literature review on food safety and hygiene

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• Published: 22 December 2022

Food safety practice and its associated factors among food handlers in food establishments of Mettu and Bedelle towns, Southwest Ethiopia, 2022

• Sanbato Tamiru 1 ,
• Kebebe Bidira 1 ,
• Tesema Moges 2 ,
• Milkias Dugasa 1 ,
• Bonsa Amsalu 1 &
• Wubishet Gezimu 1  

BMC Nutrition volume  8 , Article number:  151 ( 2022 ) Cite this article

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Food safety and hygiene are currently a global health concern, especially in unindustrialized countries, as a result of increasing food-borne diseases (FBDs) and accompanying deaths. It has continued to be a critical problem for people, food companies, and food control officials in developed and developing nations.

The objective of the study was to assess food safety practices and associated factors among food handlers in food establishments in Mettu and Bedelle towns, south-west Ethiopia, 2022.

A community-based cross-sectional study was conducted from February to March 2022, among 450 randomly selected food handlers working in food and drink establishments in Mettu and Bedelle towns, Southwest Ethiopia. Data was collected using an interviewer-administered structured questionnaire. The data was coded and entered into Epi Data version 3.1 before being exported to SPSS version 20 for analysis. Both bivariate and multivariable logistic regression models were fitted. An adjusted odds ratio and a 95% confidence level were estimated to assess the significance of associations. A p -value of < 0.05 was considered sufficient to declare the statistical significance of variables in the final model.

A total of 450 food handlers participated in the study, making the response rate 99.3%. About 202 (44.9%) of respondents had poor practices in food safety. Lack of supervision (AOR = 6.2, 95% CI: 3.37, 11.39), absence of regular medical checkups (AOR = 1.98; 95% CI: 1.14, 3.43), lack of knowledge of food safety practices (AOR =2.32; 95% CI: 1.38, 3.89), availability of water storage equipment (AOR =0.37; CI: 0.21, 0.64), and unavailability of a refrigerator (AOR =0.24; 95% CI: 0.12) were factors significantly associated with food safety practices.

The level of poor food safety practices was remarkably high. Knowledge of food safety, medical checkups, service year as food handler, availability of water storage equipment, availability of refrigerator, and sanitary supervision were all significantly associated with food safety practice. Hence, great efforts are needed to improve food safety practices, and awareness should be created for food handlers on food safety.

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Introduction

Food safety is described as the circumstance and control required to ensure the safety, wholesomeness, and suitability of the food during its production and consumption. It is the primary public health concern for many countries, which is essential to prevent foodborne illness and enhance the well-being of humans [ 1 , 2 ]. Food safety and hygiene are currently a global health concern, particularly in developing countries, as a result of increasing food-borne diseases (FBDs) and accompanying deaths, and they also continue to be a critical problem in developed and developing nations for people, food companies, and food control officials [ 2 ].

Food-borne diseases (FBD) are associated with outbreaks, threaten global public health security, and have become an international concern as a growing public health issue [ 3 ]. According to the World Health Organization (WHO), FBDs in developing nations are serious because of bad hygienic food handling methods, poor understanding, and the absence of infrastructure. This is the result of poor use of food handling and sanitation practices, inadequate food safety laws, weak regulatory systems, and a lack of financial resources [ 4 , 5 ].

Findings of different studies showed that there are relatively few food safety problems in some Asian countries like Indonesia, Jordan, and Saudi Arabia, which ranged from 10 to 19.31%, respectively [ 6 , 7 ]. But when we look at the findings of the study conducted in Malaysia, the magnitude of poor food safety practices was about 41.7% [ 1 ]. A study conducted in some parts of the country revealed that there is a high magnitude of food safety problems in food and drink establishment centers, ranging from 46.3 to 72.67% [ 3 , 8 , 9 ].

WHO disclosed that 1 in 10 individuals worldwide is sick from foodborne illnesses secondary to unsafe food practices and the use of contaminated foods [ 10 ]. Food safety practices are worse in developing countries, including Ethiopia; according to previous studies conducted in Addis Ababa and other areas of the country, less than half of food handlers have maintained satisfactory safety practices in handling food in the studied food establishments [ 3 , 8 , 9 ].

Foodborne diseases are prevalent in Ethiopia; the country’s annual incidence of foodborne illnesses ranged from 3.4 to 9.3% [ 3 ]. Food safety practices also have economic implications. The effects of food-related illness expenditures on hospital treatments are about US$ 110 billion annually in developing countries, which results in decreased production [ 11 ]. Several factors, like prevailing poor food handling and sanitation practices, inadequate food safety training, weak regulatory systems, a lack of financial resources, low educational status, and a lack of knowledge, have been identified as affecting food safety [ 12 ].

Efforts have been made globally by preparing a food safety guideline with the help of the World Health Organization. Similarly, in Ethiopia, significant work has been done with regards to food safety by preparing a national food safety policy and guidelines and assigning a regulatory department in the health office at different levels, though people are still suffering from morbidities and mortalities related to food-borne diseases. This is mainly attributed to food safety practices [ 3 , 13 ]. Only a few studies have been conducted in Ethiopia with regard to food safety practices. Hence, the purpose of this study was to assess food safety practices and associated factors among food handlers in the food establishment centers of Mettu and Bedelle towns.

Study design, period, and area

A community-based cross-sectional study was conducted from February 21 to March 21, 2022, in Mettu and Bedelle towns. The two towns are located in the Oromia Regional State of southwest Ethiopia. Mettu is the capital of the Ilubabor Zone, and Bedelle is the capital of the Buno Bedelle Zone. Mettu and Bedelle towns are located about 600 and 480 km southwest of Addis Ababa, respectively. The two towns are home to different institutions and factories like Mettu University, Mettu Karl Comprehensive Specialized Hospital, Bedelle General Hospital, Bedelle Brewery Factory that provide services for a large number people in the southwest region of the country. There were 188 food establishments and 1015 food handlers in the study area, according to data gathered from the trade and industry bureaus of the two towns.

Populations and eligibility criteria

All food handlers who worked in food and drink establishments in Mettu and Bedelle towns were considered the source population, whereas all selected food handlers who worked in selected food and drink establishments in the two towns were study participants in this study.

Food handlers working in preparation, cleaning, and service areas of food establishments at the time of the study were included in the study. However, food handlers who were not available during the data collection period and who could not give a response due to severe illness were excluded from the study.

Sample size determination and sampling procedure

The sample size was determined using a single population proportion formula:

Where Z = 1.96, the confidence limits of the survey result (value of Z at α/2 or critical value for normal distribution at 95% confidence interval).

p  = 0.5 (50%), the population proportion of food safety practices from study conducted in Fiche town [ 5 ].

d = 0.05, the desired precision of the estimate

So the calculated sample size was, \(n={(1.96)}^2\frac{\left(0.5\ast 0.5\right)}{0.05^2}=384\)

Since the total number of food handlers in the study area was less than 10,000, we have utilized correction formula, that gives nf =288. After adding a 5% non-response rate and a design effect of 1.5, the final sample size of 453 was used for this study.

The list of existing food establishments and the number of food handlers currently working in food establishments were obtained from Mettu and Bedelle towns’ Trade and Industry Office. Then, food establishments for this study were randomly selected from a total list of food establishments. Next, study participants were proportionately allocated to each selected food establishment based on the number of food handlers. Then, an updated list of food handlers was taken from the manager or owner of the selected establishment. Finally, study participants were selected using a simple random method from each establishment.

Study variables

The dependent variable of this study was food safety practice, and the independent variable includes socio-demographic factors (educational level, age, gender, marital status, and work experience), institutional factors (training, supervision, and availability of guidelines for food safety), health-related factors (medical check-ups and sick leave during illness), knowledge-related factors (knowledge of methods to prevent contamination and knowledge of food safety practices), and sanitary facility-related factors (three-compartment dishwashing systems, refrigerators in the kitchen, and water supply).

Data collection tools and procedure

Data were collected using an interviewer-administered standardized questionnaire adapted and modified from previously published studies [ 3 , 8 , 9 , 13 ]]. The questionnaire was structured into six parts: socio-demographic parts with six questions, food safety knowledge with nine questions, basic sanitary facilities with seven questions, institutional factors with four questions, health-related with two questions, and food safety practice with twelve questions.

Food safety knowledge was assessed using nine closed-ended questions with two possible answers: “yes” or “no.” The questions mainly focus on the personal hygiene of food handlers, temperature control, cross-contamination, food storage, and equipment hygiene. In assessing knowledge, one score was given for every correct answer and zero score for incorrect answers or unanswered questions. Then, the responses to these questions were added together to generate a knowledge score. Food handlers who obtained a total score greater than the mean value were considered to have good food safety knowledge, and those who had scores less than the mean value were considered to have “poor food safety knowledge.”

Food safety practices were also assessed using 12 closed-ended questions with two possible answers: “yes” or “no.” One score was given for every standard practice and zero for every unsafe practice. Food handlers with a total score greater than the mean were considered to have “good food safety practices,” while those with a score less than the mean were considered to have “poor food safety practices.” The data was collected by three diploma nurses, and the overall data collection processes were supervised by one health officer after two days of training.

Data quality assurance

The quality of the data was ensured through all data collection tools and was translated into the local language and back-translated to English by language experts to ensure its consistency. Training of data collectors and supervisors was conducted to enable them to acquire the basic skills necessary for data collection and supervision, respectively. A pre-test was done on 5% of the sample in Gore town, and based on the results of the pre-test, necessary modifications were made. After data collection, the completeness of the data was checked by the principal investigator ahead of data entry. Incomplete and inconsistent questionnaires were excluded from the analysis.

Data analysis

The collected the data was curated according to the study objectives. The coded responses were entered into EpiData and exported to SPSS for analysis. A descriptive analysis was used to describe the percentages and number of distributions of the respondents by socio-demographic characteristics and other relevant variables in the study. A binary logistic regression analysis was performed on the independent variables and their proportions, and a crude odds ratio was computed against the outcome variable. The independent variables with a p -value less than 0.25 were entered into the multivariable logistic regression analysis to control for potential confounders and identify significant factors associated with outcome variables. Finally, a p -value of less than 0.05 at the 95% CI was used to claim statistical significance.

Ethics and approval processes

The ethical clearance letter was obtained from ethical committee of Mettu University, college of health science before conducting study. After the interviewer read and clearly explained the study’s benefits and risks, a written consent was obtained from the study participants. Then literate participants signed, whereas uneducated participants put their fingerprints on the consent form to shown their willingness to participate. Confidentiality of the data was maintained at all times.

Socio-demographic characteristics of food handlers

In this study, a total of 450 food handlers participated out of a total of 453 with a response rate of 99.3%. The mean age of the participants was 29.3 years (SD = 5.28). The majority (54%) of food handlers were female. One hundred ninety-one (42.4%) of them attended secondary education, while only nine (2%) of them had least a higher education qualification. More than half (62.2%) of food handlers were married. Regarding service year as food handler, about 181 (40.2%) of respondents had worked for 2–4 years [Table  1 ].

Practice of food handlers on food safety

Among the 450 total food handlers, 417 (92.7%) of them were not checking the temperature of food. The majority, 333 (74%) of food handlers, did not wash their hands after sneezing. Two hundred and eleven (46.7%) participants did not wear hair covers. About 10.2% of food handlers did not trim their fingernails. Majority, 387(86%) of the participants, did wash their hands after touching unwrapped food, whereas 366 (81.3) of them wash their hands before touching cooked food. Moreover, 145 (32.2%) of participants did not use separate utensils for raw and cooked foods [Table  2 ].

Level of food safety practice

In general, out of all participants, 202 (44.89%) had poor food safety practices, while 248 (55.1%) had good food safety practices [Fig.  1 ].

Overall food safety practice of food handlers working in food and drink establishment in Mettu & Bedelle towns south west Ethiopia, 2022 ( n  = 450)

Factors associated with food safety practice

In the bivariate analysis, variables like sanitary inspection, medical checkup, food safety knowledge, the presence of a refrigerator, the service year as a food handler, the presence of guidelines or guiding instructions, and the unavailability of water storage equipment were shown to be associated with the outcome variable. In the multivariable logistic analysis, the variables sanitary inspection (AOR = 6.2; 95% CI: 3.37, 11.39), medical checkup (AOR = 1.98; 95% CI: 1.14, 3.43), knowledge of food safety practices (AOR = 2.32; 95% CI: 1.38, 3.89), the presence of a refrigerator (AOR = 0.24; CI: 0.12, 0.45), and availability of water storage equipment (AOR = 0.37; CI: 0.12, 0.45) were found to be significantly associated with food safety practices.

The study revealed that food handlers with a poor level of knowledge were 2.32 times more likely to have poor food safety practices than those with a good level of knowledge (AOR = 2.32; 95% CI: 1.38, 3.89). The likelihood of having poor food safety practices among food handlers who did not have regular medical checkups was nearly two times higher than among food handlers who have regular medical checkups (AOR = 1.98; 95% CI: 1.14, 3.43). Moreover, poor food safety practice was 6.2 times higher among non-supervised food handlers as compared to their counterparts (AOR = 6.2; 95% CI: 3.37, 11.39) [Table  3 ].

Ensuring optimal food safety practices is still a major global challenge, particularly in developing countries like Ethiopia. This has in turn resulted in a high prevalence of FBD [ 3 ]. This study aimed to assess food safety practices and its associated factors among food handlers in food establishments of Mettu and Bedelle towns, Southwest Ethiopia.

The findings of the present study showed that 44.9% (CI: 40.29, 49.49) of participants had poor food safety practices. This finding is higher than studies conducted in Indonesia (10%) [ 2 ], Saudi Arabia (19.3%) [ 6 ], Nigeria (30.5%), [ 14 ], Arba Minch town, Southern Ethiopia (32.6%) [ 15 ], Dessie town, Northern Ethiopia (28%) [ 16 ], and Assosa Western Ethiopia [ 17 ]]. The variation might be due to differences in study settings and food handler’s socio-demographic profile. But it was lower than studies conducted in Fiche (50%) [ 3 ], and Gondar town (53.3%) [ 12 ]. The possible reason for discrepancies might be the difference in the study design, cutoff points, and year of study. However, the present finding was comparable with studies conducted in Debra Markos town (46.3%) [ 9 ], Woldia town, Northeast Ethiopia(46.5) [ 18 ], Dangila town, North West Ethiopia(47.5%) [ 19 ] and Batu town Central Ethiopia [ 20 ].

Regarding factors associated with poor food safety practice, this study revealed that; a lack of regular medical checkup was significantly associated with poor food safety practices. The likelihood of having poor food safety practices among food handlers who did not have regular medical checkups was nearly two times higher than that of those food handlers who have regular medical checkups. This finding was supported by a study conducted in Fiche, Gondar towns, and Dessie town [ 3 , 12 , 17 ]. This might be due to behavioral change following counseling given during a medical checkup.

The study revealed that sanitary inspection is significantly associated with food safety practice. Poor food safety practice was 6.2 times higher among non-supervised food handlers as compared to their counterparts. This finding is supported by a previous study conducted in Arba Minch town of Southern Ethiopia [ 15 ].

