various levels to improve the current food safety awareness, especially for the sake of their future roles as caregivers for their families. Educating people about the basic principles of food safety hygiene could signi cantly affect the number of foodborne illnesses and leads towards better public health protection. There is a strong consensus among international experts that food safety programs should be integrated into usual school curriculum to increase awareness. Furthermore, a university setting would also be a promising place to reach and educate the young adults with key food safety concepts as they are the future cooks, chefs, food handlers and home makers. The university curriculum could also emerge as an ideal setting to provide food safety knowledge across all the disciplines regardless of food, nutrition and health background.

Limitation Of The Study
The current study has also some limitations. This study focused on the university students Lahore city, Pakistan therefore it is unlikely to be generalizable. The study measured self-reported knowledge, which may risk recall bias and cultural factors. Health related disciplines include those students who had sufficient prior knowledge about basic food safety and factors affecting consumer health. Whereas, non-health related disciplines mainly include students from fine arts and management sciences who have comparatively lesser knowledge about food safety and hygiene as compared to their counter parts.