research paper for food safety

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A Systematic Review and Meta-Analysis of the Effects of Food Safety and Hygiene Training on Food Handlers

Andrea insfran-rivarola.

1 Departamento de Ingeniería Industrial, Facultad de Ingeniería, Universidad Nacional de Asunción, Paraguay, San Lorenzo 2160, Paraguay; [email protected]

2 Facultad de Ingeniería, Arquitectura y Diseño–Universidad Autónoma de Baja California, Ensenada 22870, Mexico; xm.ude.cbau@adnaloy

Diego Tlapa

Jorge limon-romero, yolanda baez-lopez, marco miranda-ackerman.

3 Facultad de Ciencias Químicas e Ingeniería, Universidad Autónoma de Baja California, Tijuana 22390, Mexico; [email protected] (M.M.-A.); [email protected] (K.A.-S.)

Karina Arredondo-Soto

Sinue ontiveros.

4 Facultad de Ciencias de la Ingeniería, Administrativas y Sociales, Universidad Autónoma de Baja California, Tecate 21460, Mexico; [email protected]

Associated Data

Foodborne diseases are a significant cause of morbidity and mortality worldwide. Studies have shown that the knowledge, attitude, and practices of food handlers are important factors in preventing foodborne illness. The purpose of this research is to assess the effects of training interventions on knowledge, attitude, and practice on food safety and hygiene among food handlers at different stages of the food supply chain. To this end, we conducted a systematic review and meta-analysis with close adherence to the PRISMA guidelines. We searched for training interventions among food handlers in five databases. Randomized control trials (RCT), quasi-RCTs, controlled before–after, and nonrandomized designs, including pre–post studies, were analyzed to allow a more comprehensive assessment. The meta-analysis was conducted using the random-effects model to calculate the effect sizes (Hedges’s g) and 95% confidence interval (CI). Out of 1094 studies, 31 were included. Results showed an effect size of 1.24 (CI = 0.89–1.58) for knowledge, an attitude effect size of 0.28 (CI = 0.07–0.48), and an overall practice effect size of 0.65 (CI = 0.24–1.06). In addition, subgroups of self-reported practices and observed practices presented effect sizes of 0.80 (CI = 0.13–1.48) and 0.45 (CI = 0.15–0.76) respectively.

1. Introduction

Food safety is a global public health threat with frequent incidents of foodborne diseases. Additionally, the COVID-19 outbreak has put more pressure on global public health; particularly, organizations of producers and providers along the food supply chain are facing an ongoing challenge to improve and to extreme food safety and hygiene due to the pandemic. In this context, foodborne diseases are responsible for major economic costs for a country [ 1 , 2 ]. In terms of global estimates, in 2010, 31 foodborne hazards caused 420,000 deaths and 600 million foodborne illnesses derived from disease agents, such as non-typhoidal Salmonella enterica , Salmonella typhi , Taenia solium , hepatitis A, and aflatoxins, to name but a few [ 3 ]. In this regard, the application of the Hazard Analysis and Critical Control Point (HACCP) system can improve food safety; however its strength and success in preventing foodborne illnesses depend on it being applied correctly along with the provision of a sanitary infrastructure and the application of principles of good hygiene practice [ 4 ]. Current evidence suggests that a substantial number of foodborne illnesses occur through poor food handling practices of food workers [ 5 , 6 ]. Pathogens may appear in food, for instance, through unsafe farm practices, contamination during manufacturing, packaging, or distributing, or contamination in stores [ 7 , 8 ]. Additionally, food purchases from unsafe sources, inadequate cooking or reheating, holding food at room temperature, cross-contamination, poor personal hygiene, or improper food handling practices frequently contribute to foodborne illnesses [ 9 ].

To fight the battle against foodborne diseases, governments have resorted to strategies including food regulations and laws to monitor compliance with food safety standards [ 10 , 11 , 12 , 13 ]. Additionally, food companies rely on food safety methodologies, including the food Good Manufacturing Practices (GMP), the Good Agricultural Practices (GAP), the Hazard Analysis and Critical Control Points (HACCP) system, and the ISO 22000 standard to assure the safety of their food products [ 14 , 15 , 16 ]. In such methodologies, training food handlers in food safety is one of the most effective strategies for preventing foodborne diseases [ 17 ].

In an attempt to increase both knowledge and practice on food safety and hygiene, different behavioral theories have been used, including the Health Belief Model, in which an individual will perform a preventive behavior depending on their desire to avoid illness (or if ill, to get well) and the belief that a specific health action will prevent (or ameliorate) illness [ 18 , 19 ]; the KAP model, which assumes that an individual’s behavior or practice is dependent on their knowledge (K) and suggests that the mere provision of information will lead directly to a change in attitude (A) and, consequently, a change in behavior or practice (P) [ 20 ]; and the theory of planned behavior (TPB) which focuses on the individual’s intention to perform a given behavior and has been advocated by many researchers for the prediction of determinants of a food handler’s behavior [ 21 , 22 , 23 , 24 , 25 , 26 , 27 ].

In this regard, there is an implied assumption that such training leads to changes in behavior based on the KAP model [ 28 ]. In other words, training affects knowledge [ 29 ] and increased knowledge of correct food hygiene practices may be an important factor in changing behavior [ 22 ], i.e., the provision of food safety and hygiene training and the effective enactment of safe food handling practices are important for controlling foodborne illnesses [ 30 , 31 ]. Unfortunately, in most cases, food hygiene training does not translate into positive food handling behaviors [ 25 , 30 ].

In this regard, knowledge, attitude, and practice (KAP) surveys have been used widely. They are representative of a specific population to collect information on what is known, believed, and done in relation to a particular topic [ 32 ]. In this sense, several studies use training programs based on KAP as well as TPB with the aim of teaching food handlers how to identify food safety hazards and apply good practices regarding food safety.

Knowledge is accumulated through learning processes (which may involve formal or informal instruction), personal experience, and experiential sharing [ 33 , 34 , 35 ]. Traditionally, it has been assumed that knowledge is automatically translated into behavior [ 36 ], despite studies indicating that this is not necessarily true [ 37 , 38 ]. On the other hand, attitude involves evaluative concepts associated with the way people think, feel, and behave [ 39 ]. In the food industry, food handlers must gain knowledge of food safety and be aware of and implement proper food handling practices [ 40 ]. Practice refers to how people demonstrate their knowledge and attitude through their actions [ 41 ].

Previous studies have analyzed the training interventions and relationship between KAP (knowledge, attitude, and practice) and food safety in environments such as hospitals [ 42 , 43 , 44 ], colleges [ 45 , 46 , 47 ], food establishments [ 48 , 49 , 50 ], restaurants [ 51 , 52 , 53 ], and houses [ 54 , 55 , 56 ], among others. Despite the effort made [ 57 , 58 ], further evidence of the effects of training interventions on the knowledge, attitudes and practices toward food safety and hygiene of food handlers from different processes along the food supply chain is needed. To address this gap, we conducted a systematic review and meta-analysis of studies conducting training interventions among food handlers involved in different processes including on farms, in food processing facilities, and in restaurants (i.e., from farm to fork).

2. Materials and Methods

This study adhered closely to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [ 59 , 60 ]. Figure 1 presents a flowchart of the stages involved in the selection process, while the resulting PRISMA checklist summarizes all of the requirements covered (see online Supplementary Table S1 ). The review was registered in the PROSPERO International Prospective Register of Systematic Reviews (Identifier CRD42019119006).

The PRISMA flow chart.

2.1. Search Strategy

We conducted a comprehensive search on the following databases: PubMed, Cochrane Controlled Register of Trials (CENTRAL), Ebsco, Scopus, and Web of Science. Also, we searched for grey literature on Google Scholar and ProQuest. In relation to the search strategy, we relied on both the Peer Review of Electronic Search Strategies (PRESS) [ 61 ] and the PICOS (population, intervention, comparator, outcome, and study design) elements. The ultimate search strategy is described in the Supplementary Data S1 . We searched for publications in English published between January 1997 and December 2019. Likewise, we examined the reference lists of the retrieved articles to look for further relevant literature. The last search was run in April 2020.

2.2. Study Selection

Two authors reviewed the titles and abstracts of the work retrieved during the search. Discrepancies were resolved by discussion and consensus with a third author. All of the reviewed works were conducted among food handlers from different steps of the food supply chain, including farms, food processing facilities, and restaurants (i.e., from farm to fork). Interventions were defined as food safety and hygiene training sessions covering aspects such as personal hygiene, hand washing, cleaning and sanitization, cross-contamination, foodborne diseases, and temperature control. Training was given in the form of talks, demonstrations, self-practice, and different sources of communication, including posters, videos, booklets, slideshows, and fact sheets. We searched for randomized controlled trials (RCTs), quasi-RCTs, and controlled before-after (CBA) studies. In addition, we searched for non-randomized designs, including uncontrolled pre-post studies, to allow a more comprehensive and complete assessment of the available evidence in the area, recognizing that RCTs may not be feasible for many large-scale food safety education interventions [ 62 , 63 , 64 , 65 , 66 ].

The reported food safety training sessions were aligned with regulations, protocols, and guidelines, including, but not limited to, the United Nations’ (UN) Codex Alimentarius, the HACCP, the Food and Drug Administration (FDA) Food Code (including the hand-washing guidelines and protocol), the FDA’s Employee Health and Personal Hygiene Handbook, the United States Department of Agriculture (SDA) Food Safety Education campaign, the European Union General Food Law, Regulation (EC) No. 852/2004, the United Kingdom’s Safety Act, the GMPs, and the Good Hygiene Practices (GHPs). In all of the studies, the comparison group included either participants (i.e., food handlers) who did not receive food safety training or those who had not yet received proper food safety training.

As the main outcomes, all included studies evaluated changes in knowledge, attitude or practice among food handlers. Knowledge refers to the degree of understanding of food handlers about the food safety information given during training sessions. In contrast, attitude refers to a predisposition or tendency to respond positively or negatively to training. Finally, practices are the actions of an individual in response to the knowledge and attitude involved in the training sessions. Similarly, food safety practices can be defined as the increased use of evidence in healthcare practice and policy when both knowledge of, and attitude toward, food safety are present.