In the present study, knowledge of food safety was significantly associated with food safety practices. Food handlers with a poor level of food safety knowledge were 2.33 times more likely to have poor food safety practices than those with a good level of knowledge. This study is supported by cross-sectional studies conducted in Gondar city, Debra Marcos town, Dangila town, Northern Ethiopia, and Batu town, Central Ethiopia [ 9 , 12 , 19 , 20 ].

There was a significant association between food safety practices and sanitary inspection. The probability of having poor food safety practices was higher among food handlers who were not supervised than their counterparts. The present finding was supported by a study conducted in Assosa and Gondar city, Woldia town [ 12 , 17 , 18 ]. This might be due to the effect of advice and feedback given to supervised food handlers, managers, and the owners during an inspection.

The probability of having poor safety practices was 62.7% less likely among food handlers working in establishments having water storage equipment as compared to their counterparts. This might be due to easy access of water to cleansing. This finding was supported by a community based cross sectional study conducted in the Bole sub-city of Addis Ababa[ [ 8 ].

Moreover, the service year as a food handler was also significantly associated with food safety practices. The probability of having poor food safety practices among food handlers with 2–4 and 5–7 years of service was 96.8 and 88.5% less likely, respectively, as compared to those food handlers with a service year of less than 2 years. The finding was supported by a study conducted in Fiche and Debra Marcos town [ 3 , 9 ]. This might be due to the positive effect of adaptation to a specific working environment and sharing experience from coworkers.

Limitations of the study

The study was based on reported rather than observed practices related to food safety. Therefore, there was a risk that respondents may report what was expected of them but practice may be different. In addition, lack of universal consensus on the definition of good or poor practice was a challenge in the study. Furthermore, parasitic and microbiological laboratory investigations were not considered in this study.

The level of poor food safety practices was remarkably high in the study area. Almost all food handlers did not use thermometers to check the temperature of the food. More than one-third of them were not using separate utensils for raw and cooked foods. Nearly half of food handlers did not use hair covers, and three-fourths of them did not practice sanitizing or washing their hands after sneezing prior to touching foods. Generally, there is an increased risk of FBD in association with the identified poor food safety practices. Factors like sanitary inspection, medical checkup, food safety knowledge, availability of refrigerator, service year as food handlers, and availability of water storage were identified as having significant associations with the identified poor level of food safety practice. Therefore, there is need to invest much more in food safety practices, and special emphasis should be given to food safety in order to reduce the risk of FBD and ensure optimal food safety practices.

Recommendation

To improve food safety practices, all concerned bodies should play their roles. Food handlers should have regular medical checkups, maintain good hygiene, try to improve their knowledge and practice of food safety, and play a crucial role in ensuring good food safety practices. Food handlers should also use separate utensils for raw and cooked foods to reduce cross-contamination. Food establishment owners should avail themselves of equipment like refrigerators and water storage that can help ensure food safety by preventing spoilage and contamination.

Healthcare professionals and food professionals in collaboration need to conduct on-site supervision, inspect the hygiene of food handlers, and observe the way they are working towards food safety practices. They should conduct strict sanitary supervision on a regular basis and take timely corrective action (reward compliant food handler or constrain non-compliant handlers). In addition, they need to arrange for regular medical checkup of food handlers in collaboration with nearby medical facilities.

The trade and industry office should work in collaboration with health office and take food safety practices into consideration during the renewal of licenses of establishments, and the government or policy makers should enforce the implementation of HACCP as guiding instructions in all establishments as a mandatory requirement. Based on current findings, future researchers can conduct detailed investigations that are supported by microbial analysis and try to show a new approach to improving food safety practice.

Ethics statements

The study was carried out in accordance with the principles of the Declaration of Helsinki. The study was conducted after getting ethical approval and clearance from the institutional review board (IRB) of Mettu University. A supportive letter was taken from Mettu University and submitted to each hospital, and permission was obtained from each hospital. Participation was completely voluntary, with no economic or other motivation, and informed consent was obtained from the study participants. All participants were informed of the study’s purpose and given the right to respond fully or partially to the questionnaire. They also had the right to withdraw at any time. Furthermore, Participants who agreed to participate in the study were asked to sign informed consent forms. The privacy and identity of participants were protected, and participants’ confidentiality was also assured by omitting their names from the informed consent form.

Conflict of interest

The authors declare that they have no competing interests.

Availability of data and materials

All the data generated or analyzed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank Mettu University for financial support. Again, our sincere appreciation goes to study participants, data collectors, and supervisors. Moreover, we would like to thank the Mettu and Bedelle towns’ trade and industry offices for provision of background information about the study population.

This research was funded by Mettu University with grant number of Meu/2021/210.

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ST, KB, and TM participated in conceptualization of the study, methods, supervision, analysis, investigation, software, and writing of the first and final draft of the manuscript. MD, BA, and WG participated in the study methods, data curation, resource acquisition, and writing the final manuscript. Finally, all authors approved the last version of the manuscript to be published, and agreed to be accountable for all parts of the work.

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This study was approved by the Research Ethics Committee of Mettu University. All methods were conducted in accordance with the code of ethics outlined in the Declaration of Helsinki. After the interviewer read and clearly explained the study’s benefits and risks, a written consent was obtained from the study participants. Then literate participants signed, whereas uneducated participants put their fingerprints on the consent form to shown their willingness to participate. Confidentiality of the data was maintained at all times.

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Tamiru, S., Bidira, K., Moges, T. et al. Food safety practice and its associated factors among food handlers in food establishments of Mettu and Bedelle towns, Southwest Ethiopia, 2022. BMC Nutr 8 , 151 (2022). https://doi.org/10.1186/s40795-022-00651-3

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Introduction

Recently, the entire world has been plagued with the sudden appearance of a new disease commonly known as COVID-19 that was brought about by the severe acute respiratory syndrome corona virus 2 (SARS-CoV-2), ( Olaimat et al., 2020 ). On the 11th of March 2020, the World Health Organization (WHO) has declared the COVID-19 outbreak as a global pandemic as the number of cases worldwide rose to a concerning amount, with an expected increase in the number of cases in the coming months ( Cucinotta and Vanelli, 2020 ). According to World Health Organization (2020) , the new strain of the coronavirus disease was first identified in a cluster of pneumonia patients in Wuhan, China where the Chinese authorities later confirmed to be the cause of the pneumonia. COVID-19 is a respiratory illness characterized by symptoms such as fatigue, dry cough, fever, as well as lymphopenia ( Cucinotta and Vanelli, 2020 ).

This recent pandemic has brought about many changes around the world as numerous countries have implemented various lockdowns and the closure of many economic sectors in order to curb the number of rising COVID-19 cases due to the spread of the infection among the citizens. During these lockdowns, essential services were allowed to operate on strict standard operating procedures (SOPs). As a result, a new norm has been introduced where social and physical distancing must always be adhered to with masks to be worn at all times while being in public areas, as well as the prioritization of hygiene and sanitation. This pandemic has affected many aspects of day-to-day life, including social life, as well as many economic sectors. Rozaki (2020) found that many companies and businesses, including the agricultural practices and food industries have been affected by the economic uncertainty since the start of the pandemic. This study highlights the current issue of the COVID-19 pandemic that has affected the food industry, mainly in the aspect of food safety and the food supply chain in Malaysia. Due to COVID-19, many sectors in the economy were affected as companies have been forced to close down or took strict restrictions on their manufacturing and production as required by the health guidelines set by the government and authorizing bodies such as the WHO ( Rashid et al., 2021 ). Due to these restrictions, most companies had to cut down and minimize on the production and manufacturing of their products, which has caused shortages and delays of a particular product. Therefore, the objectives of this study were to review the impact and threats of the COVID-19 pandemic to food safety as well as to the food supply chain in Malaysia. Additionally, precaution and solution taken by the government were also discussed in order to provide an insight as a form of improvement to the current situation while managing the pandemic.

Literature Review

Overview of the covid-19 situation.

The recent COVID-19 pandemic has affected many countries in the world. As cases continued to rise, more and more countries have implemented lockdowns and restrictions. In China, where the first reported cases of COVID-19 originated, the Chinese government had enacted control measures which was described as “the strictest control measures since the founding of the People's Republic of China” ( Min et al., 2020 ). These measures include suspension of intra-city public transport, banning of public gatherings, and the shutdown of entertainment outlets. Additionally, restrictions had also been enforced in other countries such as the United Kingdom, where a lockdown that has restricted non-essential public gatherings, closure of businesses and educational institutions, and an order to stay at home aside for essential tasks and exercise was imposed ( Choi et al., 2020 ). In South East Asia, countries such as the Philippines have also implemented control measures which had included restrictions such as curfews, travel restrictions and check-points, as well as the indefinite suspension of business and education activities ( Tee et al., 2020 ). Globally, the government agencies have tried imposing restriction and control measures in order to closely monitor and manage the number of COVID-19 cases within each country. Nowadays, these restrictions are analyzed according to the state of each country and re-opening of other sub-economic sector were taken into consideration. However, tight SOPs are still in place as the pandemic is still far from being over globally which has eventually affected the food purchasing and consumption behavior ( Li et al., 2022 ).

In Malaysia, the first positive COVID-19 case was identified on the 25th of January 2020, and within 6 days, a total of eight positive cases were then reported, all of which were imported cases from Wuhan, China ( Shah et al., 2020 ). Furthermore, on 17th of March 2020, Malaysia recorded its first confirmed death ( Koh et al., 2020 ). Subsequently, the number of positive cases recorded skyrocketed following a religious mass gathering which has also included international participants from India, Brunei, Thailand, South Korea, China, and Japan ( Che Mat et al., 2020 ). Minhat and Shahar (2020) have expressed that the rapid transmission in positive cases was predicted to have been caused by exported cases from other countries. Following the continual increase in the number of cases in Malaysia from 99 positive to 200 positive in less than a week ( Shah et al., 2020 ), the government of Malaysia has implemented the Movement Control Order (MCO) on the 18th of March 2020. The MCO implemented has required all businesses to underwent a close down, with the exception of those that provide essential services and items ( Tang, 2020 ). Consequently, most businesses were forced to halt their activities as a form of compliance to the new MCO implemented by the government. Some of the restrictions during MCO include social distancing guidelines implemented in public places, limited operating hours, travel restrictions which have been further enforced by road blocks all over the country, in addition to the limitation of movement of a 10-km travel radius for all citizens ( Tang, 2020 ). However, even with the implementation of the MCO, after 1.5 years, Malaysia is seen still struggling to lower the number of cases among its population due to emerging new variants being transmitted.

These control measures had affected many walks of life, from workers, business owners, students, as well as children. Social life, education system and non-essential businesses have been placed on a halt. These restrictions, although implemented to stop the rising cases of COVID-19, have also impacted many economic sectors. While many companies were able to keep their businesses going by allowing their employees to work from home, the same cannot be applied for most food industries as many food companies require their workers to work hands-on with the product, especially for smaller businesses. Therefore, COVID-19 has caused some effects to the food industry, such as impacting food safety as well as the food supply chain, with similar impact found in over 16 countries. Hence, managing the whole system during a severe pandemic is utterly crucial ( Djekic et al., 2021 ).

Selection of Articles

In this study, the systematic review of articles was searched and selected from three databases (Science Direct, Scopus and Google Scholar). The literature search was conducted from Oct 2020 to September 2021. The search terms used were “food safety” and “food supply chain” under the (Article title, Abstracts, Keywords). In addition, the term “COVID-19” was used under the [Search within results] to be specific. About 1698 articles were identified through the database search and an additional 12 articles were identified (including governmental reports and newspaper articles) as indicated in Supplementary Figure 1 . Thorough screening was conducted to eliminate bias and subsequently, eligible literature were included in this study so that an overview of the food safety and supply chain during and post pandemic situations in Malaysia were able to be reflected in this study.

COVID-19 and Food Safety

What is food safety.

Food safety is a very important aspect in the food industry. According to Uçar et al. (2016 ), food safety is described as the preparation of food that shall not cause any harm to the consumer when it is eaten according to its intended use. Moreover, the Australian Institute of Food Safety (2019) describes food safety as the handling, preparation, and storage of food which can best lower the risk of sickness caused by foodborne illnesses. Food related diseases caused by foodborne pathogens can be very dangerous, and even fatal, therefore, food safety is a crucial aspect during food preparation to avoid any undesirable consequences. According to Uçar et al. (2016 ) there are a few factors which affects food safety: food hygiene, personal hygiene of food handlers, and kitchen sanitation, as shown in Supplementary Figure 2 . Previously, the responses of food safety system and management during pandemic in over 16 countries indicated that staff awareness and hygiene were the most important attributes that needed to be enforced in food industries ( Djekic et al., 2021 ).

Not only is food safety important to protect the consumers directly from foodborne diseases, but it is also significant as the consumption of safe and nutritious food will help maintain good health and well-being. Uddin et al. (2020) stated that the consumption of nutritious and safe foods helps to generate body immunity, thus, it also helps in fighting against diseases such as COVID-19. Additionally, a proper diet can guarantee that the body is strong enough to fight the virus. A healthy body and immunity are especially important during this pandemic where a sick or unhealthy person may be more susceptible to fall victim to COVID-19 as compared to a healthy person. Furthermore, it has been reported that the food consumption pattern during the pandemic has changed along with limited physical activities which could affect health condition in the long term ( Mahar et al., 2021 ). However, alongside the intake of healthy and nutritious foods in the diet, other measures such as food safety management and the good food practices are also necessary in combating the virus ( Aman and Masood, 2020 ). Thus, food safety should not be taken lightly during this pandemic. In fact, a huge shift of consumer perception toward food safety during the pandemic has influenced the purchasing power ( Thomas and Feng, 2021 ).

Impact of COVID-19 to Food Safety

Early on at the start of the pandemic, many food consumers have been concerned with the safety of their food as there was not much well-known information about COVID-19 and its transmission via food products. There were concerns of the virus being transmitted through food products as well as by the packaging of the food itself, which has caused many companies to enforce stricter hygiene rules in the manufacturing and production of their products. In this case, sanitation and sanitization is vital to ensure food safety. Sanitation is the utmost important criteria for hygienic condition so that the whole food preparation, handling area, amongst others, is in a clean environment. Additionally, during this pandemic outbreak, another step such as sanitization is needed to ensure that the surface is free from any kind of microbes and viruses that could potentially pose a threat to human health.

As more research was conducted, it was revealed that up until now, there was no study which had reported on the spread of COVID-19 through food products and the human digestive system ( Duda-Chodak et al., 2020 ; Olaimat et al., 2020 ). Food handlers in US practiced frequent hand-washing to eliminate the possibilities of contracting COVID-19 from food items ( Thomas and Feng, 2021 ). The World Health Organization (WHO), Food and Agriculture Organization (FAO), as well as the United States Food and Drug Administration (US-FDA) has advised that COVID-19 is not transmitted by the consumption of food contaminated by the virus ( Uddin et al., 2020 ). Moreover, Cable et al. (2020) reported that there was no evidence which has suggested that SARS-CoV-2, the virus causing COVID-19, is a foodborne virus, based on the conclusion brought about by the French Agency for Food, Environmental, and Occupational Health and Safety. Cable et al. (2020) has continued to state that, SARS-CoV-2 should be able to be inactivated during cooking as well as under normal pasteurization conditions, based on research conducted on other coronaviruses. This was also in agreement with the study conducted by Jawed et al. (2020) where high temperature heating of over 70°C has been found to inactivate viruses, including the Coronavirus. Thus, it is important for handlers to maintain good food safety etiquette, like cooking foods until the correct temperature was achieved in making sure that the food is safe for consumption. On the other hand, Cook and Richards (2013) has stated that even cooked foods may transmit viral diseases, if they come into contact with other contaminated foods or surfaces such as food that has been handled by a person with contaminated hands or coming into contact with food items that have previously been contaminated during processing or preparation. In the study, it has been further illustrated that viral droplets are typically considered heavy when they are more than 5 μm in size, resulting in a need for a space to land which could be any object, packaging or surfaces that in turn, could be the possible mode of transmission. Meanwhile, when the viral droplets are <5 μm in size, corona virus could be circulated in the air ( Cook, 2020 ).

Therefore, food safety is still a concern as this does not rule out the possibility of contamination through other means, such as from person-to-person, or from person-to-object. In light of recent events, food-related companies have faced even more challenges in maintaining food safety. Not only that they have been responsible in ensuring that their products were safe and free from foodborne pathogens, these companies must now also ensure that they are not exposing their employees and customers to COVID-19 ( Jawed et al., 2020 ). Hence, maintaining food safety among food handlers is still important and should not be taken lightly in food industries.

As person-to-person transmission is the main mode of transmission for COVID-19, it is of the upmost importance that safety and hygiene guidelines are implemented and enforced in food industries. For example, an infected person who does not follow social distancing and sanitation guidelines can come into contact with other co-workers and may infect them. Thus, Malaysian government has imposed strict rules to only allow workers that have completed full doses of vaccination to resume work in the food preparation area. On another note, infection among staff members is not the only concern. Uddin et al. (2020) has added that there is a great chance of exposure of infection to healthy individuals if an infected person handles the food packaging, contaminates the packaging, and gives the infected product to a healthy, unassuming customer. This is because the virus may be able to enter the body of an healthy individual via oral, nasal, or optic routes ( Pressman et al., 2020 ). Moreover, the virus may reach fresh food products such as fruits, vegetables, and baked goods, or food packaging by means of an infected person through coughing or sneezing directly on them ( Duda-Chodak et al., 2020 ; Rizou et al., 2020 ). Therefore, personal hygiene of food handlers is paramount in food safety, more so during this COVID-19 pandemic, which should include proper handwashing procedures, strict SOPs, frequent cleaning and sanitization, maintaining food respiratory hygiene and frequent usage of alcohol based sanitisers ( Jyoti and Bhattacharya, 2021 ).

Although transmission through surface contact is not the common mode of transmission for COVID-19, there is still a possibility of transmission through food packaging materials. For example, an infected worker may expose other people to the virus by contaminating environmental surfaces or objects, which will lead to an infection when an unsuspecting person comes into contact with the item ( Duda-Chodak et al., 2020 ; Pressman et al., 2020 ). It is a complex situation as we are unable to view the virus with naked eyes to postulate which site needs to be cleaned or sanitized. Under this situation, it could lead to a rather secondary or indirect transmission. Additionally, Duda-Chodak et al. (2020) has stated that the indirect transmission of coronaviruses from contaminated surfaces has been postulated. It was reported that the coronaviruses can remain for prolonged periods in environmental samples, which may boost the chance of transmission through package contact surfaces ( Olaimat et al., 2020 ). This was further supported by Desai and Aronoff (2020) where they have stated that SARS-CoV-2 may remain active on objects or surfaces for up to 72 h. Cable et al. (2020) supported this by expressing that there has been evidence of viral RNA identified on various types of surfaces, including doorknobs and gloves, and depending on the surface, the viral half-life ranges from 1 to 2 days. In addition, Pressman et al. (2020) revealed that the SARS-CoV-2 was able to remain on cardboard for up to 24 h, and on plastic and stainless steel objects, for up to 72 h. This may come as a concern as most food packages are made of cardboard or plastic. Under such scenario, it may be speculated that food packages are able to transmit the virus to consumers or employees if it is contaminated. Thus, it is important to make sure that safety measures are enforced in restaurants and food processing or manufacturing factories to avoid any sort of contamination from workers to the food packaging materials, and from the packaging to workers or consumers. Proper sanitization performed at frequent intervals is crucial to ensure cross-contamination of the virus is not available at the industry or operational sites prior to reaching the consumers. On the other hand, consumers are also encouraged to sanitize their hands and surroundings accordingly after receiving food or groceries from restaurants or shops ( Desai and Aronoff, 2020 ). Additionally, food safety in terms on kitchen sanitation and sanitization is important to minimize the risk of transmission through tools, cooking utensils, and packaging materials from workers to workers or workers to customers. Supplementary Figure 3 shows customers adhering to social distancing guidelines while dining in ( Free Malaysia Today, 2020 ).

Therefore, although COVID-19 is not a foodborne illness, it may still be transmitted during food manufacturing and processing activities. Thus, some aspects of food safety such as personal hygiene, kitchen sanitation and sanitization process should still be emphasized greatly during this pandemic. Strict protocols must be enforced during processing and handling of foods such as not allowing individuals who are showing signs of sickness to work, increase in sanitation (handwashing with soap or disinfecting with an alcohol-based sanitiser), social distancing between individuals, as well as the use of face coverings such as face masks and face shields ( Cable et al., 2020 ). In fact, completion of two doses of vaccination is important at this stage in National Recovery Plan as enforced by the Malaysian government. Supplementary Figure 4 shows a restaurant worker complying to MCO guidelines by screening individuals who wish to enter the food premises ( Lim, 2020 ).

Steps to Ensure Food Safety

Pivotal steps must be taken to ensure the food safety in order to prevent the spread of COVID-19 by operations conducted in the food industry. As what have been mentioned previously, there are a few factors which affect food safety in the COVID-19 pandemic, which are personal hygiene of food handlers as well as kitchen sanitation and sanitization. The normal practices in personal hygiene and kitchen sanitation must be followed strictly to avoid the spread of COVID-19 through food processing activities such as manufacturing, packaging, transporting, and regular restaurant operations. Frequent sanitization is important at this point of pandemic regardless of whether dine-in is allowed. According to Djekic et al. (2021) , staff awareness and hygiene has been reported to be the two of the most important aspects of the COVID-19 pandemic which affect food safety. Supplementary Figure 5 shows some practices that are conducted to maintain personal hygiene of food handlers as well as kitchen sanitation in the food industry.

Personal hygiene of food handlers is extremely important as these handlers have prolonged contact with the food products. According to Djekic et al. (2021) , many food companies have taken the initiative to implement strict hygiene procedures as well as purchasing additional personal protective equipment (PPE) for their employees in light of the COVID-19 pandemic. Furthermore, Lacombe et al. (2020) has stated that many processing plants have also reopened with the implementation of physical barriers in support of social distancing as well as the use of PPE and completion of vaccination among workers. Thus, one of the key steps which will need to be taken to ensure food safety during the COVID-19 pandemic is in the use of proper protective attire, which includes face masks, bonnets, gloves, as well as face shields ( Cable et al., 2020 ). This step has been made compulsory to stop the transmission of the virus from person-to-person or person-to-object. Since the transmission of the COVID-19 virus is mainly through respiratory droplets produced by sneezing, coughing, or talking, the use of face coverings such as face masks and face shields are extremely crucial to stop the transmission and the contamination of food products, food contact surfaces as well as food packaging. Furthermore, the use of gloves and bonnets are important to make sure that the food does not become contaminated by the handler's hair or microorganisms which live on human skin. Not only that, the use of clean clothes by handlers is also important as the virus may also contaminate clothing items ( Duda-Chodak et al., 2020 ). Hence, the handler must ensure that their clothes are clean and they should not wear items of clothing that have been previously worn before in public places as they may be contaminated by the virus. Moreover, it is also necessary to avoid smoking, coughing, sneezing, chewing, or eating in food processing areas as these activities may cause the transmission of the virus to the environment, and not to mention to other employees.

Next, kitchen sanitation is also beneficial in stopping the transmission of the virus and to maintain the safety of the food products. The hygiene of the kitchen or production area where food is prepared is extremely important as many types of contamination to foods can arise from a dirty environment. According to Redmond and Griffith (2009) , some of the reasons as to why the hygiene of a kitchen may be compromised was due to inadequate design, lacking equipment of safe food preparation, and may be used for other non-food related purposes. Thus, several steps must be taken to make sure that the environment where food is processed is safe for its quality for human consumption. Firstly, the kitchen must be set up as to allow for the ease of proper hygiene practices such as sanitation and cleaning of floors and countertops. For instance, the kitchen should be built with materials that are suitable, durable and easy to be cleaned, in addition to being safe and not to harbor microorganisms ( Uçar et al., 2016 ). Additionally, a kitchen which has been built to cater to proper hygiene practices will ensure that the employees are able to easily carry out cleaning and sanitation practices, which in turn, will motivate them to be more inclined to continue the practice. This is vital as the continuity of cleaning and sanitation practices is as important as the design and plan of the kitchen ( Uçar et al., 2016 ). If the procedures are not carried out continuously then the kitchen cannot maintain its cleanliness. Furthermore, a cleaning and disinfection plan should be developed by the management, and the plan must be enforced and adhered to by the kitchen staff. This plan should be developed to ensure that the hygienic procedures are carried out effectively. Furthermore, it is also important to train employees on the proper sanitation and disinfection of a kitchen. In this regard, Byun et al. (2005) has stated that the level of awareness of kitchen sanitation among food service were determined by the management systems employed in the workplace as well as the extent of their sanitation training. Thus, education and training must be administered frequently and continuously to employees to strengthen the food handlers' knowledge in the area ( Abdul-Mutalib et al., 2012 ). Lastly, utensils and equipment should also be cleaned and sanitized frequently. Among various chemical disinfectants that are being used against SARS-CoV-2 virus, alcohol based solution has been the best to be used in food industries. Ethanol and isopropanol (concentration 70–90%) kills SARS-CoV-2 virus within 30 s and causes membrane damage by disrupting the tertiary structure of proteins while denaturing the virus's protein and rupturing the RNA ( Al-Sayah, 2020 ).

This is especially important in the era of the COVID-19 pandemic as the virus may contaminate kitchen utensils and equipment, which may lead to transmission to other employees or to food products or food packaging. Hence, these sanitation and sanitization plan should be in place, well-documented and included in trainings so that it can be practiced when it is necessary. Since pandemic was unexpected, management system regarding food safety should be adhered according to WHO and local Ministry of Health guidelines.

Aspects of personal hygiene of handlers and kitchen sanitation are not only important for large scale food industries or restaurants, but also necessary to be adhered to by small businesses or street food vendors. During the pandemic, it will only take one infected vendor to potentially spread the virus to a countless number of customers, vendors and even delivery personnel. For example, street food vendors or small-scale food businesses should still adhere to personal hygiene practices such as the wearing of clean clothes and proper protective attire, such as face coverings and gloves. Not only that, but vendors should also avoid doing activities that might spread diseases near food preparation areas such as smoking, coughing, eating, and sneezing. Additionally, Pritwani et al. (2015) has also stated that proper handwashing during all stages of processing must be followed strictly, as this is crucial not only to stop the spread of foodborne illnesses, but also to avoid spreading the COVID-19 virus. Supplementary Figure 6 shows a scene with street food vendors and customers seen wearing masks and adhering to social distancing guidelines.

Furthermore, kitchen sanitation is also important for street food vendors and small-scale food industries. Moreover, access to clean and safe water supply should be monitored in order to conduct proper cleaning and sanitation and sanitization activities ( Pritwani et al., 2015 ; Cortese et al., 2016 ). Additionally, it is also important for the relevant authorities to regularly monitor and supervise small-scale food vendors to ensure they are complying with proper food safety practices ( Cortese et al., 2016 ). Training must also be given as most of these small-scale vendors have not been formally educated to emphasize food safety, thus it is necessary for the relevant authorities to provide education and support to ensure that these vendors can still operate their businesses without the danger of selling food that are not safe for human consumption. For example, a recent case of food poisoning that occurred in Malaysia involved 99 victims that have consumed a local food product, “puding buih” ( Malay Mail, 2020 ). According to an article reported by New Straits Times (2020) , the dessert has been purchased online from a local vendor by the victims. Following the incident, the local authorities have provided SOPs to home-based food traders to ensure that they are able to generate income during this pandemic while at the same time able to guarantee the safety of the food being sold ( Malay Mail, 2020 ).

COVID-19 and the Food Supply Chain

What is the food supply chain.

The food supply chain can be described as the different processes that occur to bring food from production to the consumer or from farm to fork. Generally, the supply chain consists of processes such as agricultural production, post-harvest handling, processing, distribution and retail, and lastly consumption ( Rizou et al., 2020 ). The food supply chain is not a singular chain of fixed entities, instead it is a complex web of interconnected entities which work together to make the food available to the consumers ( Dani, 2015 ).

The maintenance of a functional food supply chain is very important in ensuring food can be provided to the consumers continuously. The closure of a single factory may pose a risk to a certain amount of people whom work at the factory, however the obstruction of key processes in the food supply chain such as production or distribution, may endanger a larger portion of the population that depend on the food to live ( Aday and Aday, 2020 ). This is because the disruption in the supply chain will cause a snowball effect in the food industry such as halting the processing and production of food, leading to the creation of insufficient products in the market, which in turn results in the inability to attain food by the consumers for nourishment. Thus, the COVID-19 pandemic may have serious effects to the food supply chain.

Impact of COVID-19 to the Food Supply Chain

As what have been mentioned, the COVID-19 pandemic has brought on many difficulties, especially in the food industry as many companies have been forced to either partially or even fully shut down. Many countries, including Malaysia, have implemented lockdowns and partial lockdowns periodically in order to curb the rising cases of infections as well as deaths. The overall impact on agricultural practices and business entities along the food supply chain are depicted in Supplementary Figure 7 .

One of the impacts of COVID-19 is the restriction of movement which has caused issues in the supply chain. As an example, in Malaysia, the MCO implemented by the government restricted movement by implementing travel restrictions that has further enforced by road blocks all over the country, as well as the limitation of a 10-km travel radius for all citizens ( Tang, 2020 ). When workers are unable to get to work due to travel restrictions, then the processes in the supply chain will be incapacitated ( Aday and Aday, 2020 ). During the first few weeks of the implementation of the MCO in Malaysia, many food supply chains, especially those in urban areas, have been disrupted due to these travel restrictions. Many of these supply chains rely on the use of land transports such as lorries to carry their products from farms located far from the urban cities ( Chin, 2020 ). This was supported by Tumin et al. (2020) which has stated that the MCO has affected the supply chain or organic food products in Malaysia in which these restrictions have heavily impacted the distribution of products from the producers to the consumers. As a result, some farmers or growers have resorted to send their produce out to charity, or those who had rose up white flags at their homes due to financial difficulties. The raising of the white flags started initially in front of residential homes; with further neighbors tend to help out with groceries and home basic necessities. Later on, several apps such as Bendera Putih and White Flag were developed by local Malaysians to track suffering families and anyone nearby can help out based on the app. Website Kita Jaga Malaysia ( kitajaga.co ) has also been developed for this cause ( Angelin, 2021 ).