Changes in levels of knowledge were measured in the studies through survey-questionnaire data gathered in Likert-type scales with sub-dimensions such as food poisoning, cross-contamination, temperature control, and personal hygiene. Changes in self-reported attitudes toward food safety and hygiene were also measured through survey-questionnaire data on Likert-type scales. Finally, changes in practices were measured, such as self-reported practices and observed practices, the former through survey-questionnaire data in a Likert-type scale and the latter through checklists. Both used different sub-dimensions, including personal hygiene, food safety, and hygiene, temperature control, cross-contamination, sanitation, storage, and food display. We discarded any case report/series and/or review studies with data missing (e.g., sample size, mean, standard deviation), as well as studies conducted among people other than food handlers (e.g., consumers and food transporters).

2.3. Data Extraction and Quality Assessment

Two independent reviewers screened each potential article to identify its abstract, title, keywords, and concepts reflecting both the article’s contribution and the research context. Disagreements were overcome by discussion. Then, the relevant full-text studies were retrieved and independently assessed by two reviewers against the review’s inclusion/exclusion criteria. Once more, disagreements were overcome by discussion and consensus with a third author. The data were extracted by one reviewer and checked by a second reviewer. The extracted raw data from each study included authors’ names, year of publication, country of origin, title, study setting, study length, study aim, study design, study population, participant demographics, details on the training interventions and control conditions, recruitment and study completion rates, outcomes, measurement times, and information on the risk of bias. The data were arranged manually and tabulated using standardized forms including data from studies that fulfilled our requests for additional information.

2.4. Data Synthesis and Analysis

We stratified data into comparable subgroups for meta-analysis for each outcome: knowledge, attitude, and practice. Furthermore, we separated practice into two subgroups: self-reported practices and observed practices. As in similar cases [ 57 , 66 ], due to studies using different measurement instruments and scales, we calculated the Hedge’s g standardized mean differences (SMD) to measure the effect size, as proposed by Borenstein et al. [ 67 ]. Due to variation across studies, we conducted a random effect meta-analysis using Hedges’s g with a 95% confidence interval (CI) and the two-sided p -value for each outcome [ 67 , 68 ].

Heterogeneity among the studies in terms of effect measures was assessed using the I² statistic. This index can be interpreted as the percentage of total variability in a set of effect sizes due to true heterogeneity (between-studies variability) [ 69 ]. Higgins et al. 2003 suggested the use of I 2 values of 25%, 50%, and 75% as low, moderate, and high, respectively [ 70 ]. Thus, an I 2 value greater than 50% is indicative of substantial heterogeneity. We also assessed the evidence of risk of publication bias through a funnel plot and statistical tests, including Egger’s test [ 71 ] and the Begg’s test [ 72 ] (with a 95% confidence interval). We ran the meta-analysis in RStudio using the metafor package [ 73 ] and the meta package [ 74 ]. To reduce the risk of bias, two independent reviewers assessed each study. Randomized studies were assessed by using Cochrane’s tool RoB2 [ 75 , 76 ]. Here, the judgment criteria included 3 levels (low risk of bias, some concerns, or high risk of bias) for each of the 5 bias domains. Nonrandomized studies were assessed by using the ROBINS-I tool [ 77 ]; the judgment criteria included 5 levels (low, moderate, serious, critical, and no information) for each of the 7 bias domains [ 78 ]. The risk of bias visualization was done using robvis [ 79 ]. Finally, we summarized the findings reported in each study ( Table 1 ).

Summary of Findings.

Note. SD indicates standard deviation; RCT, Randomized control trials; CS, Cross-sectional studies; TL, training length; FU, follow up; GMP, good manufacturing practices; n , sample; nc , control group sample; ni , intervention group sample; mo., Months; h, Hours; min, Minutes. The last name of the main author and the publication year are shown.

During the initial search, we found 1094 papers. Then, after removing duplicates, our database was reduced to 321 papers. Following data screening and the application of exclusion criteria, we removed 200 more studies. One hundred twenty-one studies underwent full-text review. However, after applying the inclusion criteria, only 31 papers were eligible for inclusion in the literature review (see Figure 1 ). We classified the 31 final papers into three categories based on their main outcomes: changes in knowledge, attitude, and practices toward food safety and hygiene following training interventions. Twenty-six of the 31 studies reported changes in knowledge, 12 discussed changes in attitude, and 16 reported changes in food safety practices. Regarding the publication rate, we found that food safety and hygiene training interventions seem to have increased since 2011. Regarding the country of origin, most of the studies were published in the United States (29%), followed by Malaysia (13%), and Canada, Brazil, and the United Kingdom, with equal proportions (6.5%), see Supplementary Tables S2 and S3 . As for the research settings, the studies were conducted mainly in schools or universities (5/31), food process facilities (4/31), hospitals (4/31), restaurants (3/31), street food establishments or food trucks (3/31), farms/greenhouses (2/31), and multi-settings (2/31), among others.

Regarding the sample size, the studies varied from n = 10 to n = 194. There were 64 different interventions conducted among the 31 studies, with face-to-face/lectures (25/64) being the most frequent type of training intervention, followed by lectures combined with practice demonstrations (14/64), computer-based training (6/64), videos (4/64), videos combined with either a lecture (1/64) or a lecture and a demonstration (2/64), lectures combined with an incentive (1/64) or with demonstrations and incentives (2/64), and booklets (2/64), among others. We found that no studies used any kind of intervention involving social media. Regarding the type of study, eleven studies were pre-post studies, twelve relied on RCT, and eight performed a cross-sectional study with a trained group and a non-trained group. As for the measurement instruments, twelve studies administered surveys, one administered a test, two used checklists, and the rest did not report the used measurement instruments. Regarding gender, 13 papers reported that the majority of participants were female, while males represented the majority in nine studies, and one study had an equal proportion (50% of each). Eight studies did not report gender. The main outcomes, descriptions, statistics, and other relevant information of each study are summarized in Table 1 .

We performed a meta-analysis of the effects of food safety training interventions on the KAP of food handlers. Overall, we found that food safety training interventions had a significant effect on knowledge changes, with an SMD of 1.24 (CI = 0.89 to 1.58; p -value = 0.0001). In relation to attitude, our analysis results indicate that food safety training has a positive effect, giving an SMD of 0.28 (CI = 0.07 to 0.48; p -value = 0.008) for the attitudes of food handlers toward food safety and hygiene. Finally, with respect to practice, the overall effect size was estimated to be SMD = 0.65 (CI = 0.24 to 1.06; p -value = 0.0018). For those interventions with self-reported practices, we found an effect size of SMD = 0.80 (CI = 0.13 to 1.48; p -value = 0.0201). In contrast, for studies reporting observed practices, the effect size was SMD = 0.45 (CI = 0.15 to 0.76; p -value = 0.0035). Figure 2 , Figure 3 , Figure 4 , Figure 5 and Figure 6 show the forest plot for each outcome. Overall, food safety KAP was significantly higher as a result of training interventions. This phenomenon was particularly noticeable in the knowledge component. The forest plot in Figure 2 shows that most of the individual results lay close to 1. Such results strongly suggest that training increases knowledge of food safety and improves food safety attitudes and practices among food handlers.

Forest plot—Knowledge.

Forest plot—Attitude.

Forest plot—Overall practice.

Forest plot—Observed practice.

Forest plot—Self-reported practice.

We graphically assessed the risk of publication bias through funnel plots which, as the supplementary Figures S1–S5 depict, were symmetric. The null hypothesis for the Begg’s and Egger’s tests indicated an absence of bias in the selected studies. For knowledge, the Egger‘s test did not indicate any risk of publication bias, while the Begg’s test did indicate a moderate level of risk (i.e., Begg’s test: p -value = 0.044 and Egger’s test: p -value = 0.054); however, the data seem symmetric in the funnel plot (see Figure S1 ). As for the effects of food safety training on attitude changes, we also found no evidence of publication bias, both in tests and in the plot (Begg’s test: p -value = 0.653 and Egger’s test: p -value = 0.763). Finally, we found no statistical evidence of a risk of publication bias for the practice component (Begg’s test: p -value = 0.472 and Egger’s test: p -value = 0.608) and the graphic shows symmetry as well. In this review, the heterogeneity was considered high for knowledge (I 2 = 95.3%), attitude (I 2 = 77.7%), and for practice (I 2 = 94.9%). Regarding the risk of bias for randomized studies, six studies were evaluated with some concerns of risk of bias, four studies with low risk, and two studies with high risk. For nonrandomized studies, ten were evaluated with moderate risk of bias, nine studies with serious risk, and none as low risk. The visualization data are shown in Supplementary Tables S4 and S5 .

4. Discussion

This systematic review has summarized the effects of training interventions on the knowledge, attitudes, and practices of food handlers towards food safety and hygiene. Change in knowledge was assessed in 26 out of 31 studies; therefore, this was the most frequently reported outcome. This result is consistent with previous studies [ 58 , 107 ], and a significant amount of information is available, so it is probably easier to measure knowledge than attitude or practice. We found evidence that training interventions have a significant effect on increased knowledge toward food safety and hygiene across different type of settings such as fresh produce [ 91 ], food service operators [ 108 ], schools [ 80 ], restaurants [ 82 ], households [ 101 ], and multi-settings [ 97 ]. On the other hand, one study found no difference in knowledge between a control and an intervention group except for a positive attitude, so it can be considered to be optimistically biased [ 90 ]. This phenomenon has been demonstrated in previous research [ 90 , 109 , 110 ].

Attitude was assessed in 12 out of 31 studies, most of them assessing one intervention while some studies evaluated two [ 9 , 95 ] or three interventions [ 87 ]. Considering the summarized effect size, a SMD = 0.28 suggests a moderate effect for the positive attitude of food handlers; this is similar to previous studies [ 57 , 58 , 66 ]. Both studies [ 9 , 95 ] reported similar improvements in attitudes, either with face-to-face training or computer-based (CB) instruction. This is consistent with [ 84 ], who stated that participants learned equally well whether the instructional format was CB or instructor-led training. In addition, in studies where food handlers had attended food hygiene training previously [ 97 , 103 ], food safety attitude remained the same. According to our findings, most studies reporting an increase in knowledge also reported an increase in attitude [ 9 , 97 , 105 , 106 ]. However, an increase in knowledge might not necessarily bring about an improvement in attitude. This was the case for four studies [ 80 , 85 , 86 , 100 ]. The reason for this is unclear, yet some factors that could partially explain this could be length of the training [ 80 ], lack of repetition of the training [ 86 ], or previous hygiene enforcement program within the control group [ 85 ]. Attitude is a measure of the degree to which a person has a favorable or unfavorable evaluation of behavior [ 27 ]. In this regard, providing employees with training that does not promote a positive change with attitude [ 80 ], subjective norms, and perceptions of control may not contribute to improving intention (and ultimately behavior) to perform the behaviors [ 111 ].