Furthermore, lockdowns have led to other disruptions in the food supply chain, which was due to a shortage of labor ( Singh et al., 2020 ). Verma and Prakash (2020) have stated that about 13 million people all over the world may face unemployment, according to the International Labor Organization (ILO). Moreover, Nicola et al. (2020) has further indicated that the restrictions brought on by the pandemic has led to a reduction in the workforce across all economic sectors, causing many jobs to be lost. The National Recovery Plan has been introduced in June 2021 to minimize the surging number of COVID-19 cases in Malaysia due to the third-wave. Under this plan, the workers were encouraged to get vaccinated to reduce the overloading the hospitals.

As an example, Dr. Tey Yeong Sheng, a researcher at the Institute of Agricultural and Food Policy Studies at Universiti Putra Malaysia has stated that labor shortages was one of the main difficulties faced by local farmers in food production ( Chung, 2020 ). These farmers were faced with many obstacles as they are reliant on workers to harvest crops as well as for preparation of land. Thus, when these workers face difficulty in crossing states and traveling, the food production will be disrupted. This has affected the processing of crops, livestock, and fishery sub-sectors in the food industry, and it has impacted the agriculture value chain as well as the availability of these foods ( Vaghefi, 2020 ). Supplementary Figure 8 shows a lone farmer working in a field ( Man, 2020 ).

Labor shortages affect many levels of the food supply chain as each process requires workers to complete hands-on tasks such as harvesting, processing, and manufacturing. Even though some companies manage by allowing their employees to work from home, the same cannot be applied for the food industry as most businesses require workers to work hands on, such as in agricultural production or post-harvest handling. For instance, a vegetable producer may experience problems from shortage of labor, thus not allowing the farmer to harvest as many vegetables as usual. Therefore, there will be a shortage in the production of fresh vegetables.

Moreover, labor shortages will also affect the food distribution system due to the unavailability of workers, such as truck drivers to transport the food products from the distributors to the consumers ( Mahajan and Tomar, 2020 ; Singh et al., 2020 ). Surendran (2020) also pointed out that the number of employees working in day-to-day operations on farms has also been limited during the period of MCO in Malaysia. This view was supported by Nicola et al. (2020) , where the restrictions imposed due to the COVID-19 pandemic has been found to have impacted the availability of workers such as inspectors as well as delivery staff in ensuring the verification and transportation of food products. This in turn will cause a lack of food items being made available to the consumers ( Singh et al., 2020 ).

In addition, labor shortages also cause losses for the farmers. For example, due to the MCO conducted in Malaysia, 2,300 farmers had suffered a reported loss of RM1 million per day due to their inability in selling harvested produce, thus they were discarded as waste ( Man, 2020 ). Similarly, it has been reported that about 200 farmers were unable to sell their vegetables in Gua Musang, leading to a total loss of RM400,000 a day. They had been forced to discard up to 200 metric tons of vegetables per day. This is because agricultural produce such as vegetables and fruits are perishable items, and as such, when there are not enough workers available to harvest, process, and transport the products for sale, then the produce will not be sold and has to be discarded as waste. Furthermore, this situation occurs as consumers opt for online purchases rather than to go out to obtain their weekly groceries.

Additionally, the farmers also suffered loss as the MCO had required closure of many businesses as well as restriction of the number of people allowed in a certain area. This was due to the difficulty of exercising social distancing in many markets where farmers usually sell their produce, thus many of these markets have been forced to close down, or allowed to open but with limitations ( Chin, 2020 ). Supplementary Figure 9 shows a vendor in a market wearing protective clothing while waiting for customers ( Hassan and Leong, 2020 ). In order to support the current economic situation, National Recovery Plan has been introduced in a few phases based on number of cases and utilization of ICU beds in hospitals in different states. Hence, workforce is allowed with 2 completed doses of vaccination and to maintain strict SOP at the workplace.

For example, a wholesale market in Selayang, Selangor has been ordered to reduce the amount of workers and its operating hours, which has caused vegetable farmers and fishermen to forcefully dump their stock of produce as the products were unable to be sold ( Hassan and Leong, 2020 ). This situation had also been seen occurring in farmers in Cameron Highlands that had to dump or gave away their produce due to the perishable nature of their products ( Ng and Wahid, 2020 ). Supplementary Figure 10 shows a photograph of a worker destroying vegetables on a farm as they cannot be sold due to issues arising from the COVID-19 pandemic ( Surendran, 2020 ).

In addition, unavailability of food products is also a resulting effect from the COVID-19 pandemic on the food supply chain. For example, during the start of the pandemic where initial lockdowns were announced, many consumers have exhibited panic buying and hoarding ( Aday and Aday, 2020 ; Singh et al., 2020 ). As COVID-19 was still unknown then, consumers were uncertain of the severity of this virus and how to handle the lockdown restrictions, thus many had been seen buying large amounts of food items that they could store and use in an emergency such as canned foods. Furthermore, Koh et al. (2020) has stated that panic buying may occur when people observe other people in buying certain products, then mass fear infects the individual as they do not want to be left out of owning an item that appears to be running out. This was seen when people kept buying items even if they did not necessarily need them. However, these hoarding and panic buying have caused the sudden surge of demand for food items ( Singh et al., 2020 ), As a result, many manufacturers and retailers had not been able to keep up with the demand, thus some less unfortunate people were unable to buy any food products to stock up during the lockdown. Furthermore, panic buying has also caused the increase in concerns of food shortages, including long-life foods like UHT milk, rice, pasta, as well as canned foods ( Nicola et al., 2020 ). The unavailability of food products would also induce price spikes due to high demand ( Aday and Aday, 2020 ; Mahajan and Tomar, 2020 ; Reardon et al., 2020 ). The increase in prices will negatively affect poorer households as certain food items will no longer become accessible to them ( Mahajan and Tomar, 2020 ). Lastly, the lack of food products in the market will give health repercussions as well-due to a decrease in intake of nutritionally balanced foods and lack of diversity in the diet ( Mahajan and Tomar, 2020 ). This is especially dangerous during a pandemic as maintaining one's health is of upmost importance in order to avoid contracting COVID-19 ( Uddin et al., 2020 ). Supplementary Figure 11 shows consumers crowding at a grocery store following announcements of a MCO ( Free Malaysia Today, 2021 ).

Conclusion and Recommendations

In conclusion, the COVID-19 pandemic has brought on some effects to food safety and the food supply chain. Although COVID-19 is said to not be a foodborne virus, it is still important to maintain proper food safety protocols in the food industry. The novelty of this study is to highlight that maintaining good personal hygiene of handlers is utterly important in food industries. Completion of the vaccination dosage is vital to achieve herd immunity. Besides, it is significant to point that the maintenance of kitchen sanitation is essential during this pandemic. This is due to the possibility of transmission of COVID-19 through the food handlers as well as by food packaging materials. It is important for food handlers to maintain good hygiene and kitchen sanitation to help keep themselves safe, as well as their surroundings clean and free from contamination, which in turn will minimize the spread of COVID-19. It seems like a complex mechanism, however, the safety of food and handlers can be maintained altogether if managed properly. Furthermore, COVID-19 has also made an impact on the food supply chain. Due to the strict lockdowns as well as many protocols involving social distancing and travel restrictions, the food supply chain has seen some negative effects in light of this pandemic. Some of these effects include shortages in labor which have caused disruption in the supply chain, as well as the lack of distribution of food products to consumers. Next, other effects include shortages of food, increase in prices, and health repercussions to the consumers due a lack of diversity in the diet and a decrease intake of nutritious foods. It is therefore crucial to ensure that the food supply chain has a smooth progression to maintain the constant supply of food commodity for consumption in Malaysia. At the moment, it is quite common to have delays in supply than usual due to current supply chain situation. All the threats and implication presented in this review have been assessed thoroughly, where the information was extracted from reports, local newspaper articles and manuscripts. This study is important to policymakers in the food industries, enabling designing management system and training needed during and post-pandemic situation to ensure continuous food safety and supply chain are in good progression.

As a recommendation, more research must be conducted in the future to combat this virus. Since there are currently no official guidelines and protocols that exist to detect the presence of the SARS-CoV-2 virus on surfaces as well as public places ( Lacombe et al., 2020 ), relevant bioanalytical tools such as a method of tracing and detection of SARS-CoV-2 in the environment where food is processed, manufactured, and handled ( Rizou et al., 2020 ) should be developed. This would be useful in distinguishing the presence of the virus on environmental surfaces, as well as help minimize and eliminate the possibility of transmission through food products, food packaging materials and surrounding environments. Lockdown cannot be considered a permanent solution to fight this pandemic in the long run due to its many implications in the social perspective as well as in the economical perspective ( Singh et al., 2020 ). Until then, everyone must do their part to protect themselves, and everyone around them from this virus by practicing social distancing, frequent handwashing, and sanitization, in addition to using face masks in public as well as in achieving herd immunity by completing the vaccination doses required. At the same time, minimizing transmission within places where food is handled, including food processing facilities, restaurants, and grocery stores, is key in protecting workers and customers, as well as in combating the spread of COVID-19 ( Cable et al., 2020 ).

Data Availability Statement

The original contributions presented in the study are included in the article/ Supplementary Material , further inquiries can be directed to the corresponding author/s.

Author Contributions

NE conducted the research, as well as literature search. AF and SR gave input on drafting the review article and conceptual the article based on current pandemic situation. TM gave constructive comments to improve the article. All authors contributed to the article and approved the submitted version.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

The authors would like to thank the Grant Scheme: 600-RMC/GPK 5/3 (229/2020) from Universiti Teknologi MARA.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fsufs.2021.682263/full#supplementary-material

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Keywords: food safety, food supply chain, post pandemic, Malaysia, threat

Citation: Nurul Eiman MS, Aida FMNA, Mahmudiono T and Raseetha S (2021) Systematic Review on Food Safety and Supply Chain Risk Assessment Post Pandemic: Malaysian Perspective. Front. Sustain. Food Syst. 5:682263. doi: 10.3389/fsufs.2021.682263

Received: 31 March 2021; Accepted: 28 October 2021; Published: 29 November 2021.

Reviewed by:

Copyright © 2021 Nurul Eiman, Aida, Mahmudiono and Raseetha. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Siva Raseetha, raseetha@uitm.edu.my ; orcid.org/0000-0002-4106-4903

This article is part of the Research Topic

COVID-19: Food System Frailties and Opportunities

• Research article
• Open access
• Published: 03 May 2021

Food safety knowledge, attitude, and hygiene practices of street-cooked food handlers in North Dayi District, Ghana

• Lawrence Sena Tuglo 1 ,
• Percival Delali Agordoh 2 ,
• David Tekpor 3 ,
• Zhongqin Pan 1 ,
• Gabriel Agbanyo 3 &
• Minjie Chu   ORCID: orcid.org/0000-0002-7533-9119 1  

Environmental Health and Preventive Medicine volume  26 , Article number:  54 ( 2021 ) Cite this article

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Metrics details

Food safety and hygiene are currently a global health apprehension especially in unindustrialized countries as a result of increasing food-borne diseases (FBDs) and accompanying deaths. This study aimed at assessing knowledge, attitude, and hygiene practices (KAP) of food safety among street-cooked food handlers (SCFHs) in North Dayi District, Ghana.

This was a descriptive cross-sectional study conducted on 407 SCFHs in North Dayi District, Ghana. The World Health Organization’s Five Keys to Safer Food for food handlers and a pretested structured questionnaire were adapted for data collection among stationary SCFHs along principal streets. Significant parameters such as educational status, average monthly income, registered SCFHs, and food safety training course were used in bivariate and multivariate logistic regression models to calculate the power of the relationships observed.

The majority 84.3% of SCFHs were female and 56.0% had not attended a food safety training course. This study showed that 67.3%, 58.2%, and 62.9% of SCFHs had good levels of KAP of food safety, respectively. About 87.2% showed a good attitude of separating uncooked and prepared meal before storage. Good knowledge of food safety was 2 times higher among registered SCFHs compared to unregistered [cOR=1.64, p =0.032]. SCFHs with secondary education were 4 times good at hygiene practices of food safety likened to no education [aOR=4.06, p =0.003]. Above GHc1500 average monthly income earners were 5 times good at hygiene practices of food safety compared to below GHc500 [aOR=4.89, p =0.006]. Registered SCFHs were 8 times good at hygiene practice of food safety compared to unregistered [aOR=7.50, p <0.001]. The odd for good hygiene practice of food safety was 6 times found among SCFHs who had training on food safety courses likened to those who had not [aOR=5.97, p <0.001].

Conclusions

Over half of the SCFHs had good levels of KAP of food safety. Registering as SCFH was significantly associated with good knowledge and hygiene practices of food safety. Therefore, our results may present an imperative foundation for design to increase food safety and hygiene practice in the district, region, and beyond.

Introduction

A report by the World Health Organization (WHO) (2015) showed that about two million incurable cases of food poisoning materialize annually in unindustrialized nations. The WHO further estimates that 600 million food-borne diseases (FBDs) each year were related to poor food safety and hygiene practice with 420,000 deaths [ 1 ], the majority attributed to meat-related vulnerabilities [ 2 ]. About, 76 million FBDs caused 325,000 hospitalizations in the USA which led to 5000 deaths [ 3 ]. The source was associated with the consumption of turkey contaminated by Salmonella enterica serovar Heidelberg , responsible for salmonellosis in the USA [ 4 ]. Almost, 1.3 million FBDs resulted in 21,000 hospital stays reported in England which led to 500 deaths. The contamination was due to sprouts by Escherichia coli O104 [ 3 ]. Around 53% of the food-borne problems and 31% of its associated illness were attributed to meat consumption in the Netherlands [ 2 ]. The rate of FBDs in Malaysia was 47.8% out of 100,000 people who patronized street-cooked foods [ 5 ]. In Ghana, about 65,000 persons including 5000 kids below 5 years died yearly due to FBDs [ 6 ].

The risk factors such as inappropriate time interval, unsuitable temperature, weather condition, unhygienic activities, unacceptable handling of foods, foodstuff from insecure origins, impoverished self-cleanliness, improper cleaning of cooking materials, using untreated water, and improper food storages were attributed to the causes of FBDs [ 7 , 8 , 9 ]. Also, neglect of hygienic measures by food handlers has been implicated as enablers for the spread of pathogenic microorganisms [ 10 ] and the cause of infections among consumers [ 11 ].

Studies recount that 12 to 18% of food-borne illnesses are attributable to contaminations [ 12 , 13 ], poor food safety, and inappropriate hygiene practices which were accredited to street-cooked food handlers (SCFHs) [ 14 , 15 ]. These SCFHs are people who are wholly or partly engaged in the food preparation, processing, and production value chain and who have a direct touch on food and cooking utensils [ 9 , 16 ]. Foods prepared by food handlers under unhygienic conditions become a public health concern both in industrialized and low-income countries [ 17 ]. Food safety and hygienic practices of SCFHs are essential to ensure that food is free from any forms of contamination through preparation and processing for consumption and to prevent the spread of FBDs [ 18 , 19 ].