Practice and behavior were measured in 16 studies, two of them assessing two outcomes (self-reported and observed practice) and the rest just one. The summarized effect of food safety training on practices showed that the interventions increased food safety practices, both for the 11 studies with self-reported practices and the seven studies with observed practices. Previous studies reported similar improvements, either self-reported or observed practices, but with a slightly smaller effect for the self-reported practices [ 38 , 97 ]; this consistent agreement between self-reported and observed behaviors was reported previously [ 23 ]. However, this is contrary to expected, since self-reported data are usually susceptible to social desirability bias [ 112 ], i.e., the tendency of respondents to give socially desirable responses in such a way as to be viewed favorably by others [ 113 ]. Thus, respondents tend to overestimate their food safety practices as being higher than their actual practices deserve [ 38 , 66 , 114 , 115 ]. On the other hand, observed practices could be affected by the “Hawthorne effect” where the changes in a person’s behavior may be due to the presence of an observer.

In this research, inconsistencies between self-reported and observed practices were detected by [ 106 ], with 95% being the self-reported rate of washing hands and 82.5% for keeping hair covered with a cap; however, the observations showed only 50% and 17.5% of compliance, respectively. For studies assessing practices thorough observations, evaluation was mainly done using a checklist [ 38 , 97 , 98 , 99 , 116 ].

The implementation of food safety and hygiene practices has the final objective of preventing foodborne illnesses. Food safety behaviors are often subdivided into specific behavioral constructs such as personal hygiene, adequate cooking of foods, avoiding cross-contamination, keeping foods at safe temperatures, and avoiding food from unsafe sources [ 117 ]. Behavior outcomes provide a more direct measure of intervention effectiveness compared to knowledge and attitudes [ 66 ]; however, food safety practices were measured in only 16 out of the 31 studies. This is consistent with the proportions reported by Viator et al. [ 107 ]. Moreover, an integrative review conducted by Zanin et al., [ 118 ] stated that 50% of the selected studies reported no translation of knowledge into attitudes/practices. In this review, we found evidence of close to 25% translation into both attitudes and practices. In addition, food safety practices of food handlers are associated with the type of management, i.e., tending to be higher in corporate-managed than owner-operated [ 31 ]. Incorporating practical assessment, such as observations, could help owner-operated organizations, since in some cases observation is more important than self-reported practices in order to represent actual behaviors [ 99 , 119 ].

4.1. Food Safety and Hygiene Training

Overall, all nine food safety training interventions that incorporated theory and practice (T&P) demonstrations were more effective in terms of knowledge gain than those that only incorporated theoretical training. This is consistent with [ 83 ], who found that training that incorporated active participation was more effective than traditional passive instruction. Nevertheless, those studies reporting T&P presented a poor improvement in attitude [ 85 , 86 ]. Finally, the seven and eleven interventions based on T&P and theory, respectively, showed similar practice improvement in 71% and 80% of the studies, respectively.

Although the ultimate goal is to prevent foodborne diseases, no study reported an impact on this goal. As expected, the results were based around the change in KAP as a mean to avoid food safety risk. Thus, theoretical training based on KAP is commonly used to improve handlers’ food safety performance [ 106 ]. However, some authors have reported flaws, mainly in the assumption that the received information is translated into practices and behaviors [ 100 , 103 ].

Food safety and hygiene are critical in all steps in the farm-to-fork chain. In an ideal scenario of the farm-to-fork continuum, a total absence of foodborne pathogens and opportunistic bacteria is obviously desired [ 120 ]. Nevertheless, despite good knowledge, attitude, and self-reported practices, there may be poor performance in hygiene [ 121 ] and food safety practices. Bacteria might exist in nature in a range of different metabolic stages, such as dormant, active, and growing; thus, it is important to detect bacteria and ascertain whether they are potentially active [ 120 ]. Despite the central role that food workers’ hands play in bacterial transfer among food and various surfaces [ 81 ], only one study assessed the number of bacteria growing on cultures obtained from the hands [ 86 ], while another demonstrated cross-contamination with hand hygiene sessions using GloGerm ® powder and UV light [ 91 ]. Both studies showed improved knowledge of food handlers. Similarly, it is well known that an effective way to control food poisoning is to maintain hygienic surroundings [ 103 ]. Thus, additional evaluations and inspections including surface cleanliness and hand cultures seem to be a suitable part of training [ 122 ]. Similarly, frequent practical and hands-on sessions will create a much more vivid experience for workers [ 83 , 89 , 91 ]. Active learning, e.g., a training session that raises awareness of the possibility that E. coli bacteria may accumulate under the fingernails should also demonstrate the correct handwashing procedure and require the learner to practice until he or she can successfully demonstrate effective performance of that procedure [ 85 ].

Also, risk perception acts as a guide for decisions about behavior and can be a barrier to following a particular activity or procedure or not [ 123 ]. In this regard, there are different approaches to food safety training. Some include cases of victims of food poisoning [ 91 ] during food safety training to connect with audiences’ lifestyles, incorporate fear, and enhance the perception of risk [ 58 ]. Moreover, to be effective, training programs should be based on appropriate adult education theory [ 124 ], the possibility of human error [ 125 ], and make sure that the reading comprehension level of the text is suitable for most food handlers [ 9 ]. Training programs that are more closely associated with a worksite are potentially more effective, especially if supported by practical reinforcement of the message [ 85 , 126 ].

The frequency [ 51 ] and length of exposure [ 127 ] for a training program are significative factors in the obtained outcome. For studies reporting the length of intervention, the majority were conducted in one day with a follow-up period between 2 and 8 weeks, with 1 year being the longest follow up period [ 82 ]. Moreover, because knowledge decreases over time [ 5 ], food safety and hygiene training should be provided frequently [ 51 ] to prevent the information from being forgotten and also to increase the level of knowledge [ 86 ]. Some studies suggest refresher retraining after 2 years [ 108 ] and before 5 years from initial certification [ 5 ]. For food establishments, we found that the educational level and professional training have significant effects on knowledge, practice [ 49 , 98 ], and food handlers’ positive attitudes [ 49 , 103 ]. However, the inclusion of adult education concepts, skill-based programs with interconnected sessions [ 85 ], and even the use of YouTube ® videos [ 91 ] can be effective for low literacy audiences. In this regard, farm employees with low educational attainment have also demonstrated significant knowledge gain [ 85 , 91 ].

Commitment and motivation from supervisors and management, as well as proper support and facilities given to staff are critical for the success of food safety and hygiene intervention. Training moves people in the right direction but not far enough [ 88 ]. In this regard, food handlers’ attitudes are significantly related to the management environment [ 31 ], thus supervisory support enforcement plays a significative role [ 85 ] in demonstrating and emphasizing the importance of following proper food safety practices [ 88 ], as well as being role models themselves [ 91 ]. Moreover, because transforming knowledge into behavior is complex, training from top management to all employees is crucial [ 128 ], inasmuch as successful food safety intervention must be based on firm theories [ 99 ]. Furthermore, additional key factors are the supervisors’ years of experience [ 5 ], clear responsibilities of food managers, and written agreement related to practicing sanitization procedures [ 99 ], as well as trained and certified managers helping to reduce critical food safety violations [ 129 ].

In terms of settings, most of the studies were carried out in restaurants and street food establishments, hospitals and schools, greenhouses and farms, and industrial food processing companies. This is in accordance with a previous study which found that the most frequently reported settings were restaurants and street food establishments [ 58 ]. In this context, the restaurant industry has been labeled as one of the most recurrent sources of foodborne illness outbreaks [ 130 ]. Therefore, food safety certification of kitchen managers appears to be a significant factor in outbreak prevention in restaurants [ 131 ]. A combination of inspection results with a mandatory training and certification program may mitigate food safety risks [ 132 ].

Many barriers and factors (environmental, social, cultural, belief systems, and so on) can affect whether food handlers effectively implement food safety practices in their workplaces [ 30 , 31 , 122 , 133 ], including a lack of adequate food safety training, time pressure, competing job tasks, lack of or inconvenient locations of equipment/resources, lack of managerial support, lack of motivation/incentive, lack of reminders, or lack of clarity in food safety messages [ 25 , 90 , 98 , 122 , 134 , 135 , 136 ]. As expected, studies from developing countries have experienced some fundamental barriers, including a lack of infrastructure, poor working conditions, ill-functioning equipment, a lack of water, and insufficient supervision [ 89 , 93 ]. Interestingly some studies from developed countries have experienced some limitations regarding literacy [ 94 ] and a potential language barrier [ 83 ], mainly because food handlers were not native speakers.

Regarding the training interventions among the selected studies, 27% were based on international guidelines (including WHO, HACCP, GMP, and ServSafe ® ), 18% on national guidelines, 18% on previous studies, and the remaining studies did not report this information. The guidelines vary by sector (restaurants, meat industry, dairy industry, etc.), legislation, or requirements of the country or region in which a company is located, market conditions, and certifications. Despite the frequent food-related incidents attaching great importance to the certification system [ 137 ], only 41% of the included studies awarded some national or international certification for food handlers. High costs could discourage companies from implementing certifications. In this sense, local governments should support organizations [ 137 ], mainly those that rarely invest in training or certification. A powerful way to win the interest of politicians and policy makers is to be able to attach a monetary value to food-related illness [ 138 ]. In this regard, the overall annual estimated cost of foodborne illness has remained relatively constant since 2005 at approximately GBP 1.5 billion in England and Wales and 152 billion USD in the USA [ 138 ]. Even though regulations and voluntary certifications are commonly thought of as driving forces to improve the safety and quality of food products [ 137 ], legislation might lead food handlers to undergo training only for certification without being motivated to acquire and use new knowledge [ 97 ]. A study found that the number of food safety violations did not differ as a function of certification [ 129 ]. Thus, certifications and legal requirements may not guarantee food safety [ 139 ].