Food safety knowledge (FSK) is the understanding of food learned from skills or schooling, food safety attitude (FSA) refers to sensation or belief about food safety, and food safety practice refers (FSP) to the act or use of food safety [ 20 ]. Food safety knowledge, attitude, and practices (KAP) are important because inadequate knowledge, poor attitude, and poor sanitation practices by SCFHs have a severe danger to food safety applications in food companies [ 21 ]; hence, KAP of food safety contributes significantly to the occurrence of food poisoning and FBDs among consumers [ 22 ].

A study conducted in Brazil among food truck food handlers revealed poor hygiene, poor clean observes, poor environments, and higher contaminated meals [ 23 ]. The problem of FBDs was higher in Southeast Asian and African counties [ 24 ]. Ma et al. [ 25 ] study in China, among street food vendors, revealed poor behaviour practices and knowledge of food safety among the respondents. Tabit and Teffo [ 26 ] in South Africa found over 60% of the respondents keep good knowledge and acceptable hygiene performance of food safety. Lema et al. [ 27 ] in Ethiopia reported that below half of the respondents obtained good food cleanliness applications. The effects of food-related illness expenditures in hospital treatments are about US$ 110 billion annually in developing countries, which resulted in decreasing production [ 28 ].

The recurrent happenings of food-related illnesses brought in its wake concerns about the food safety knowledge and hygiene among SCFHs [ 29 ]. Maintaining food safety involves establishing global laws conferring to an agreement between institutions that actualized this agenda [ 30 , 31 ]. The Government of Ghana affirmed food safety regulations in collaboration with the Food and Drug Authority (FDA) [ 30 ]. Yet, its application is undermined due to ineffective supervision by appropriate agencies [ 32 ]. The problem was due to the broad governmental assembly in cities and communities under the local administration [ 31 ]. Some local studies conducted in the four regions of Ghana such as Greater Accra, Northern, Western, and Central have reported adequate knowledge, good attitude, and positive behavioural practices of food safety and handling practices [ 11 , 33 , 34 , 35 ]. Studies have shown that SCFHs were not knowledgeable about the WHO’s Five Keys to Safer Food for food handlers [ 33 , 36 ] which include keeping clean, separating raw and cooked food, cooking thoroughly, keeping food at safe temperatures, and using safe water and raw materials [ 37 ].

Hence, the acceptance and the use of the KAP instrument as a problem-solving approach in this study are validated from previous researches [ 23 , 38 , 39 ]. This would adequately support the policymaking development and the change of embattled intervention policies for the prevention and control of FBDs. The KAP’s tool assessment defined in this study is considered appropriate to other frameworks if the statements in the KAP’s sections are validated. To our knowledge, no research has yet been done on KAP of food safety among SCFHs selling commonly consumable foods on the street in Volta Region, Ghana. Hitherto, the high cases of FBDs such as diarrhoea, cholera, and typhoid fever outbreak occurrences in the district are presumed to be influenced by SCFHs. The KAP of SCFHs on food safety and hygiene precautions ruins uncertainty in the district, and a swift policy to mend some causes central to the occurrence of FBDs is obligatory. This would help the District Health Directorate’s regulatory agency to plan the prevention methods. Therefore, this study assessed knowledge, attitude, and hygiene practices of food safety on SCFHs in North Dayi District, Ghana.

Materials and methods

Study design and setting.

This study was a descriptive cross-sectional carried out between August and November 2020 and used a validated, pretested, and structured questionnaire to collect data from stationary SCFHs along the principal streets within North Dayi District. North Dayi District is one of the 18 administrative districts in the Volta Region, Ghana [ 40 ]. It shares boundaries with Kpando Municipal to the north, South Dayi District to the south, and Afadzato South District to the east. The entire residents of the North Dayi District are 39,913 covering 46.7% men and 53.3% women [ 40 ]. The people of the District constitute 1.9% of the total population of the Volta Region [ 40 ]. Farming is the foremost financial activity, making it one of the main sources of income in the district [ 40 ]. We carried out this study because of the recent cases of food-borne illness reported among the residents such as diarrhoea, cholera, and typhoid fever in the district [ 41 ].

Eligibility criteria

Stationary SCFHs who directly served already cooked food to customers and those who owned their outlets were included in the study. SCFHs who dissented to partake in the research were excepted including all assistants and helpers. The assistants and helpers were excluded because not all vendors had assistants or helpers and they tend to be more in numbers than the vendor-owners themselves. So for as not to allow bias in the results, we chose to sample only the vendor-owners. Moreover, vendor-owners tend to have direct responsibility for monitoring the food safety environment of their vending sites; hence, we chose to sample them as the focus of this study.

Sample size and sampling

Cochran’s formula Z 2 p  (1 −  p )/ e 2 [ 42 ] for unknown study populations was used. Since a similar study in the Volta Region of Ghana among the population subgroup is unavailable, 50% was used for response distribution, with 95% confidence level, and a margin of error of 5% for the populace, plus 10% non-response rate which gave us a sample size of 423.

Data collection tools

A structured questionnaire was designed based on different studies conducted globally [ 16 , 20 , 38 , 39 , 43 , 44 , 45 , 46 ]. Similar versions of the questionnaires were used in studies conducted in Ghana [ 47 , 48 , 49 ]. The instrument was distributed into 4 parts: socio-demographics, knowledge, attitude, and hygiene practices. The statements on KAP were adapted from the WHO’s Five Keys to Safer Food guidebook for food handlers [ 37 ]. The questionnaire was firstly designed in English, then converted to local dialects, and translated back to English to ensure reliability and simplicity of the question. Four professionals in the field of the study assessed the face and the content validity of the questionnaire. The questionnaire was pretested on 12 stationary SCFHs in Tanyigbe located 7 km from the study area. The pretesting findings were not added to the main study but were used to modify some questions to improve their clarity. The most pertinent modifications done on the study instrument were a cooked meal should stay hot more than 60°C before serving, putting uncooked and prepared meal separating prevent cross-contamination, and checking and dispose of meal that past their expiry date. The data were collected through trained research assistant-led interviews which lasted for about 25 min per respondent. The interviewer-administered questionnaire was given to the SCFHs who could read and write to answer by themselves while those SCFHs who could not read and write have been aided by the research assistants in answering the questionnaire.

Determination of knowledge, attitude, and hygiene practices on food safety

Section 2 of the questionnaire contained 10 structured questions on knowledge of food safety with 3 likely responses; “true”, “false”, and “do not know”. The questions precisely covered the respondents’ knowledge of individual cleanliness, food-borne illnesses, microbes, infection control, and sanitary practices. Each correct knowledge item reported was awarded a score of 1 point. Incorrect knowledge was awarded a 0 score (including “do not know”). In this study, if “true” is the correct answer, then “true” is score 1 point while “false” is score 0 point or otherwise reverse.

Queries relating to attitudes in the third segment of the questionnaire were designed to assess the knowledge of SCFHs on food wellbeing and hygiene. This part of the section assessed psychological state concerning views, opinion, morals, and characters to act in particular [ 21 , 48 ]. It contains 10 structured queries with 3 likely answers: “agree”, “disagree”, and “not sure”. Each correct attitude reported was awarded a score of 1 point while the other incorrect attitude option was rated a 0 score (including “not sure”). In this study, if “agree” is the correct answer, then “agree” is score 1 point while “disagree” is score 0 point or otherwise reverse.

• Hygiene practice

Section 4 of the questionnaire measured food hygiene and sanitation practices of SCFHs. It contained 10 structured queries with 2 likely answers: “yes” and “no”. Each correct hygiene practice reported was awarded a score of 1 point while incorrect hygiene practices reported were awarded a score of 0. This method of assessment was used in previous studies [ 28 ]. In this study, if “yes” is the correct answer, then “yes” is score 1 point while “no” is score 0 point or otherwise reverse.

The grouping method is appropriate and suitable for studies allied to the assessment “of food handlers” KAP of food safety and hygiene [ 27 , 28 , 34 , 46 , 47 , 50 , 51 , 52 ]. The knowledge and attitude questions with “do not know” or “not sure”, thus the third option, had been presented to enable simplicity of responding by SCFHs for fascinating for thoughts considered by an undecided or doubtfulness [ 28 ]. This third option “do not know” or “not sure” always scores a 0 point due to the cumulative percentage approach adapted which considers only the acceptable response or the correct answer [ 53 ]. The cumulative percentage scoring method of assessment considers only the acceptable answer and the total cumulative score is converted to 100% [ 53 ]. The cumulative scores below 70% of the acceptable responses on WHO’s Five Keys to Safer Food-related knowledge, attitude, and hygiene practices were considered as “poor”, and cumulative scores 70% and higher were considered as “good” [ 27 , 34 , 39 , 46 , 48 ].

Data analysis

Questionnaires were checked manually before entering into Microsoft Excel 2016 spreadsheet. Coding and analysis were done in IBM Statistical Package for Social Sciences (SPSS Inc., Chicago, USA; https://www.spss.com ) version 24.0. Categorical variables were expressed as frequency and percentage. The disparity between categorical variable groups was verified using the Fisher exact or chi-square test where appropriate. Significant parameters were used in bivariate and multivariate logistic regression models to calculate the power of the relationships observed. A p -value <0.05 was considered statistically significant.

Ethical consideration

Approval was sought from Ghana Health Service, North Dayi District Health Directorate, with the identity (NDDHD/GR/002/20) 15/07/2020. The research assistants introduced themselves and written informed permission was sought from the respondents. The research method was plainly explained to the respondents in their native dialects (English, Ewe, or Twi). Participants were identified by study numbers. The study numbers of the participants were kept in both locked files and secured computer files and accessible only to key investigators. All data were anonymized and unlinked to the respondents’ identities during the data analysis.

Demographic data

A total complete of 423 questionnaires were conveniently distributed for data collection based on the availability of SCFHs at their dedicated vending sites. Questionnaires of 407 were fully answered and collected from the respondents with a 96.2% (407/423) success rate. n = Z 2 p  (1 −  p )/ e 2   = 1.96 2 0.5 (1 − 0.5)/0.05 2 =384.16+38.416 =422.576. The majority ( n =343; 84.3%) of SCFHs were female, were between the age range of 26 and 35 years ( n =153; 37.6%), and were married ( n =311; 76.4%). Over one-third ( n =144; 35.4%) of SCFHs had attained secondary education. Most ( n =168; 41.3%) of SCFHs earned an average monthly income between GHc501 and GHc1000. Over half ( n =217; 53.3%) of SCFHs had 3–10 years of working experience. Regarding SCFH registered, n =297 (73.0%) reported that they have registered. More than half ( n =228; 56.0%) of SCFHs had not attended a food safety training course (Fig. 1 ).

Demographic data of respondents

Food safety knowledge

Almost all ( n = 381; 93.6%) of SCFHs knew about the washing of hands for 1 min using water and soap before touching food. The majority ( n =313; 76.9%) of SCFHs knew that similar chopping board should not be used for uncooked and prepared foods if it appears wash; n = 336 (82.6%) knew that cooked meal should stay hot before serving (more than 60°C); and n = 275 (67.6%) knew that excess meal should be kept at zone temperature and eat for the following mealtime. Most ( n =239; 58.7%) of SCFHs knew that uncooked meal should be kept individually from a prepared meal; n = 363 (89.2%) knew that treated water should be used for cooking; n = 363 (89.2%) knew that cockroach and house flies should not be allowed into the kitchen; and n = 274 (67.3%) knew that wiping cloths can spread microorganisms and cause disease. However, the majority ( n =235; 57.7%) of SCFHs did not know that food cooking utensils should not be cleaned using tap water only. Also, n = 202 (49.6%) of SCFHs did not know that fresh meat should not be stowed anyplace in the fridge once it is cool (Table 1 ).

Food safety attitude

The majority ( n =277; 68.1%) of SCFHs disagreed that regular hand cleaning throughout meal processing is needless; n = 323 (79.4%) agreed that cleaning kitchen shells lessen the danger of infection, and n = 355 (87.2%) agreed that putting uncooked and prepared meal separating stop infection. Below half ( n =181; 44.5%) of SCFHs agreed that they should be able to differentiate healthy diets and rotten food through eyeing; n =262 (64.4%) disagreed that using different knives and chopping materials for a fresh and prepared meal require more time; n = 366 (89.9%) agreed that they cough or sneeze inside the elbow if towel or paper not available; n = 291 (71.5%) agreed that checking meal for cleanliness and healthiness is important; and n =377 (92.6%) agreed that it is vital to dispose of meals that have gotten to expiring date. Nevertheless, n = 332 (81.6%) of SCFHs agreed that it is acceptable to use the same cloth for dusting and drying and n =217 (53.3%) disagreed that is unhealthy to allow prepared meal stay outside of the fridge for over 2 h (Table 2 ).

Food safety hygiene practice

The majority ( n =343; 84.3%) of SCFHs cleaned their fingers throughout meal cooking; n = 267 (65.6%) washed their cooking utensils used to cook a meal before using for a different meal; n =234 (57.5%) used different cooking bowls and chopping material if cooking a fresh and prepared meal; and n =359 (88.2%) dispersed uncooked and prepared meal before preservation. Also, n =278 (68.3%) keep prepared food at room temperature for 2 h when finished cooking; n =269 (66.1%) checked and disposed of meal past its expiry date; n =372 (91.4%) cleaned fresh food that needs no cooking before consumption; n =320 (78.6%) inspected if a meal is cooked by eyeing; and n =359 (88.2%) examined if a meal is grilled by touching it. Moreover, n =253 (62.2%) used similar kitchen cloth to clean shells and hands (Table 3 ).

SCFH knowledge, attitude, and hygiene practice on food safety classification

A high proportion ( n =274, 67.3%; n =237, 58.2%; and n =256, 62.9%) of SCFHs had good levels in knowledge, attitude, and hygiene practices on food safety (Fig. 2 ).

Levels of respondents’ knowledge, attitude, and hygiene practice on food safety

Association between knowledge, attitude, and hygiene practice and demographic data

Statistical significance was observed in the knowledge section among registered SCFHs ( p =0.031). None of the respondent’s socio-demographic data was statistically significant in the attitude section of food safety p < 0.05. The study found significant differences ( p <0.05) in the hygiene practice scores section with the educational status, average monthly income, registered SCFHs, and SCFHs completing food safety training course of food safety among SCFHs (Table 4 ). The odds ratio showed registered SCFHs were 1.6 times good at food safety knowledge likened to unregistered SCFHs [cOR=1.64 (95% CI 1.04–2.59), p =0.032]. The logistic regression analysis revealed that respondents who had secondary education were 4.1 times good at hygiene practice of food safety [aOR=4.06 (95% CI 1.63–10.11), p =0.003] compared to informal education. The respondents with average monthly income greater than GHc1500 were 4.9 times more likely to have good food safety and hygiene practices compared to those who earned less than Ghc500 average monthly income [aOR=4.89 (95% CI 1.56–15.34), p =0.006]. Meanwhile, registered SCFHs were 7.5 times more likely to have good food safety and hygiene practices compared to unregistered SCFHs [aOR=7.50 (95% CI 4.27–13.19), p <0.001]. The SCFHs who had completed a food safety training course were 6 times more likely to have good food safety and hygiene practices compared to those who had no such training [aOR=5.97 (95% CI 3.50–10.18), p <0.001] (Table 5 ).