4.2. Limitations

Our study has several major limitations. Firstly, differences in data (settings and data collection/processing approaches) and the multi-component nature of food safety and hygiene training makes it difficult to generalize the results. Second, most studies used observational pre–post designs. As a result, the absence of matched comparison groups, the potential presence of confounding variables, and the lack of randomization prevented the reported outcome improvements from being causally linked to the interventions. Third, the evaluation of KAP limited our ability to make conclusions about the behavior of the food handler. Fourth, knowledge, attitude, and practice are often subdivided into specific constructs; however, our ability to investigate these concepts in detail was limited by the availability and reporting of primary research, as many studies only reported overall scores or scales. Moreover, the determination of workers’ behavior using the self-reported technique before education was an important limitation in some included studies. Finally, there is a possibility that the “Hawthorne effect” led to the improvements reported in the studies.

5. Conclusions

Foodborne diseases continue to be a global problem, causing substantial morbidity and mortality and significant costs. According to our results, food safety and hygiene training have positive impacts on food handlers’ knowledge, attitude, and practice. Effective and frequent food safety training of food handlers continues to be an initial step in ensuring that food safety concepts are at least introduced. Despite knowledge being delivered by training, it cannot just be translated into desired changes in attitudes and practice. The inclusion of practical demonstration and continuous support might increase positive attitudes towards food safety and hygiene practices among food handlers with the ultimate goal of minimizing the incidence and prevalence of foodborne hazards. Moreover, effective food safety training should be relevant to the situation, promote active learning, increase risk perception, and consider the work environment. Because computer-based (CB) training was not found to differ from face-to-face training in terms of the outcome obtained, CB programs could be used more extensively, since they are an efficient and cost-effective way to educate staff.

In this regard, we identified several barriers to attaining proper food safety and hygiene practices, which should be considered by educators with appropriate adjustments according to the stage of the food supply chain, as well as the market, regional, and cultural characteristics. Similarly, training interventions should be based on international or national guidelines and adapted to different sectors, legislations, and certifications. Furthermore, local governments should support organizations, especially those that rarely invest in training and certification like SMEs, small farms, restaurants, or street food services. Finally, certifications and legal requirements may not guarantee food safety and hygiene, but when properly supported by resources, commitment, leadership, and a receptive management culture, food safety and hygiene practices may improve.

Acknowledgments

This study was supported by Mexico’s National Council of Science and Technology, the Programa para el Desarrollo Profesional Docente, para el Tipo Superior (PRODEP) Program and the Universidad Autónoma de Baja California.

Supplementary Materials

The following are available online at https://www.mdpi.com/2304-8158/9/9/1169/s1 , Table S1: PRISMA checklist, Data S1: Search strategy, Table S2: Geographical distribution of studies selected, Table S3: Distribution per year of studies selected, Figure S1: Funnel plot for knowledge, Figure S2: Funnel plot for attitude, Figure S3: Funnel plot for overall practice, Figure S4: Funnel plot for self-reported practice, Figure S5: Funnel plot for observed practice, Table S4: Risk of bias for randomized studies, and Table S5: Risk of bias for nonrandomized studies.

Author Contributions

Conceptualization, A.I.-R. and D.T.; methodology, D.T. and J.L.-R.; formal analysis, A.I.-R., D.T., J.L.-R., M.M.-A., and K.A.-S.; investigation, A.I.-R., D.T., Y.B.-L., and S.O.; writing—original draft preparation, A.I.-R., D.T., J.L.-R., and M.M.-A.; writing—review and editing, Y.B.-L., K.A.-S., and S.O.; supervision, D.T., Y.B.-L., K.A.-S., and S.O. All authors have read and agreed to the published version of the manuscript.

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

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Environment and food safety: a novel integrative review

• Review Article
• Published: 25 August 2021
• Volume 28 , pages 54511–54530, ( 2021 )

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• Shanxue Jiang 1 , 2 , 3 ,
• Fang Wang 1 , 2 , 3 ,
• Qirun Li 1 ,
• Haishu Sun 4 ,
• Huijiao Wang 5 &
• Zhiliang Yao   ORCID: orcid.org/0000-0001-5125-8245 1 , 2 , 3  

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Environment protection and food safety are two critical issues in the world. In this review, a novel approach which integrates statistical study and subjective discussion was adopted to review recent advances on environment and food safety. Firstly, a scientometric-based statistical study was conducted based on 4904 publications collected from the Web of Science Core Collection database. It was found that the research on environment and food safety was growing steadily from 2001 to 2020. Interestingly, the statistical analysis of most-cited papers, titles, abstracts, keywords, and research areas revealed that the research on environment and food safety was diverse and multidisciplinary. In addition to the scientometric study, strategies to protect environment and ensure food safety were critically discussed, followed by a discussion on the emerging research topics, including emerging contaminates (e.g., microplastics), rapid detection of contaminants (e.g., biosensors), and environment friendly food packaging materials (e.g., biodegradable polymers). Finally, current challenges and future research directions were proposed.

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Zahra Aghalari, Hans-Uwe Dahms & Mika Sillanpää

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Introduction

Environment and food safety have been two important topics in the world (Zhang et al. 2015 ; Bilal and Iqbal 2020 ; Liu et al. 2020b ; Song et al. 2020 ; Ye et al. 2020 ; Qin et al. 2021 ). Human activities have posed great threats on environment and food safety. For example, due to the intensive use of disposable masks which are mainly made of non-biodegradable polymers, massive amount of waste is produced. In fact, environment and food safety are closely intercorrelated (He et al. 2016 ; Sagbara et al. 2020 ). As shown in Figure 1 , on the one hand, food safety is strongly affected by environment (Lu et al. 2015 ). Contaminants from polluted soil, water, and air could migrate into crops, vegetables, fish, animals, and so on (Lu et al. 2015 ; Sun et al. 2017 ; Li et al. 2020a ). On the other hand, in order to ensure food safety and quality, various processing procedures are carried out, which increase the burden on the environment and even cause environmental pollution (Yao et al. 2020 ). For example, food processing industry produces a huge amount of wastewater (Li et al. 2019 ; Ahmad et al. 2020 ; Akansha et al. 2020 ; Boguniewicz-Zablocka et al. 2020 ). If the wastewater is discharged into rivers directly, the rivers will be polluted. As food industry wastewater typically contains high concentrations of organic matters, eutrophication can easily take place (Feng et al. 2021 ; Jiang et al. 2021 ). In addition, food packaging materials are widely used as food containers and to preserve food from decay (Vitale et al. 2018 ; Wohner et al. 2020 ; Zeng et al. 2021 ). When the food is consumed, a mass of packaging waste is produced, which will cause environmental problems if not disposed properly (Poyatos-Racionero et al. 2018 ; Bala et al. 2020 ; Brennan et al. 2020 ; Liu et al. 2020a ). However, plastics, as one of the most commonly used packaging materials, cannot be disposed easily and can exist in the environment for hundreds of years (Barnes 2019 ; Chen et al. 2021b ; Mulakkal et al. 2021 ; Patrício Silva et al. 2021 ).

Illustration of the relationship between environment and food safety and their impacts on human health

Environment and food safety have strong impacts on human health (Fung et al. 2018 ; Gallo et al. 2020 ). Many studies are conducted to investigate the migration of contaminants from the environment to food, and finally to human beings. For example, it is reported that heavy metals in the aquatic environment can migrate into fishes via bioaccumulation and bioconcentration (Baki et al. 2018 ; Korkmaz et al. 2019 ; Arisekar et al. 2020 ). When these polluted fishes are consumed, the heavy metals will migrate into human bodies (Saha et al. 2016 ; Gholamhosseini et al. 2021 ). Although the concentrations of heavy metals in the fishes are usually below the maximum allowed level (Velusamy et al. 2014 ; Safiur Rahman et al. 2019 ), the fact that humans are at the top of the food chain cannot be ignored. In other words, as there are various food sources for human beings, the heavy metals in our bodies could accumulate and finally reach a level that causes serious health risks, such as cancer (Badamasi et al. 2019 ; Yu et al. 2020a ). In addition to the common types of contaminants (e.g., heavy metals, pesticides, pathogen, particulate matter), there are also some emerging types of contaminants (e.g., microplastics, personal care products, pharmaceuticals), and more efforts are needed to study their effects on human health (Aghilinasrollahabadi et al. 2020 ; Li et al. 2020b ; Zhang et al. 2020 ).

Given the importance of environment and food safety, it is not surprising that a lot of related studies have been published, including many review studies. For example, Qin et al ( 2021 ) reviewed the effects of heavy metals in soil on food safety in China and discussed the sources (e.g., pesticides, fertilizers, vehicle emissions, coal combustion, sewage irrigation, mining) and remediation strategies (e.g., soil amendments, phytoremediation, foliar sprays). Suhani et al. (Suhani et al. 2021 ) reviewed the effects of cadmium pollution on food safety and human health with a focus on the mechanisms (e.g., cellular or molecular alterations). Deshwal et al. (Deshwal and Panjagari 2020 ) reviewed the effects of metal-based packaging materials on food safety and health issues (e.g., bisphenol A migration, metal migration, dissolution, blackening, and corrosion). Sun et al. (Sun et al. 2017 ) reviewed the relationship between air pollution and food security with a focus on the food system (e.g., the effect of agricultural policy on food security). However, most of these review studies only focus on certain subfields (Ayelign and De Saeger 2020 ; Endersen and Coffey 2020 ; Imathiu 2020 ; Nelis et al. 2020 ; Singh et al. 2020a ). In addition, most of these reviews are based solely on the subjective experiences of the researchers in the related fields. In the age of big data, it is necessary to give a timely update on the research of environment and food safety through objective data analysis. The scientometric-based statistical method provides a powerful tool to disclose research trends and progress on certain research areas through data analysis of published documents. However, although there are already quite a few scientometric studies on other research areas (Jiang et al. 2018 ; Li et al. 2018 ; Kamali et al. 2020 ; Khalaj et al. 2020 ; Zakka et al. 2021 ; Zeb et al. 2021 ; Ni et al. 2021 ), the scientometric studies on environment and food safety are very limited. Therefore, the aim of this study is to provide an integrative review on environment and food safety via objective statistical analysis coupled with subjective review on strategies to protect the environment and ensure food safety, followed by a discussion on emerging research topics.