Pearson correlation between knowledge, attitude, and hygiene practice toward food safety

The study revealed a positive correlation in the knowledge with the attitude outcomes sections (FSA) of food safety ( r =0.153, p =0.002) (Table 6 ).

The present study investigated knowledge, attitude, and hygiene practices of food safety on SCFHs in North Dayi District of Volta Region, Ghana. This study showed that the majority of SCFHs had good knowledge of food safety. This would help decrease the threat to contamination of foods, food poisoning, and FBDs to the consumers. Studies conducted in Saudi Arabia, Ethiopia, and Ghana have identified the importance of knowledge of food safety to SCFHs and have recommended training programmes on food safety to cultivate the knowledge into hygiene practices [ 14 , 27 , 34 ]. Our finding is inconsistent with previous studies done in Ethiopia and Jordan [ 38 , 45 ], however consistent with studies conducted in Ghana and Malaysia [ 47 , 54 ]. The possible reasons could be the type of food training courses received, the sample size, the scoring rubric applied, and understandings acquired on the subjects. This supported claims, creating an optimistic culture of food safety, inhibit food contamination if incorporated periodically [ 44 , 46 ]. This scenario affirms that the food safety training courses may remarkably enhance the knowledge of food handlers, especially concerning FBDs.

This study found that most of SCFHs knew about the washing of hands for 1 min using liquid and cleanser before touching food, which coincides with the study done in Iran [ 39 ]. The washing of hands with soap and water could reduce contamination of hands, cooking utensils, and cooking preparation surfaces leading to a substantive reduction of the risk of FBDs. Our finding does not corroborate with finding from a study done in Malaysia where a vast majority of SCFHs were knowledgeable of the 4th WHO Five Keys to Safer Food to keep the meal at healthy temperatures [ 20 ]. In our study, the SCFHs wrongly answered that fresh meat should be bestowed at any place in the fridge once it is cool. This misapplication of temperature could result in contamination and possibly proliferating of microbes in food. The reason is that appropriate temperatures can significantly lessen the risk at which foods will deteriorate, thereby preventing FBDs; hence for safety, foods must be held at an appropriate temperature sufficient to slow down the growth of microorganisms or kill microbes.

Attitude is one of the key elements that influence food safety and the practice and lessen the recurrence of food-related illnesses [ 51 ]. This study showed that most of SCFHs had a good attitude toward food safety. It means they understood their roles in food safety which was transmitted into attitude because they possibly serve as a vector for infectious pathogens which lead to food contamination. This agrees with studies conducted in Ghana and Haiti [ 48 , 55 ], but differs from a study done in Malaysia [ 36 ], where the majority of SCFHs had a poor attitude toward food safety. Possibly these could be due to the variances in socio-demographic characteristics, study population, and the study settings. These attitudinal variations could also be due to public reputation preference. Our study showed that visual checking was one of the key ways of differentiating healthy food from rotten ones, which concurs with a study conducted in Iran [ 39 ]. This finding is disturbing because the process of identifying food contamination cannot be performed by visual checking, since pathogens or toxins might be present in those foods without necessarily affecting SCFHs’ sensory aspects (smell, colour, or taste); therefore, food handlers who rely on visual checking for the identification of food contamination might expose consumers to an increased risk of contracting FBDs [ 39 , 56 ]. Therefore, the regulatory authorities must ensure that all SCFHs are trained professionally and certified.

The present study revealed a vast majority of SCFHs agreed that putting uncooked and prepared meal separating prevent cross-contamination, which corresponds to a study done in Haiti [ 55 ]. This act of putting fresh foods separating from cooked food could help prevent cross-contamination, which in turn may prevent infections from happening and halt FBDs. This is one of the highly endorsed public health measures to prevent cross-contamination [ 57 ]. This study found that almost all of SCFHs agreed that they coughed or sneezed into their elbows if a towel or paper is not available. Coughing and sneezing into the elbow or covering coughs and sneezes, and immediately washing the hands, could help to avert the spread of severe respiratory infections such as influenza and whooping cough. Our finding contradicts with other studies conducted in Malaysia and America; they reported that almost all respondents sneezed right away into their hands and never clean it [ 20 , 58 ]. This unpleasant attitude is harmful to the public since sneezing and coughing let out droplets of watery and perhaps transmittable microorganisms which can contaminate foods leading to FBDs.

Preservation of good sanitary behaviours is one of the goals for any food establishment, thereby its observance is vital to ensure safe meals for consumers [ 28 , 59 ]. The proportion of SCFHs in this current study with good hygiene practices of food safety corroborates with previous studies conducted in Saudi Arabia and Ghana [ 21 , 34 ]. This is an indication that SCFHs can be relied upon to act as the first-line responder to prevent several FBDs when they practice what they know. This would help reduce accidental contamination of foodstuffs due to improper management of cooking utensils and surroundings. Contradictory, in the present study, the scores obtained on the practices section were higher than hygiene practices of food safety reported in studies done in China and Nigeria [ 25 , 60 ]. The likely explanations of the difference reported could be as a result of the research population, the study cut-off used, the disparity in food safety courses, and differences in the law enforcement regimes. Our study revealed that the level of hygiene practices score was greater than the level of the attitude score attained by the SCFHs which corresponds to a study conducted in Malaysia [ 15 ]. The probable justification could be the SCFHs tend to provide responses they trust will create a good picture of their hygiene practices which account for the greater level score. The current study revealed that a vast majority of SCFHs washed their cooking utensils used to cook meals before using them for different meals, which is in line with a study done in Iran [ 39 ]. This act is acceptable because food handlers have been mostly identified as a significant vector for food contamination and responsible for FBDs [ 14 , 15 ]. Our study found that SCFHs practised wrongly by using similar kitchen cloth to clean shells and hands at the time which concurs with a study done in Malaysia [ 20 ]. The possible justification could be due to the non-compliance of the respondents to food safety training received. It could also be that they lack understandings of food safety education received. Hence, this displeasing practice may eventually result in contamination of hands and transfers of microorganisms to the consumers. This study showed that a vast majority of SCFHs cleaned fresh food that needs no cooking before consumption, which is in line with a study conducted in Malaysia [ 20 ]. This good hygiene practice is necessary to the elementary control of the spread of possibly FBDs.

Our study revealed a positive relationship between knowledge and the attitude of food safety which corresponds to earlier studies conducted in Malaysia, Iran, and Ghana [ 15 , 39 , 47 ]. Nevertheless, the strength of the correlation identified in the knowledge with the attitude scores of food safety was not strong, which implies that it is vital for the respective agency to monitor SCFH activities and enforce safety standards. Previous studies conducted in Malaysia and Iran found no significant relationship in the knowledge with the hygiene practices of food safety [ 20 , 39 ], which corresponds to our finding but contradicts with studies done in Malaysia and Ghana [ 15 , 47 ]. This result confirms the assertion that good knowledge does not affect the hygiene performance of food safety [ 61 ]. Hence, food handlers should be encouraged by food safety regulatory agencies to at least practise good hygiene irrespective of their levels of knowledge of food safety. In our study, no statistical association was found in the attitudes with the hygiene practice scores of food safety, which opposes earlier studies conducted in Malaysia, Iran, and Ghana [ 39 , 47 , 54 ]. These disparities could be due to their levels of knowledge of food safety and also possibly as a result of the kind of food safety training courses received. This present study found that registered SCFHs were more likely to have good food safety knowledge likened to unregistered SCFHs which is in line with earlier research in Lebanon [ 51 ] but differs in the study done in Malaysia [ 62 ]. The potential explanation is that maybe before SCFHs have been given their certification of registration, they probably have been taken through food safety training courses which provide them with adequate knowledge of food safety and offer them a good understanding of food poisoning, contamination, and hygiene. This shows the importance of registering food handlers who have successfully been through food safety training courses to acquire knowledge on food safety.

This study showed that the odds of good hygiene practices were higher among SCFHs who had secondary education likened to those with no formal education which is in line with a study conducted in Ethiopia [ 12 ]. In contrast to our findings, other studies conducted in Ethiopia and Ghana found SCFHs with primary education as more likely to have good hygiene practices of food safety likened to secondary education [ 27 , 34 ]. The possible reasons are because most food preparation skills, personal hygiene, and cleanliness are learned from friends, relatives, parents, and media but not necessarily from formal education. However, a lower level of education reduces awareness but the higher one gets educated the better the knowledge which affects their attitude and eventually may reflect into hygiene practices. It implies that food handlers should be encouraged to attain at least basic education before engaging into the cooking business, although it serves as the first sources of income for most uneducated people in the societies. Nevertheless, a study conducted in Ghana showed that regardless of educational background, the food safety actions of SCFHs remain an issue in many nations [ 48 ].

The present study showed that SCFHs who earned average monthly income above GHc1500 were more likely to have good hygiene practices compared to respondents who earned less than Ghc500. Our finding confirms a study conducted in Ethiopia and Jordan that found good hygiene practice among food handlers with higher monthly income than those with lower higher monthly income [ 27 , 63 ]. The possible justification is that SCFHs with high monthly income can afford to purchase items needed to establish themselves in hygienic environments and afford more employees to help in cleaning and waste treatment which could result in a reduction in food poisoning and cross-contamination. This means the high monthly income of food handlers determine their ways of hygiene practices, purchasing more cooking utensils for preparing different meals and managing their leftovers foods to prevent contamination.

The present study showed that registered SCFHs were in favour of good hygiene practices of food safety than the unregistered. The likely description is because of the food safety training courses they received before being registered as food handlers which provides them with an in-depth and comprehensive understanding of hygiene practices such as proper handling of food, personal cleanliness, and sanitation while preparing food. However, there is no research found relating registration of food handlers with hygiene practice scores; hence, the lack of the associated literature offers difficulties to compare our finding to collective results reasonably with concrete answered questions. Nonetheless, our finding shows the importance of registering food handlers after they have been through food safety training courses to encourage them to practise good hygiene.

This study found that SCFHs who have completed training courses on food safety were in favour of good hygiene practices of food safety likened to respondents who had not. Our finding asserts with previous studies done in Ethiopia, Malaysia, and Ghana [ 36 , 38 , 47 ]. The probable justification is that SCFHs who have completed food safety training courses had gained the talents and awareness necessary to handle food safely and sustain great ethics of self-cleanness and hygiene practices. Our finding affirms the assertion that training upsurges understanding of food safety which might reflect into hygiene practices [ 48 ]. Hence, a lack of or inadequate training of SCFHs on food safety may inadvertently result in poor hygiene practices, thereby encouraging food contamination [ 26 , 36 ]. This implies providing food safety training to food handles is important to keep consumers from food poisoning and other wellbeing dangers that could arise from eating unsafe food.

In this present study, it is significant to highpoint SCFHs’ knowledge, attitudes, and hygiene practices are unpredictable from the study conceded, though most of SCFHs properly responded by answering appropriately to related questions of WHO’s Five Keys to Safe Foods guidelines for food handlers. This theoretic-based assessment of the KAP method applied to assessed food handlers’ food safety KAP has some limitations. Firstly, the postulation that the received knowledge on food safety is translated into attitude is not entirely true. The existence of a social desirability bias could similarly have added to the discrepancy amid interview-responded KAP of SCFHs. Social desirability bias is the propensity of SCFHs to provide publically anticipated answers which will be regarded approvingly by people [ 64 ]. This proclivity has been shown by their descriptions and overrating socially anticipated KAP questions on food safety. Secondly, as we beforehand mentioned, the research assistants revealed their identities and the purpose of the study to the SCFHs; therefore, the SCFHs were mindful of the hygiene practices and the significance of observing them, but they remained keen to acknowledge their nonconformity and these could likely affect the self-reported hygiene practices. Thirdly, the unavailability of sufficient data from related studies in the district impedes an evaluative comparison of our findings to determine an improvement of food safety KAP among SCFHs; therefore, our findings ought to be interpreted with caution. However, due to the representative nature of the sample assessed, the findings of this study can be generalized to other SCFHs in the district. After all, it makes a substantial impact concerning food safety KAP in North Dayi District because it is the first study conducted in the district that presents an imperative foundation for design to increase food safety and hygiene practice in the district, region, and beyond.

Over half of the respondents had good levels of KAP of food safety. This study found a significant relationship in the knowledge and hygiene practice scores of food safety with SCFH registration. This shows the importance of strict enforcement of registration and certification of SCFHs by regulatory agencies as a means of protecting the consuming public. Therefore, the government agency through FDA should intensify the vitality of undertaking food safety training on WHO’s Five Keys to Safer Food by food handlers before being registered. Furthermore, the District Health Directorate should properly and effectively supervise food handlers engaging in cooking businesses to ensure they transmit the link between knowledge with the attitude of food safety into hygiene practice. Further studies should assess the kind of food safety training modules received and their impacts on the KAP of WHO’s Five Keys to Safer Foods as well as evaluating their hygiene practices with observational checklists.

Availability of data and materials

The datasets generated during and/or analyzed during the current study are not publicly available due to ethical consideration but are available from the corresponding author on reasonable request.

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Lawrence Sena Tuglo, Zhongqin Pan & Minjie Chu

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Tuglo, L.S., Agordoh, P.D., Tekpor, D. et al. Food safety knowledge, attitude, and hygiene practices of street-cooked food handlers in North Dayi District, Ghana. Environ Health Prev Med 26 , 54 (2021). https://doi.org/10.1186/s12199-021-00975-9

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Good Manufacturing Practices for the 21st Century for Food Processing (2004 Study) Section 2: Literature Review of Common Food Safety Problems and Applicable Controls

August 9, 2004

Table of Contents

This section presents ERG's literature review of preventive controls for microbiological, chemical, and physical food safety problems in the food processing industry. Microbiological safety hazards cause most of the foodborne illnesses and include pathogenic bacteria, viruses, and parasites. Historically, pathogenic bacteria have been the most prevalent food safety hazard, with viral cases following closely behind according to the most recent CDC report on the etiology of foodborne illness (CDC, 2004). Chemical food safety hazards vary widely, but the most common problems cited in the literature include contamination with pesticides, allergens, and natural toxins, including scrombotoxins found in fish and mycotoxins found in crops. Foreign objects, or physical safety hazards, are the least likely to affect large numbers of people and usually are easily recognized.

Many of the microbiological food safety problems discussed in the literature can potentially be addressed by good manufacturing practices (GMPs) codified in 21 CFR 110, such as proper employee hygiene, adequate training, and effective cleaning and sanitizing of the manufacturing equipment and environment. For example, niche environments, which are sites within the manufacturing environment that can harbor bacteria, are a significant cause of post-processing contamination but difficult to reach with average cleaning and sanitizing procedures. Food plants that put in a greater than average effort must identify and eliminate niches by taking apart equipment in order to minimize the risk of post-processing contamination from niche environments. Others take an even more stringent approach by applying a post-package pasteurization method, virtually eliminating the risk of post-processing contamination due to niche environments.