A scientometric review

As shown in Figure 2 , during the past 20 years, there were nearly 5000 publications on the topic of environment and food safety (detailed method was provided in the Supplementary Information ). From 2001 to 2020, there was a steady increase in publications every year. Meanwhile, it was indicated that the increase in research output slowed down in 2020, possibly due to the terrible coronavirus pandemic which suspended researchers’ lab work. In terms of document types, the 4904 publications were categorized into 10 types, where research article, review, and proceedings paper were the top three, accounting for 73.23%, 16.54%, and 13.09% of the total publications, respectively (Supplementary Table 1 ). In terms of languages, most of the documents were published in English, accounting for 96.76% of the total publications (Supplementary Table 2 ). The following languages were German (0.67%), Chinese (0.57%), Portuguese (0.43%), Spanish (0.41%), French (0.39%), etc. The language analysis revealed that a SCIE journal is not necessarily an English journal. For example, among the journals included in the data, the SCIE journal Berliner und Munchener Tierarztliche Wochenschrift publishes research results in German, and the SCIE journal Progress in Chemistry publishes research results in Chinese. To be available to researchers from all over the world, an English version of the titles, keywords, and abstracts of these publications are also provided. However, as the main text is not written in English, the impact of these publications is usually limited to the local research community, i.e., the papers written in German is normally only read by German researchers while the papers written in Chinese is normally only read by Chinese researchers.

Number of publications per year and cumulative number of publications from 2001 to 2020

In terms of journals, about 165 journals published at least 5 papers, and the total papers published in these journals accounted to about half of the total publications (more details are provided in supplementary data ). Furthermore, as shown in Figure 3 , the total papers published in the top 20 most publishing journals accounted to about one-fourth of the total publications. These results revealed that the research on environment and food safety is of broad interest.

Number of publications and cumulative percentage of the top 20 most publishing journals

In terms of publishing countries/regions, more than 100 countries/regions contributed to these publications (more details are provided in supplementary data ). Especially, more than 50 countries/regions contributed at least 20 publications to the research on environment and food safety during the past 20 years. These results again revealed that the research on environment and food safety is of global interest. As shown in Figure 4 , in terms of research output, the USA and China were leading the research on environment and food safety. Specifically, among the countries/regions, the USA was undoubtedly the most publishing country, which accounted for nearly one-fourth of the total publications. The runner-up was China, which contributed to around 15% of the total publications. However, it does not mean that the USA and China have contributed to around 40% of the total publications because many papers are published as a result of collaborations among several countries.

Number of publications and corresponding percentage of the top 20 most publishing countries/regions

Generally, over 400 research institutes had contributed at least 5 publications to the research on environment and food safety, and nearly 50 research institutes published at least 20 papers during the past 20 years (more details are provided in supplementary data ). The top 20 most publishing research institutes were summarized in Table 1 . Chinese Academy of Sciences (CAS), which ranked the first place based on number of publications, is the largest cluster of research institutes in China. The research conducted by CAS is quite diverse and multidisciplinary. Especially, the research on environment and food safety is loosely conducted by different CAS research institutes, including but are not limited to Research Center for Eco-Environmental Sciences (RCEES), Institute of Urban Environment, and Institute of Soil Science. For example, researchers from RCEES found that water pollution and soil pollution had serious effect on food safety and human health (Lu et al. 2015 ). The next one, USDA ARS, short for United States Department of Agriculture Agricultural Research Service, is a leading research institute in the USA focusing on food safety and human health from the aspect of agriculture. Similarly, US FDA is short for United States Food and Drug Administration and is exclusively focusing on food and drug-related research so as to protect public health. INRA, short for French National Institute of Agronomic Research, is a very famous research institute in Europe focusing on agricultural research. Similarly, Istituto Superiore di Sanità is a leading research institute in Italy focusing on public health. In addition to the above 5 research institutes, the remaining 15 research institutes are all universities, and their research on environment and food safety is mainly conducted by the related departments or research centers of the universities. For examples, the Department of Food Technology, Food Safety and Health at Ghent University (located in Belgium) is renowned for its state-of-the-art research on food technology, food microbiology, food chemistry, food safety, etc. Similarly, Wageningen University (located in Netherlands) has a research institute named Wageningen Food Safety Research. Another two European universities were both from Denmark, namely University of Copenhagen and Technical University of Denmark. The Department of Food Science at University of Copenhagen and the National Food Institute at Technical University of Denmark are mainly responsible for food-related research. Besides, there were also two universities from China (i.e., China Agricultural University and Zhejiang University) and one university from Canada (i.e., University of Guelph). The remaining 8 universities all came from the USA, accounting for over half of the universities in the top 20 most publishing research institutes, which corresponded well with the above countries/regions analysis.

Table 2 summarized the top 20 most-cited articles on environment and food safety. As revealed by Table 2 , the research on environment and food safety is diverse, and there are quite a few research directions which received a lot of attention. Generally, the research topics disclosed by the most cited papers included food inspection/detection technique, heavy metal pollution, food additives, food packaging, food allergy, food pesticide, foodborne pathogen and diseases, microplastics, food processing, and production. Various food inspection/detection techniques have been reported, including electrochemical strategies to detect gallic acid in food (Badea et al. 2019 ), thermal imaging technique coupled with chemometrics (Mohd Ali et al. 2020 ), paper-based analysis device for rapid food safety detection (Qi et al. 2020 ), line-scan spatially offset Raman spectroscopy technique for subsurface inspection of food (Qin et al. 2017 ), surface-enhanced Raman spectroscopy for detection of mycotoxins in food (Wu et al. 2021b ), chromatography, and mass spectrometry (Pauk et al. 2021 ; Suman et al. 2021 ). In addition, heavy metal pollution has posed great threats on food safety, and a lot of studies are conducted, including the soil heavy metal pollution and food safety (Qin et al. 2021 ) and the impacts of various heavy metals (e.g., cadmium, lead, arsenic) on food safety and human health (Corguinha et al. 2015 ; Suhani et al. 2021 ). Furthermore, there are a variety of food additives used in different situations. For example, feed additives such as antibiotics have been used in animal nutrition; however, the use of antibiotics can cause antimicrobial resistance which can further increase the morbidity and mortality of diseases (Silveira et al. 2021 ). Therefore, as will be discussed below, laws and regulations are needed to strictly control the use of food additives. Furthermore, foodborne pathogen also has strong impacts on food safety. As an effective way to kill or inhibit foodborne pathogen, antimicrobial food packaging is gaining growing research interest in recent years (Woraprayote et al. 2018 ; Motelica et al. 2020 ; Alizadeh-Sani et al. 2021 ).

TC , total citations; the TC data was collected based on Web of Science core collection; PY , publishing year

As shown in Supplementary Figure 1 and Supplementary Figure 2 , food, safety, and environment were the top three most common words in titles. The following ones were assessment, health, risk, and environmental. It is well known that environmental pollution can pose risks on food safety and finally threatens human health. A further analysis revealed that a lot of studies were related to risk assessment, such as risk assessment of antimicrobial resistance (Likotrafiti et al. 2018 ; Pires et al. 2018 ), risk assessment of heavy metals (Yasotha et al. 2020 ), risk assessment of pesticide (Frische et al. 2014 ), risk assessment of veterinary drugs (Tsai et al. 2019 ), environmental risk assessment (More et al. 2020 ), and health risk assessment (Akhbarizadeh et al. 2020 ). The next one was efficacy, which was usually combined together with safety, such as safety and efficacy of feed additives (Bampidis et al. 2020 ). Besides, Listeria monocytogenes was intensively studied by researchers (Anast et al. 2020 ; Kawacka et al. 2020 ; Wu et al. 2020b ). Another common word was analysis, such as analysis of herbicide (Pan et al. 2020 ), analysis of bacteria (Kang et al. 2020 ), and analysis of microplastics (Primpke et al. 2020 ). Other common research topics revealed by title analysis included but are not limited to food quality, food production, food processing, food additive, food contamination, detection of food contaminants, food microbiology, environmental impact, as well as water, soil, animal, fish, meat, and dairy.

The top 20 most used keywords were listed in Table 3 (more details are provided in supplementary data ). It could be seen that microbiology was closely related to food safety, and a lot of studies were conducted on Listeria monocytogenes, biofilm, salmonella, and antibiotic resistance. In addition, additives, such as zootechnical additives and nutritional additives, were also intensively investigated by researchers. Other topics included aquaculture, poultry, and agriculture. Another keyword worth mentioning was food security. Food security is different with food safety. Briefly, food security is a more inclusive term and focuses more on the availability of food while food safety is about the quality of food. On the other hand, food security and food safety are closely related to each other (Vipham et al. 2020 ). For instance, if food security becomes a big issue, then usually food safety is not guaranteed, and vice versa. Generally, the results revealed by keywords analysis were in consistent with the above title and keywords analysis.

The keywords network graph revealed some interesting results. As shown in Figure 5 , the network had three centers, namely the “ food safety ”-centered network, the “ safety ”-centered network and the “ efficacy ”-centered network. Interestingly, the “ safety ”-centered network and the “ efficacy ”-centered network were closely related, while they were relatively unrelated with the “ food safety ”-centered network. Furthermore, the results again uncovered that food safety involved many aspects, many of which were already discussed above.

Keywords network graph. Keywords whose cooccurrence exceeded 10 times were connected with lines

The publications in this study were divided into over 200 Web of Science categories (more details are provided in supplementary data ). The top 20 Web of Science categories were shown in Figure 6 . Undoubtedly, the Food Science & Technology category ranked the first place, followed by the Environment Sciences category. As revealed by Figure 6 , food safety was closely related to microbiology, chemistry, and agriculture. Microorganisms such as foodborne pathogens pose great threats on food safety and a lot of studies are focusing on it. For instance, Lin et al (Lin et al. 2021 ) studied the role of Salmonella Hessarek, an emerging foodborne pathogen, in egg safety. Anyogu et al. (Anyogu et al. 2021 ) reviewed the microorganisms and indigenous fermented foods with a focus on microbial food safety hazards. Van Boxstael et al. ( 2013 ) studied the impacts of bacterial pathogens and viruses on food safety in the fresh produce chain. Also, a lot of studies are focusing on food safety and chemistry, such as untargeted food chemical safety assessment (Delaporte et al. 2019 ), chemical safety of recycled food packaging (Geueke et al. 2018 ), and chemical food safety hazards of sausages (Halagarda et al. 2018 ). Furthermore, studies on food safety and agriculture include but are not limited to chemical and biological risks in urban agriculture (Buscaroli et al. 2021 ), biosensors for sustainable agriculture and food safety (Griesche and Baeumner 2020 ), agricultural soil contamination, and the impact on food safety (Wang et al. 2019b ). In addition, the Materials Science category was also on the top list, which indicated that materials are also important research directions in environment and food safety. A further analysis revealed the common materials studied by researchers, including biomaterials, food packaging materials, biodegradable materials, coating materials, sensors and biosensors for food detection, and nanoparticles. The research area analysis showed similar results with Web of Science categories (Supplementary Table 3 ).

Number of publications and corresponding percentage of the top 20 Web of Science categories

Strategies to protect environment and ensure food safety

The above scientometric analysis revealed that the studies on environment and food safety were diversified and multidisciplinary. Further analysis of the above results disclosed the challenges and strategies to protect environment and ensure food safety. As discussed earlier, environment and food safety are closely related to each other. It should be noted that the environment here is not limited to the broad environment (e.g., air, water, soil) which the public are familiar with. In other words, in addition to the broad environment, there are also food-related environments which exist in various processes, including but are not limited to food processing, food packaging, food transportation, food storage, and food consumption. In order to ensure food safety, contaminants/pollutants from the environmental side should be prevented from reaching the food side. An example of food chain pollution control is presented in Figure 7 . It can be seen that from growing wheat to making bread, there are a variety of processes which could cause pollution and control strategies are needed, which are summarized as follows. Firstly, from wheat growing to wheat harvesting: the pollutants/contaminants could be taken in or migrate into the wheat via contaminated soil, water, and air, and therefore strategies are needed to prevent soil, water, and air from being contaminated, such as reducing the use of pesticides and fertilizers. Secondly, initial processing of wheat: after the wheat is harvested, traditionally it needs to be dried by the farmers before it is sold. During this process, contamination can easily occur if the wheat is dried directly on the road which is common in rural China. In addition, the containers of the harvested wheat are also sources of pollution which should be carefully controlled. Alternatively, the pollution can be avoided if the wheat is directly sold and transported to the flour mill from the farm without being dried by the farmers. Thirdly, during the transportation processes (e.g., from farm to flour mill, from flour mill to bread bakery, from bread bakery to supermarkets), contamination can also take place and control strategies are needed. Fourthly, during the wheat processing at the mill and bread baking at the bakery, contamination can take place due to environment exposure, insufficient frequency and quality of facility washing and cleaning, use of additives, etc. Fifthly, during the bread packaging process, the workers can be an important source of bread contamination if the bread is packed manually. Finally, when the consumers buy the bread and do not consume the bread timely, the bread can decay. Based on the above discussion, the food chain pollution control can be generally categorized into the following sections: source pollution (i.e., soil, water, air) control, pollution control during food processing, pollution control during food packaging, pollution control during transportation, pollution control during storage, and pollution control during consumption.

Demonstration of the whole food chain pollution control from wheat growing to bread consuming

Especially, based on the type of chemicals, the contaminants/pollutants can be categorized into pesticides and herbicides, heavy metals, food additives, pathogens, microplastics, antibiotics, and so on (Van Boxstael et al. 2013 ; Tóth et al. 2016 ; He et al. 2019b ; Rajmohan et al. 2019 ; Bonerba et al. 2021 ). Therefore, the corresponding strategies are to control the use of chemicals and materials which can produce these contaminates. For example, as will be discussed in the following section, microplastics come from the wide use of plastics and are receiving growing concern. In order to reduce the amount of microplastics, the use of plastics should be controlled or restricted. Based on the media of migration, these contaminants can reach at the food side via air, water, and soil. Therefore, the corresponding strategies are to remove contaminants from air, water and soil. Alternatively, strategies can be deployed to prevent these contaminants from contacting the food. For example, as will be discussed later, food packaging is a common strategy to protect food from being contaminated by the environment (Risyon et al. 2020 ). To sum up, by controlling the sources and migration routes of food contaminants, food safety can be improved. Furthermore, in order to ensure food safety, whole process monitoring techniques and platforms are necessary. A lot of studied have been conducted on food safety monitoring. For example, De Oliveira et al. ( 2021 ) proposed that environmental monitoring programs (EMPs) are necessary to ensure food safety and quality. The EMPs are used to prevent environmental contamination of the finished product, via checking the cleaning-sanitation procedures, and other environmental pathogen control programs with a range of sampling analysis. Medina et al. (Medina et al. 2019 ) proposed food fingerprints as an effective tool to monitor food safety. Weng et al. (Weng and Neethirajan 2017 ) reviewed microfluidics as an effective method to realize rapid, cost-effective, and sensitive detection of food contaminants such as foodborne pathogens, heavy metals, additives, and pesticide residues. Other monitoring methods/techniques/devices include but are not limited to pH-sensitive smart packaging films (Alizadeh-Sani et al. 2020 ), point-of-care detection devices (Wu et al. 2017 ), and real-time pathogen monitoring via a nanotechnology-based method (Weidemaier et al. 2015 ). Food safety monitoring can be done by either government officials or the relative bodies (e.g., self-monitoring), or both. Furthermore, from the time the food raw materials are being cultivated in the farmland, pasture, fishing ground or other places, to the time the food is being consumed by customers, inspecting and detecting should be deployed. This can be done by the government officials and/or the stakeholders. Although the term “inspection” and “detection” are often used as the same, here, food safety inspection is regarded as an administrative strategy, which is carried out by governmental officials to check whether the relative workers/factories/bodies have followed the food safety requirements/regulations, while food safety detection is regarded as a technique-based strategy, which is used to detect food contaminants and check whether the quality of the food meets the relative standards. Meanwhile, food safety laws need to be enacted to discourage or prevent the relative workers/factories/bodies from affecting the food safety, whether purposely or not.

On the other hand, during the process of food production, the environment can be polluted as well. For example, in order to increase crop yield, a lot of fertilizers are used, which will migrate into the soil and water bodies, and cause soil and water pollution. Therefore, the use of fertilizers should be restricted, which can be realized through agricultural innovations (Liu et al. 2021 ), government policies (van Wesenbeeck et al. 2021 ), etc. Furthermore, during food processing, a large amount of solid waste or/and wastewater are produced which can cause environmental pollution. Therefore, techniques are needed to dispose the food waste properly. Especially, food waste usually contains high amount of organic compounds and therefore falls into the category of biomass, which can be used to produce useful biochemicals like biofuels (Wainaina et al. 2018 ; Chun et al. 2019 ). For example, agro-food waste is an important source of lignocellulosic biomass; the valorization of lignocellulosic biomass is regarded as a sustainable source of energy and has the potential to replace conventional fossil fuels (Ong and Wu 2020 ; Lee and Wu 2021 ; Lee et al. 2021 ; Mankar et al. 2021 ; Zhenquan et al. 2021 ). Furthermore, the concepts of recycling and sustainable development can be deployed. For example, food packaging materials can be recycled and used again. Another example is to use cloth bags to replace plastic bags when shopping. These strategies can reduce the burden on the environment as the amount of food-related waste can be reduced. In addition, novel environment-friendly materials (e.g., biodegradable polymers) can be developed and used in food industries (Stoica et al. 2020 ; Cheng et al. 2021 ). To summarize, the above strategies to protect environment and ensure food safety are presented in Figure 8 .

Emerging studies on environment and food safety

Scientometric analysis is powerful in disclosing the research trend and is relatively subjective compared to conventional type of review. However, as it is essentially a statistical study which relies on a huge amount of data, it is less effective to reveal the emerging research directions which could be ignored in the scientometric study. Therefore, it is necessary and important to carry out a subjective discussion on emerging studies on environment and food safety as an indispensable supplement (Figure 9 ).

Emerging contaminants

There are various contaminants affecting environment and food safety. Among the various types of contaminants, emerging contaminants, such as microplastics, are receiving growing concern due to their potential effects on human health (Sarker et al. 2020 ). Because of the wide application of plastics, microplastics are found almost everywhere in the environment, including soil, water, and air (Álvarez-Lopeztello et al. 2020 ; Chen et al. 2020 ; Wang et al. 2021c ). For example, microplastics are reported to exist in bottled water (Zhou et al. 2021 ) and take-out food plastic containers (Du et al. 2020 ). Furthermore, researchers have found that microplastics could serve as the carrier for many other contaminants such as heavy metals and antibiotics (Zhou et al. 2019 ; Purwiyanto et al. 2020 ; Yu et al. 2020b ). Studies reveal that the ability to absorb heavy metals increase as the microplastics age (Lang et al. 2020 ). As a result, the risks of microplastics on environment, food safety, and human health could be significantly increased. However, the research on microplastics is still at an early stage, and more efforts are needed to uncover the world of microplastics. For example, there is no standard procedures to extract, identify, and quantify microplastics so results by different methods could be different and uncomparable (Kumar et al. 2020 ; Zhou et al. 2020 ). Meanwhile, due to the various sizes, shapes, forms, sources, and types of microplastics, it is difficult and time-consuming to characterize microplastics (Wu et al. 2020a ). Therefore, it is important to develop new methods for rapid and effective detection of microplastics (Li et al. 2020c ).

In addition to microplastics, there are other emerging contaminants which can have negative effects on the environment, food safety, and human health. These emerging contaminants include but are not limited to persistent organic pollutants (Titchou et al. 2021 ), antibiotics (Koch et al. 2021 ), personal care products (Scaria et al. 2021 ), pharmaceuticals (Chaturvedi et al. 2021 ), endocrine-disrupting compounds (Kasonga et al. 2021 ), and non-nutritive artificial sweeteners (Praveena et al. 2019 ). More research efforts are needed to gain a better understanding of the migration, degradation, accumulation characteristics, as well as the potential risks of these contaminants.