Many chemical food safety problems are also addressed by following good manufacturing practices, such as pest control and proper storage. The rigor of the controls in place varies by plant, however. Further, some food safety problems, such as allergen control, may be better addressed by a Hazard Analysis and Critical Control Point (HACCP) plan in addition to GMPs. Physical hazards may also be better controlled by a HACCP plan. Controls may include foreign body detection systems, such as metal detectors, in addition to putting preventive measures in place.

Table 2-1 summarizes the range of problems associated with each type of hazard as identified in the literature. The following three sections provide a more detailed overview of each hazard and the preventive controls to address each problem, as noted in the literature. Each section also includes a summary flowchart that highlights the potential problems, the relevant CFR section or guidance that addresses each problem, the industry/product covered, and the types of preventive controls typically recommended to eliminate or minimize the type of food safety hazard risk posed. Finally, Section 2.4 discusses other issues to consider when evaluating food safety controls, in addition to GMPs.

2.1 Microbiological Safety

The microbiological safety hazards include pathogenic bacteria, viruses, and parasites. Some of the problems that lead to the contamination of food with these microorganisms at the processor level can be easily remedied with improved employee training programs and effective hygienic practices. Others are more difficult to control, such as post-processing contamination with Listeria monocytogenes , a pathogen that is ubiquitous in the processing environment.

Inefficient hygienic practices among employees . Employee hygiene is paramount to plant sanitation and is one of the leading causes of food contamination (Higgins, 2002). One of the challenges that food processors have to overcome is how to motivate employees to comply with hygienic practices. Training is one step in the process, but is often not enough to ensure employee compliance. Companies have adopted several aids to ensure employee compliance. For example, Atlanta's Buckhead Beef Company requires workers to key in their Social Security Numbers to activate the hand sanitizer dispensers on the plant floor. The company then uses the collected data to impose financial reprisals on employees found to be deficient in hand-sanitizing practices. Other controls include a sensor-equipped towel that prevents the cross-contamination that can occur with hand cranks. These units also count the number of towels dispensed. A signal dispenser that beeps when users have washed their hands sufficiently is also available to ensure adequate hand-washing time.

Language barriers . Current training programs, even those that include Spanish signage and instructional manuals, can be inadequate if the first language of plant employees is one other than English or Spanish. Even Spanish training materials can be problematic due to dialectical differences in translations. Some industry experts therefore recommend a picture-and-symbol approach to training to overcome language barriers (Higgins, 2002).

Table 2-1. Range of Processor-Level Problems by Type of Food Safety Hazard Posed

Ineffective training of employees . Although effective training is crucial to ensuring that sanitation standards are met, it is not clear that current training methods are sufficient. In the third Annual Best Manufacturing Practices Survey conducted by the Food Engineering magazine in 2002, a panel of food manufacturing professionals rated employee training as the lowest among all food safety measures in terms of effectiveness (Gregerson, 2002). Employee training that companies conduct may be too generic. For example, external consultants may not be familiar enough with a plant's operations and requirements to give effective advice. Other impediments to effective training might include training the wrong people, not training enough people, or not providing enough training (Blackburn and McClure, 2002).

Biofilms . Biofilms occur when bacteria form a slime layer upon a surface and provide an environment for pathogens to proliferate. The adhesion of pathogenic bacteria to a biofilm is a food safety hazard because the biofilm can detach and become a significant source of food contamination. Cleaning to remove biofilms prior to sanitation is often sufficient to prevent this problem. However, studies have shown that attached bacteria may survive conventional cleaning methods (Austin and Berferon, as cited in Stopforth et al, 2002). Adequate cleaning prior to sanitizing is therefore paramount to controlling this problem. Further, coating drains and equipment parts with antimicrobial material can counteract biofilms although it does not eliminate the need for proper cleaning and sanitizing (Higgins, 2003).

Niche environments . Niche environments are sites within the manufacturing environment where bacteria can get established, multiply, and contaminate the food processed. These sites may be impossible to reach and clean with normal cleaning and sanitizing procedures. Examples include hollow rollers on conveyors, cracked tubular support rods, the space between close-fitting metal-to-metal or metal-to-plastic parts, worn or cracked rubber seals around doors, and on-off valves and switches (Tompkin, 2002). Tompkin (2002) provides an extensive list of potential niches. Manufacturers must identify and eliminate niches. Microbiological sampling of the environment and equipment can detect a niche. Third-party validation of test results might be useful to further establish confidence in environmental sampling results. Further, sanitary equipment design can help prevent niches (AMI, 2003). Proper maintenance to keep equipment parts from providing potential niches is also essential.

Plant renovations . Outbreaks of listeriosis have been linked to environmental contamination of food caused by plant renovations (FDA/CFSAN, 2001a). While no data were identified in the literature on this issue, plant renovations are likely to require revisions in standard operating procedures (SOPs) to prevent contamination due to changes in processes.

Ineffective use of cleaning agents and disinfectants . Different cleaning agents vary in their ability to remove different soil types (Blackburn and McClure, 2002). Thus, the correct choice of cleaning agent is essential to ensure effective cleaning in a food processing facility. The efficacy of disinfectants is dependent on microbial species, pH, presence of biofilms, temperature, concentration, and contact time (Stopforth et al., 2002; Blackburn and McClure, 2002). Stopforth et al. (2002) found that commonly used disinfectants were not as effective as desired, possibly due to inadequate pre-cleaning steps. While there were no examples in the literature of plants having problems with this issue, the potential for ineffective sanitation is clearly present. Food manufacturers should always confirm the efficacy of their cleaning and disinfection programs with tests from the supplying companies or in-house trials (Blackburn and McClure, 2002).

Lack of sanitary equipment design . Good hygienic design of equipment prevents or minimizes microbiological contamination of food. The materials used for food processing equipment should be easily cleanable. As noted earlier, niche environments are known sources of pathogens; surfaces also deteriorate with age, and this abrasion makes cleaning more difficult (Blackburn and McClure, 2002). For cleaning and sanitation to be effective, all parts of the equipment should be readily accessible. Another way to improve equipment hygiene is to use antimicrobial coatings on equipment parts (Higgins, 2003).

Reactive rather than routine/predictive maintenance . In the Best Manufacturing Practices Survey conducted by Food Engineering magazine in 2001, 56 percent of respondents reported having routine preventive programs (Gregerson, 2002). Only 8.5 percent of respondents noted having predictive maintenance programs; the remaining respondents described their programs as reactive in nature, i.e., "run it 'til it breaks." Reactive maintenance can result in food contamination before a failure is identified. Niches can develop or controls can become defective in processing equipment that is not routinely maintained. For example, in 1994, a Listeria monocytogenes outbreak was linked to the use of defective processing equipment in the production of chocolate milk (FDA/CFSAN, 2001a).

Ineffective application of sanitation principles . It may be difficult for a food processor to apply sanitation principles consistently and effectively to each batch of product. Food processors have found that improving the effectiveness of sanitation principles is dependent on using redundant processing controls (FDA/CFSAN, 1999c). Validation of cleaning processes may also be necessary. Automation that makes it unnecessary for humans to conduct the cleaning, such as robotic spray washers, may also improve sanitation. The extent to which these practices are used in the industry is unclear and should be explored with industry experts.

Internalization of pathogens in fruit . Fruit is usually contaminated by direct or indirect contact with animal feces. Studies have shown that pathogens can infiltrate fruit through damaged or decayed areas or through the flower end of the fruit (FDA/CFSAN, 1999a; FDA/CFSAN, 1999b; FDA/CFSAN, 1999c). While employing best control practices--such as not using dropped fruit, removing damaged fruit, and washing/brushing fruit prior to processing--minimizes these risks, the problem can only be controlled with some certainty by a kill step, such as pasteurization. Other possible controls are listed in the FDA Report of 1997 Inspections of Fresh, Unpasteurized Apple Cider Manufacturers and listed again in the annotated bibliography.

Contamination of raw materials . Many pathogens, like E. coli and Salmonella, enter the food processing environment via raw materials contaminated with those pathogens. A number of studies have shown that methods currently in place to prevent this are not sufficient (FDA/CFSAN, 1999a;

FDA/CFSAN, 1999b; FDA/CFSAN, 1999c; Riordan et al., 2001; Tilden et al., 2002). Raw material contamination can affect any industry, but is more common in industries that use animal-derived products or products at risk of cross-contamination by animal feces. There are numerous preventive controls available to address the hazard. Some controls minimize the risks of raw material contamination (i.e., ensuring that raw material suppliers comply with good agricultural practices) and others (i.e., irradiation, pasteurization) involve a kill-step to eliminate any pathogens.

Post-processing contamination . Products can also be contaminated if the post-processing environment, utensils, or equipment have been contaminated with a pathogen. This issue is especially relevant to the pathogen Listeria monocytogenes , due to its hardiness and pervasiveness in the environment. Effective controls against post-process contamination include eliminating the pathogen from the post-processing environment by using environmental sampling to eliminate niches, effective sanitation, and various in-package pasteurization methods. Use of preservatives, such as nisin, to slow down the growth of Listeria monocytogene are also becoming more common.

Figure 2-1: Microbiological Safety Problems, Related CFR Section or Guidance, Industries Affected, and Sample Preventive Controls Suggested

2.2 Chemical Safety

Chemical safety hazards include intentionally added chemicals (e.g., allergens), unintentionally added chemicals (e.g., cleaners and solvents), and natural toxins (e.g., mycotoxins). Chemicals can also contaminate food through corrosion of metal processing equipment/utensils and residues of cleaning chemicals left on processing equipment. Further, adding too much of an approved ingredient, such as a vitamin in vitamin-fortified products, may compromise the safety of foods.

Raw material contamination with pesticides . FDA has found that roughly 1 percent of sampled domestic produce has pesticide residue in violation of EPA standards (FDA/CFSAN, 2002). While the incidence of contamination is low, consumers remain concerned about pesticide residues. Aside from washing and testing the produce, manufacturers can select produce from organic suppliers to avoid raw material contaminated with pesticides. Other alternative farming systems, such as low-input sustainable agriculture (LISA) and integrated pest management, are also control options at the farm level (Moulton, 1992). These systems, which use much less pesticide than conventional agricultural systems, rely on biological, chemical, cultural, and physical principles and tools to control pests throughout the farming operation. Other preventive control options may include genetic engineering with resistance against pests or developing safer chemicals (Moulton, 1992).

Indiscriminate spraying of facilities against pests. Chemicals can contaminate food if pesticides against insects and rodents are used indiscriminately in a processing facility. Therefore, food experts generally recommend that pest control be performed only by professionals to avoid residues in food (Folks, 2001).

Mistaken identity of pesticides . Food can become contaminated with pesticides if pesticide container labels are misread or when products are stored in containers that have had another use. The best way to control the risk of mistaken identity is to store pesticides away from food ingredients, keep an inventory of pesticides, and store the products in their original containers (Tybor, 1990; Folks, 2001; Bryan, 1997).

Spillage of pesticides or other chemicals . Pesticides should be handled like poisons to avoid potential spillage. Storing chemicals away from food and packaging materials will minimize accidental spillage of pesticides and other chemicals (Tybor, 1990). Further, processors should only use food-grade lubricants and greases in manufacturing.

Corrosion of metal containers/equipment/utensils . Metal poisoning can occur when heavy metals leach into food from equipment, containers, or utensils. When highly acidic foods (e.g., citrus fruits, fruit drinks, fruit pie fillings, tomato products, sauerkraut, or carbonated beverages) come into contact with potentially corrosive materials, the metals can leach into the food (Tybor, 1990). One solution to the problem is to use appropriate, non-corrosive materials in food processing.

Residue from cleaning and sanitizing . If equipment and other food handling materials are not rinsed well, then residue from detergents, cleaning compounds, drain cleaners, polishers, and sanitizers can contaminate a food product. This problem can best be controlled by properly training personnel about cleaning and sanitizing (Folks, 2001; Tybor, 1990).

Accidentally adding too much of an approved ingredient . Some substances, such as preservatives, nutritional additives, color additives, and flavor enhancers, are intentionally added to food products. But adding an approved ingredient in inordinate amounts by accident--such as adding too much nitrite to cured meat--can result in a toxic product (Bryan et al., 1997). Thus, Tybor (1990) recommends that nitrite be stored in a locked cabinet and weighed and bagged separately before being added to any product. Nutritional safety issues can also arise when product labels' nutrition information is incorrect. Thus, it can be dangerous to public health when too little or too much of a specified nutrient is added. For example, malnutrition can occur if infant formula does not deliver the expected nutrient content during its shelf life. Due to the risk involved, infant formula quality control procedures and labeling requirements are addressed outside of GMPs in 21 CFR 106 and 107, respectively. There are also many examples of nutritional food safety issues arising when too much of a nutrient gets added to a product unintentionally. For example, some vitamins that are added to fortified foods (such as Vitamin A) are known to be toxic at high doses. And iron, a necessary dietary component, can cause severe illness and death if too much is ingested. Controlling chemicals by keeping an inventory of additives minimizes the occurrence of this type of contamination (Folks, 2001).

Natural toxins . Food can be contaminated with naturally occurring chemicals that cause disease. Toxins such as mycotoxins (discussed further below) and marine toxins are naturally produced under certain conditions. Given that these toxins generally occur in raw materials, especially crops and seafood, manufacturers should require suppliers to certify hat the products they purchase are free from natural toxins.

Cross-contamination with allergens on production lines . A product can become cross- contaminated with allergens on the production line. To minimize the risk of cross-contamination, equipment must be cleaned and sanitized to remove all traces of allergens when the next run includes product that should not contain allergens (Minnesota Department of Agriculture, 2003). Wash-down techniques may need adjustment to ensure that they remove allergens as well as pathogens (Higgins, 2000). Rinsing with water only or only cleaning at the end of the day is not adequate (FDA/CFSAN, 2001a). Some equipment may need to be disassembled to be cleaned. The cleaning process should be verified by visual inspection. Enzyme-linked immunosorbent assay (ELISA) tests can also help verify cleaning procedures (Deibel et al., 1997; Morris, 2002). Manufacturers may choose to physically separate lines for allergen- and nonallergen-containing products (Morris, 2002). This may be too costly for most plants; scheduling longer production runs to minimize changeovers, with allergen-containing product runs scheduled at the end of the day, may be a more suitable alternative (Deibel et al., 1997; FDA/CFSAN, 2001b; Floyd, 2000; Gregerson, 2003; Minnesota Department of Agriculture, 2003; Morris, 2002). Crossover points on production lines, including conveyor belts that transport products, should be enclosed to prevent cross-contamination. Physical detachments and lockouts can be used for equipment common to allergen- and nonallergen-containing foods (Deibel et al., 1997). Maintenance tools should be color-coded to prevent cross-contamination (FDA/CFSAN, 2001b; Morris, 2002). Allergenic materials should be stored separately from nonallergenic materials, with dedicated utensils and containers. Putting all of the ingredients for a specific batch on a pallet before taking them to the processing area, or "staging," will also minimize the risk of cross-contamination. Line clearance, such as removing all the ingredients from the production area and checking for cleanliness, can also help prevent cross-contamination (Floyd, 2000). Product can also be tested for the presence of allergens, although this does not appear to be a common industry practice (FDA/CFSAN, 2001a). Finally, allergens should be evaluated as part of a hazard analysis, and a HACCP plan or similar approach can be taken to identify process areas that are at high risk for contamination with allergens (Morris, 2002).