Rapid detection of contaminants

Not limited to the detection of microplastics, it is also necessary to develop rapid detection methods for common contaminants. For example, due to the widespread application of pesticides in agriculture, pesticide residue is becoming a serious environment and food safety issue (Farahy et al. 2021 ). Traditionally, food contaminants are detected by instrumental analysis, such as chromatography and mass spectrometry (Ye et al. 2019 ). However, the instrumental analysis process is expensive, complicated, and time-consuming (Zhang et al. 2019 ). Furthermore, the contaminants are usually in low concentration, but can accumulate gradually in human bodies via bioconcentration. Therefore, it is important to develop rapid method to detect trace-level concentration of food contaminants. Biosensor is an emerging and promising technology in detecting food contaminants such as pesticides, and a variety of biosensors have been developed in recent years (Majdinasab et al. 2018 , 2019 ). For example, Ouyang et al. (Ouyang et al. 2021 ) developed a sensitive biosensor to detect carbendazim pesticide residues based on luminescent resonance energy transfer from aptamer-labelled upconversion nanoparticles to manganese dioxide nanosheets. Capobianco et al. (Capobianco et al. 2021 ) developed an enzyme-linked immunoelectrochemical biosensor to detect pathogenic bacteria in large volume food samples without subsampling. Wang et al. (Wang et al. 2019a ) developed a magnetic quantum dot-based lateral flow biosensor to detect protein toxins in food samples. Kaushal et al. (Kaushal et al. 2019 ) developed a novel biosensor using gold nanorods capped by glycoconjugates which demonstrated potential in optical detection and ablation of foodborne bacteria. Generally, a biosensor is mainly composed of a biological sensing element (also known as bioreceptor), a transducer, and an electrical output system (Santana Oliveira et al. 2019 ; Majdinasab et al. 2021 ). The bioreceptor will interact with the analyte, and the transducer will convert the interaction into a detectable signal, which is then processed and displayed on the output system. Common materials used in the biological element include antibodies, enzymes, nucleic acids, antigens, aptamers, whole cells, and bacteriophage (Arora et al. 2011 ; Rotariu et al. 2016 ; Griesche and Baeumner 2020 ; Singh et al. 2020b . Biosensor technology has obvious advantages compared to traditional detection technologies. It is rapid, highly sensitive and selective, accurate, relatively compact, and easy to operate (Dominguez et al. 2017 ). However, there are still some challenges to widely commercialize biosensors, such as limited lifetime of the biological sensing elements and limited range of analytes that can be detected (Di Nardo and Anfossi 2020 ). Furthermore, as a specific type of biosensor is only effective in detecting a specific type of contaminant, more efforts are needed to develop integrated biosensors which can detect different types of containments simultaneously (Majdinasab et al. 2020 ). In addition to biosensors, there are also a variety of other reported methods for rapid detection of food contaminants, such as surface-enhanced Raman scattering (SERS) (Yao et al. 2021 ), optical sensors based on nanomaterials (Chen et al. 2021a ), hyperspectral imaging technology (He and Sun 2015 ), and perfluorinated compounds (PFCs) (Cai et al. 2021 ).

Environment friendly food packaging materials

As revealed above, food packaging is closely related to food safety. Although there are different kinds of food packaging materials, the non-biodegradable plastic materials (e.g., polyethylene, polypropylene, polyvinyl chloride, polystyrene, polyethylene terephthalate) are the most common ones and are widely used in our daily life (Cazón and Vázquez 2021 ). However, the non-biodegradable plastic materials have caused serious environmental problems, commonly known as white pollution. Especially, because of the coronavirus pandemic, take-out food becomes more popular. As plastic materials are the most common packaging materials for take-out food, the demand for plastic materials increases dramatically. Meanwhile, plastic materials also have food safety issues. It is found that the monomer residues used to make plastic polymers could migrate into food, which could cause health problems (Pilevar et al. 2019 ). Especially, the migration rate is not only affected by the quality of these materials, but also affected by the food properties. In addition to monomer residues, additives in these plastic materials could also migrate into food, causing health risks (Hahladakis et al. 2018 ). For example, bisphenol A, a common additive used in plastics, can adversely affect human endocrine system, block normal cell function, affect thyroid hormone, affect testosterone levels, and could also possibly induce cancer (Huang et al. 2019 ; Vilarinho et al. 2019 ). Another very common additive in plastics is phthalates, which is used as plasticizer to soften the plastics. It is reported that phthalates in plastic bottles could migrate into water, and the amount of migration increases as the storage time increases (Luo et al. 2018 ). Similar to bisphenol A, phthalates can also disrupt human endocrine system and cause bad effects on human health (Wang et al. 2018 ). Not limited to bisphenol A and phthalates, there are many types of plastic additives which could migrate into food and cause food safety issues.

As the conventional non-biodegradable plastics can cause both environmental problems and food safety issues, a lot of studies are carried out to find alternatives to non-biodegradable plastics for food packaging. Biodegradable polymers are regarded as the one of the most promising alternatives for food packaging (Othman 2014 ). As its name indicates, biodegradable polymers can be decomposed by microorganisms. Common biodegradable polymers studied as food packaging materials include but are not limited to polylactic acid (PLA) (Swaroop and Shukla 2018 , 2019 ; Mohamad et al. 2020 ), polybutylene adipate terephthalate (PBAT) (Pattanayaiying et al. 2019 ), polysaccharides (such as starch (Osorio et al. 2019 ; Menzel 2020 ; Saraiva Rodrigues et al. 2020 ), cellulose (Balasubramaniam et al. 2020 ; Riaz et al. 2020 ), pectin (Nešić et al. 2018 ), chitosan (Haghighi et al. 2020 ; Priyadarshi and Rhim 2020 )), polyhydroxyalkanoates (PHAs) such as polyhydroxybutyrate (PHB) (Adeleye et al. 2020 ; Fernandes et al. 2020 ; Shahid et al. 2020 ), polycaprolactone (PCL) (Khalid et al. 2018 ; Mugwagwa and Chimphango 2020 ), and cellulose acetate (Xie and Hung 2018 ; Rajeswari et al. 2020 ).

However, in addition to high production cost, there are some critical technical challenges which must be solved so as to widely commercialize biodegradable polymers and replace conventional plastics (Pérez-Arauz et al. 2019 ). Generally, biodegradable polymers have low thermal stability, low mechanical stability, and poor barrier properties (Risyon et al. 2020 ). One way to improve its performance is to add additives during production. For example, Risyona et al. (Risyon et al. 2020 ) prepared PLA-based film using different concentrations of halloysite nanotubes as additives. They found that the PLA film with 3.0 wt.% of halloysite nanotubes demonstrated optimal properties. Dash et al. (Dash et al. 2019 ) prepared starch and pectin-based film using different concentrations of titanium dioxide nanoparticles. They found that addition of the nanoparticles could effectively improve the mechanical properties and moisture barrier properties of the films. However, similarly to conventional plastics, these additives might also migrate into food (He et al. 2019a ). Another strategy being intensively studied is polymer blending, which integrates the merits of different polymers (de Oliveira et al. 2020 ). For example, Rajeswari et al. (Rajeswari et al. 2020 ) blended polysaccharides and cellulose acetate together, and the resulting film showed improved thermal stability and tensile strength. The prepared films also demonstrated antimicrobial properties towards certain types of microorganisms. Sangroniz et al. (Sangroniz et al. 2018 ) blended poly(butylene adipate-co-terephthalate) with poly(hydroxi amino ether), and the resulting film showed great improvement of barrier properties. However, polymer blending could also have its drawback. For example, if the blending polymers are immiscible with each other, the mechanical strength and barrier properties of the resulting materials will be affected (Corres et al. 2020 ).

Conclusions, challenges, and future research directions

In this review, a scientometric-based statistical study was firstly conducted on the research of environment and food safety, which revealed that the research on environment and food safety was growing steadily from 2001 to 2020. Interestingly, statistical analysis of the most-cited papers, titles, abstracts, keywords, and research areas revealed that the research on environment and food safety is diverse and multidisciplinary. Furthermore, strategies to protect the environment and ensure food safety are discussed, such as controlling the use of chemicals and materials which can produce environment and food contaminates, preventing these contaminants from contacting the food, developing whole process monitoring techniques and platforms, and utilizing the food waste properly. In addition, emerging research topics are discussed, such as emerging contaminants, rapid detection of contaminants, and environment friendly food packaging materials.

Although environment and food safety are receiving growing concern, there are still some very challenging issues. These challenges can be categorized into four parts. Firstly, it is challenging to eliminate environmental pollutions (Hao et al. 2018 ; Christy et al. 2021 ). Air pollution, water pollution, and soil pollution are still serious environmental problems in many parts of the world (Wu et al. 2016 , 2021a ; Rajeswari et al. 2019 ; Shen et al. 2021b ). Although a lot of studies have been carried out, the mechanisms of some pollutions (e.g., haze weather) are still unclear (Shen et al. 2020 ; Wang et al. 2021a ). Secondly, it is challenging to dispose food waste effectively and efficiently. It is reported that a substantial amount of food waste is produced along the food supply chain (Aschemann-Witzel 2016 ; Li et al. 2019 ). Especially, food wastewater typically contains very complex components, and the treatment process is very energy intensive and costly. Thirdly, it is challenging to realize whole-process monitoring of contaminants, due to the diverse contaminants during food cultivation, processing, packaging, transportation, and retailing. Fourthly, the accurate effects of environmental pollution on human health are still unclear, and it is challenging to establish procedures to accurately assess the risks of environmental pollution on human health. For example, it is well reported that ozone pollution and PM2.5 pollution can cause negative effects on human health (Guan et al. 2021 ; Shen et al. 2021a ; Wang et al. 2021b ). However, the underlying mechanisms, accurate assessment procedures, and quantitative studies are still lacking. In order to address these challenges, more research efforts are needed to (1) uncover the underlying mechanisms of contaminant formation, migration and fate; (2) develop more cost-effective and sustainable food waste treatment and utilization technologies, targeting net zero emissions; (3) develop rapid detection methods and in situ monitoring technologies for environment and food safety; and (4) establish health risk assessment models and procedures.