Raw material contamination with allergens . When controlling a production process for allergens, manufacturers must maintain a close working relationship with suppliers of raw materials. The ingredient specification should provide assurance that the product is allergen free (Deibel et al., 1997; FDA/CFSAN, 2001c). Manufacturers should also obtain full ingredient lists from their suppliers (Deibel et al., 1997; Gregerson, 2003). Reconditioned ingredients and oils should not be purchased (Minnesota Department of Agriculture, 2003). The manufacturer should also audit suppliers each year to determine other products that are run on the same production line, whether any allergenic processing aids or rework have been used in the product, and whether any contamination from other common equipment could have occurred (Gregerson, 2003). A training program may be necessary to educate suppliers about allergen control, especially if suppliers have not implemented an allergen control plan (Deibel et al., 1997, Minnesota Department of Agriculture, 2003).

Contamination with allergens by utilization of rework . Proper use of rework is essential to prevent contamination of product with allergens. A documented rework plan should be available. Rework areas, equipment, and containers must be clearly identified and documented, as well as the rework itself (Deibel et al., 1997; Gregerson, 2003). This can be done through the use of color tags, plastic liners, or bar coding.

Not declaring an allergen on labeling . Unavoidable product contamination with allergens may occur if it is impossible to verify that all residue has been removed from a line or if other controls cannot be put in place (Floyd, 2000). A good manufacturing practice includes reviewing the labeling to ensure that the allergen is declared. However, a study of inspections conducted by FDA/ CFSAN (2001a) indicated that many firms do not have label review policies. Further, a large percentage of these manufacturers had undeclared allergens in their products. Controls to prevent this problem can include removing old label and packaging inventories from plants, verifying labels by scanning bar codes, and conducting label audits (FDA/CFSAN, 2001b; FDA/CFSAN, 2001c; Minnesota Department of Agriculture, 2003).

Older equipment . Effective cleaning is paramount to controlling allergen contamination. Older equipment, however, may not be designed to verify cleaning with a visual inspection (Deibel et al., 1997). As noted in the section on microbiological issues and controls, all parts of the equipment should be readily accessible and visible for cleaning and sanitation to be effective. Further, equipment surfaces should not harbor allergens. Gregerson (2003) reports one such case in which cross-contamination with allergens occurred due to the surface nicks on the processing table. Thus, sanitary equipment design is necessary to ensure proper removal of allergens from equipment.

Infestation of mycotoxins due to drought . Toxigenic fungi, or mycotoxins, are found primarily in foods of plant origin, although they can also pass through the food chain in milk and meat. Drought can encourage the growth of mycotoxins in certain crops. For example, drought stress can cause aflatoxin, a type of mycotoxin, to grow in corn and treenuts (Moss, 2002). Drought can be minimized through adequate irrigation schedules (Park et al., 1999). Thermal and chemical treatments are also available for use on crop that is already affected by mycotoxins (Park et al., 1999). Thermal inactivation, however, is not effective on certain types of mycotoxins, such as aflatoxin. Chemical treatments, such as ammoniation and activated carbons and clays, are other possible controls (Boutrif, 1999; Horne et al., 1989; Park et al., 1999; Suttajit, 1989).

Infestation of mycotoxins due to damage . Insect damage is associated with high levels of mycotoxin infection, as is mechanical damage from harvesters (Boutrif, 1999; Moss, 2002; Park et al., 1999). Diseases, such as ear rot in corn, also cause damage that leaves the crop susceptible to mycotoxin infestation (Moss, 2002). Delayed harvesting can also make crops more susceptible to disease due to higher moisture levels (Park et al., 1999). Damage to the product, whether through insect feeding or mechanical harvesters, provides a potential entry point for the mold that produces the mycotoxin. Controls available include pest management to prevent insect damage, breeding cultivars that are resistant to pest damage, timely harvesting, hand picking or electronic sorting to remove damaged crops, and thermal or chemical treatment as noted above (Boutrif, 1999; Moss, 2002; Park et al., 1999; Suttajit, 1989). Possible biological control of insects and diseases in the field is also being investigated (Moss, 2002).

Infestation of mycotoxins due to moisture/heat during storage . Post-harvest storage that protects the product from heat and moisture is essential to prevent mycotoxin infestation (Boutrif, 1999). Grains should be dried as soon as feasible, and storage under modified atmospheric conditions is desirable (GASCA/CTA, 1997). Products should be dried rapidly to less than 10 percent moisture (Park et al., 1999). Products can also be sampled for mycotoxins during storage (Boutrif, 1999). Methods include visual inspection with black light, ELISA tests, and complex laboratory analysis using high-pressure liquid chromatography (Horne et al., 1989). While prevention with proper storage conditions is the best way to control mycotoxin infestation, thermal and chemical inactivation, as described earlier, can control any mycotoxins that do form under storage.

Patulin production in apples . Patulin is a mycotoxin that is produced by a number of molds associated with fruit spoilage (Bisessur et al., 2001). Control methods often used in the production of apple juice include using tree-picked apples, culling apples, washing apples, charcoal treatment, chemical preservation using sulfur dioxide, gamma radiation, fermentation, trimming of fungus-infected apples, and clarification methods (Bisessur et al., 2001; Jackson, et al., 2003).

Figure 2-2: Chemical Safety Problems, Related CFR Section or Guidance, Industries Affected, and Sample Preventive Controls Suggested

2.3 Physical Safety

Materials that do not belong in food, like glass or metal, cause physical safety hazards. A physical safety hazard is any extraneous object or foreign matter in food that can cause injury or illness in the person consuming the product (Folks, 2001). Rocks, metal, wood, and other objects are sometimes found in raw ingredients. Further, contamination can occur during transport, processing, and distribution of foods due to equipment failure, accidents, or negligence (Institute of Medicine/National Research Council, 1998). Separation equipment should be used to separate the foreign bodies from the product. Detection methods include metal detectors, x-ray machines, and optical systems (Wallin and Haycock, 1998).

Foreign matter in raw materials . Sources of foreign matter in raw materials can include nails from pallets and boxes, ingested metal from animals, harvesting machinery parts, elements from the field, veterinary instruments, caps, lids, closures, and more (Wallin and Haycock, 1998). Mechanical harvesters will often collect more than the product. Processors can include separation equipment, such as destoners, air cleaners, magnets, screens, sieves, traps, scalpers, and washers as part of their production lines. For example, grain processors use four screens to remove foreign materials (Stier, 2001). Foreign matter in raw materials can be controlled with raw material inspections and vendor certifications or guarantees from suppliers. X-ray technology is also available to examine incoming material (Folks, 2001).

Poorly maintained equipment and lines . Pieces of equipment can break off and enter food products during processing if equipment is poorly maintained. Routine or preventive maintenance and other periodic checks of equipment can minimize the risk from this safety issue. Risk is further minimized with the use of metal detectors and x-ray machinery. Proper calibration of equipment and minimizing contact between pieces of machinery is also helpful (Folks, 2001; Stier, 2001).

Lighting fixture/other glass breakage . Glass can be controlled by having a glass breakage policy, such as throwing away all food and containers within 10 feet of the incident (Stier, 2001). Light fixtures can be protected so that if they break, the glass does not spill out (Folks, 2001). Other controls include examining of empty glass containers visually or cleaning a container with water or compressed air and inverting the container to remove any shards. Capping equipment should be properly calibrated and lines should be monitored for evidence of glass breakage. X-ray technology can also be helpful in identifying glass pieces in food (Olson, 2002).

Human factors . Production line workers can be a major source of contamination. For example, jewelry can fall off or break, fingernails can break, and pens can fall into food. Jewelry removal is required under GMPs. If pens are metallic, a metal detector can detect them. Production workers' fingernails should be cut short and gloves should be worn under certain processing conditions.

Introduction of foreign matter during storage . Pests can enter products during storage, leaving remnants behind. Effective pest control is the solution. It can include preventive measures such as filling in all non-functional openings in a building; fully sealing doors, windows, and vents; protecting intake points with filters or grills; and protecting drains and other facility intakes and exits. Professional extermination is needed once pests have established. UV light traps can also be used, although they need to be designed to prevent further contamination from the tray that collects the insect remains (Wallin and Haycock, 1998).

Figure 2-3. Physical Safety Problems, Related CFR Section or Guidance, Industries Affected, and Sample Preventive Controls Suggested

2.4 Other Considerations

There is a wide range of issues related to the safety and wholesomeness of food in addition to GMPs. These should be considered in addition to the problems identified at the food processing level when evaluating the effectiveness of food GMPs. They include the following and are discussed in more detail below:

• New trends contributing to foodborne illness,
• Most common causes of foodborne illness,
• High-risk foods, and
• Role of market incentives

New trends contributing to foodborne illness . A number of recent trends contribute to the incidence of foodborne illness. For example, in recent years, there has been an increase in consumer purchases of ready-to-eat (RTE) foods, made popular by the busy lifestyles of people today. Many cases of foodborne illness are caused by RTE foods that were cross contaminated with pathogenic bacteria. Since RTE foods are generally not cooked prior to consumption, the likelihood of foodborne illness is high when these products are contaminated.

Another alerting trend is the increase in new and drug-resistant infectious foodborne agents since the GMPs were last revised. Listeria monocytogenes and Cryptosporidium are examples of newly recognized agents that has been of great concern in the last few years. Some pathogens have also shown antimicrobial resistance, such as Campylobacter jejuni and Salmonella typhimurium DT104. There is also evidence of well-known viruses, such as hepatitis A and Salmonella entertidis , appearing in new foods like produce (Institute of Medicine/National Research Council, 1998). The evolution of these new agents and new vehicles transmitting known pathogens makes prevention of food contamination a moving target for those in charge of ensuring food safety.

The aging population in the United States is another trend of concern: this group is at higher risk for developing illness from contaminated food. As the baby boomer generation enters their retirement years, one can expect this trend to become even more pronounced. These and other changes over time significantly increase the risk of contracting foodborne illness, necessitating a new look at food GMPs in light of these factors.

Most common causes of foodborne illness . Pathogenic bacteria are the most commonly reported agents of foodborne illness, closely followed by viruses (CDC, 2004). Further, most reported cases of foodborne illness are attributable to poor handling at the home or at retail food establishments rather than failures at the food processing level (CDC, 2000). It is not possible to determine (with certainty) the cause of foodborne illness in roughly 50 percent of all foodborne illness cases. Moreover, many foodborne illness cases go unreported.

High-risk foods . The level of risk to public health varies by type of food. Some food products, such as refrigerated RTE foods, have a higher risk of being contaminated by pathogenic bacteria (e.g., Listeria monocytogenes ) than others, such as frozen RTE products (NFPA, undated). Further, FDA/CFSAN (2001a) has also shown in their Listeria monocytogenes risk assessment that the level of risk varies for different types of RTE foods. Therefore, from a risk perspective, indiscriminate application and/or recommendation of controls and policies may unduly burden manufacturers as well as the FDA and in some cases lead to inadvertent outcomes. For example, under the current zero-tolerance policy of the Food Safety and Inspection Service (FSIS) for Listeria monocytogenes , when a plant's testing program detects Listeria monocytogenes on plant equipment, the plant is required to recall all product produced on that line during the period of contamination. FSIS may also obtain test data if a plant has a suspected problem with Listeria monocytogenes. While there is a consensus in the industry that aggressive environmental monitoring is essential to controlling Listeria monocytogenes, Tompkin (2002) argues that the zero-tolerance policy discourages, rather than encourages, the RTE food industry from confirming the presence of Listeria monocytogenes in their environmental sampling programs. Many companies may conduct less (rather than more) aggressive environmental monitoring and product testing to avoid regulatory conflict.

Role of market incentives . FSIS is required to inspect meat and poultry slaughtering and processing plants carcass by carcass. As a result of the continuous inspection requirements, FSIS's inspection budget is four times that of FDA (Institute of Medicine/National Research Council, 1998). The lack of inspection resources may contribute to less enforcement of food safety statutes under FDA's jurisdiction. Given the lack of resources, it is important to evaluate the role of other, non-regulatory incentives that encourage food safety. For example, food safety problems can be a major liability for manufacturers of brand name products. If food is said to be unsafe, these manufacturers can face a huge public relations crisis that will negatively affect their bottom line (Ballenger and Ollinger, 2003). Consumers may also shun an entire category of food (Institute of Medicine/National Research Council, 1998). Most producers of branded products, therefore, invest more to ensure the safety of the food they produce. Grocery stores and wholesalers also require strict food safety controls from their suppliers to protect their reputations. For example, USDA's Economic Research Service (ERS) researchers recently surveyed 1,000 slaughtering plants and found that contractual agreements covering food safety standards result in higher levels of food safety with regards to equipment, testing, dehiding, sanitation, and operating procedures (Ballenger and Ollinger, 2003). A similar study for FDA-regulated products may yield comparable results.

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A scoping review protocol on food handlers' knowledge, attitude, and practices towards food hygiene and safety in low and middle-income countries

Affiliations.

• 1 Welcomgroup Graduate School of Hotel Administration (WGSHA), Manipal Academy of Higher Education, Manipal, Karnataka, India., India.
• 2 Public Health Evidence South Asia (PHESA), Department of Health Information, Prasanna School of Public Health (PSPH),, Manipal Academy of Higher Education, Manipal, Karnataka, India., India.
• PMID: 36176544
• PMCID: PMC9493400
• DOI: 10.12688/f1000research.122822.1

Background: Food safety and hygiene has emerged as the foremost cause of concern in recent time, especially post-pandemic and has changed the eating out behaviour of the consumers. Consumers often consider food safety and hygiene as one of the most prominent factors and hence it is important for food handlers to have adequate knowledge and the right attitude towards food safety and food hygiene. The review will summarise the evidence on food handlers' behaviours towards food safety and hygiene and associated factors that inhibit positive behaviour towards following food safety protocols and standards.

Methods: This scoping review protocol is guided by updated methodology from Joanna Briggs Institute (JBI). The search will be conducted on Medline (PubMed), Scopus and Web of Science. Google Scholar will be used to locate pertinent grey literature. A citation search will also be employed for identifying additional relevant studies. Quantitative and qualitative studies published from 2011- present will be included. Two reviewers will independently screen and extract the data. A third reviewer will be involved in resolving disagreements between reviewers. A two-stage screening including title/abstract and full-text will be conducted. Data extraction will be done using a pilot-tested data extraction form. The data extracted from included studies will be organised and presented using narrative synthesis. The review will also attempt to identify the unaddressed gaps in the literature with the available evidence.

Ethics and dissemination: An ethical clearance is not required for this scoping review as findings from existing published literature will be summarised. The review findings will be disseminated through conference presentations and journal publications.

Keywords: Attitude; Food Hygiene; Food Safety; Food handlers; KAP; Knowledge; Practices.

Copyright: © 2022 Dabral P et al.

• Developing Countries*
• Food Safety
• Health Knowledge, Attitudes, Practice*
• Review Literature as Topic

Associated data

• figshare/10.6084/m9.figshare.20055176.v1

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