Data availability

All data generated or analyzed during this study are included in this published article.

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This work was supported by the Beijing Municipal Commission of Education (grant no. PXM2019_014213_000007) and School Level Cultivation Fund of Beijing Technology and Business University for Distinguished and Excellent Young Scholars (grant no. BTBUYP2020).

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Jiang, ., Wang, F., Li, Q. et al. Environment and food safety: a novel integrative review. Environ Sci Pollut Res 28 , 54511–54530 (2021). https://doi.org/10.1007/s11356-021-16069-6

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Factors associated with food safety practices among food handlers: facility-based cross-sectional study

• Jember Azanaw 1 ,
• Mulat Gebrehiwot 1 &
• Henok Dagne 1  

BMC Research Notes volume  12 , Article number:  683 ( 2019 ) Cite this article

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The primary objective of this study was to assess factors associated with food safety practices among food handlers in Gondar city food and drinking establishments. The facility-based cross-sectional study was undertaken from March 3 to May 28, 2018, in Gondar city. Simple random sampling method was used to select both establishments and the food handlers. The data were collected through face-to-face interview using pre-tested Amharic version of the questionnaire. Data were entered and coded into Epi info version 7.0.0 and exported to SPSS version 22 for analysis.

One hundred and eighty-eight (49.0%) had good food handling practice out of three hundred and eighty-four food handlers. Marital status (AOR: 0.36, 95% CI 0.05, 0.85), safety training (AOR: 4.01, 95% CI 2.71, 9.77), supervision by health professionals (AOR: 4.10, 95% CI 1.71, 9.77), routine medical checkup (AOR: 8.80, 95% CI 5.04, 15.36), and mean knowledge (AOR: 2.92, 95% CI 1.38, 4.12) were the factors significantly associated with food handling practices. The owners, managers and local health professionals should work on food safety practices improvement.

Introduction

Food safety continues as a critical problem in developed and developing nations for people, food companies and food control officials [ 1 , 2 ]. Food-borne diseases (FBD) are associated with outbreaks and threatens global public health security and has got an international concern [ 3 ]. Food safety is a growing public health issue [ 4 ]. FBD is responsible for significant morbidity and mortality rates [ 5 ]. The worldwide incidence and financial expenses of food-borne diseases are hard to determine [ 6 ]. However, reports estimate that 2.1 million individuals died each year as a result of foodborne disease [ 5 ].

According to the WHO, FBDs in developing nations are serious because of bad hygienic food handling methods, bad understanding and absence of infrastructure [ 7 ]. This is due to the prevailing poor food handling and sanitation practices, inadequate food safety laws, weak regulatory systems, lack of financial resources, etc. [ 6 , 8 ]. Evidence revealed that around 70% of diarrhoea cases were attributed to food-borne routes in developing countries [ 6 ]. Like other developing countries, the burden of food-borne diseases is growing in Ethiopia [ 18 ].

Approximately 10 to 20% of FBD outbreaks are because of contamination due to poor food handling practice of the food handlers [ 9 ]. In the absence of well-maintained and proper food handling practices in mass catering establishments have the potential to impart a disastrous effect on human health [ 6 , 11 ].

Good personal hygiene and food handling practices are important for preventing the transmission of pathogens from food handlers to the consumers [ 12 , 13 , 14 ]. Close to 75% of food-borne illness outbreaks are attributed to lack of safe food handling practices by food handlers in food service establishments [ 5 ]. Food handlers play a key role in ensuring strict adherence to food safety principles throughout the whole process [ 15 ].

There is a high expansion of food establishments observed in the country including Gondar city. But ensuring safe food service has been one of the major challenges and concerns for producers, consumers and public health officials. Studies revealed that lack of basic sanitary facilities/infrastructures, poor knowledge and practice of hygiene and sanitation among food handlers in food service establishments, and negligence in safe food handling are major reasons of poor food safety practice in food establishments [ 16 , 17 ]. Therefore, it is very essential to identify factors affecting safe food handling practices, especially during preparation and serving. Thus, this study aimed to evaluate factors associated with food safety practice among food handlers in Gondar city food establishments.

This facility-based cross-sectional study was conducted from March 3 to May 28, 2018 at Gondar city. Gondar city is one of the highly populated cities in northwest Ethiopia. There were a total of 326 food establishments and 4232 food handlers in Gondar city according to tourism office data. The city is found at 738 km away from Addis Ababa the capital city of Ethiopia. Ninety-eight food establishments were included using the rule of thumb by taking 30% of the total food establishments. n = N × 30% = 326 × 30/100 = 97.8 ≈ 98 none star food establishments.

The sample size was computed using a single population proportion formula with 95% CI, 5% marginal error (d) and p = 52% proportion of food handlers having good food handling practice from the previous study [ 19 ]. Based on these assumptions, 384 food handlers were included in the study.

To select food establishments and food handlers, a simple random sampling technique was used. In each institution, four food handlers were interviewed. After adaptation from similar literature [ 12 , 19 , 20 , 21 ], the questionnaire was first prepared in English and translated to local language Amharic version. The pre-test was performed on 5% food handlers out of the study area before actual data collection. Then, correction and modification were undertaken based on the gaps identified during the pre-test. Reliability of the questionnaire was also evaluated. The information was gathered via a face-to-face interview using the questionnaire’s Amharic version. Four Environmental Health Officers have been engaged as data collectors and the principal investigator was involved as a supervisor. Food safety practice was the dependent variable in this research. Socio-demographic variables and behavioural factors were the independent variables. Food handling practice: food handlers were asked seventeen questions and those who scored less than or equal to the mean value were considered as having poor practice and those who scored greater than the mean value were considered as having good practice [ 19 , 21 ]. Knowledge: Respondents were asked ten questions and those who scored less than or equal to the mean value were considered as having a poor knowledge [ 12 , 22 ].

Consistency and completeness of data were verified during collection, entry and analysis. Data were entered and coded into version 7.0.0 of Epi Info and exported for evaluation to version 22 of SPSS. The data were analysed using descriptive (frequency and proportion), bivariate, and multivariable regression analysis. Variables with p-value < 0.25 during bivariate analysis were included in multivariable regression to assess the independent effect after controlling other variables [ 23 ].

We did Hosmer and Lemeshow test to check the model fitness. SPSS Cronbach’s Alpha test result for practice questionnaire was 0.83. Finally, 95% confidence level, AOR and p-value less than 0.05 were considered for determining statistically significant variables.

Sociodemographic characteristics of study participants

Of the three hundred eighty-four food handlers, 338 (88%) were females, 300 (78.1%) were unmarried; and 318 (82.8%) had an income of 500–1000 Ethiopian birr (28 ETB = 1 USD) (Table  1 ).

Knowledge of food handlers regarding the cause of food-borne disease, mode of transmission and way of food contamination

Three hundred sixteen (82.29%) of food handlers stated that food-borne diseases are caused by germs. More than half 199 (51.8%) of food handlers found this information from health center about food safety practices (Table  2 ).

Food handling practice of food handlers in food and drinking establishments

More than half of (51.5%) food handlers use hair net during food preparation. One hundred ninety (49.5%) of food handlers did not attend routine medical checkups. About 37% of the respondents were not wearing a uniform during handling and preparation of food (Table  3 ).

Factors associated with food safety practices

Multivariable logistic regression analysis revealed that marital status, food safety training, routine medical checkup, supervision by health professionals and knowledge were statistically associated variables with food safety practices.

Single food handlers were 64.0% less likely to practice food safety than the single food handlers (AOR: 0.36, 95% CI 0.05, 0.85). Food handlers supervised by health professionals were 4.10 times more likely to practice good food safety than non-supervised (AOR: 4.10, 95% CI 1.71, 5.27). Knowledgeable food handlers were 2.92 times more likely to practices good food safety than non-knowledgeable (AOR: 2.92, 95% CI 1.38, 4.12). Trained food handers were 4.01 times more likely to have good food handling practice than non-trained food handlers (AOR: 4.01, 95% CI 2.71, 9.77). Food handers followed routine medical checkup had 8.80 times more likely to have good food handling practice than not- followed food handlers (AOR: 8.80, 95% CI 5.04, 15.36) (Table  3 ).

One hundred eighty-eight (49.0%) food handlers had good food safety practice. This finding is lower than the findings of studies in Bahir Dar (67.6%) [ 24 ], Arba Minch (67.4%) [ 21 ] and in Dubai (81.74%) [ 17 ]. While the finding was close with studies in Dangila town (52.5%), Addis Ababa (52.3%), Imo State, Nigeria (50%) and Turkey (48.4%) [ 6 , 19 , 25 , 26 ], respectively. However, it is higher than the studies done in Gondar town (22.1%) [ 5 ], South-Western Nigeria (19.0%) [ 27 ], Ogun, Nigeria (31.5%) [ 19 ]. These variations might be due to the difference in the study design, variation in training, and the provision of food hygiene and safety inputs. About 109 (28.4%) of the food handlers were certified in food safety training. This result is higher as compared with findings from Bahir Dar (21.8%) and Mekelle (15.7%) [ 12 , 28 ]. Food handler training is seen as one strategy whereby food safety practice can be increased, offering long-term benefits to the food establishments [ 29 ]. This finding is supported with studies conducted India [ 10 ], Nigeria [ 30 ], Ghana [ 31 ] and Dubai [ 32 ]. The number of food handlers who recieved food safety training in the current study is higher than with findings from Bahir Dar (21.8%), and Mekelle (5.4%) [ 12 , 28 ]. Food handlers who received training would have a better understanding of safe food handling practice as they might get professional advice during training. Training could enhance food handlers overall performance in safe food handling practice [ 21 ]. In this study, food handlers who got safety training had higher odds of good food safety practice. This might be due to trained food handlers gain good awareness through training. This supported with other similar study done in Sarawak [ 33 ]. Training programs are important for improving the knowledge of food handlers [ 34 ]. Food safety practice was also positively associated with the level of knowledge. The probability of having a good food safety practice among participants with good level of knowledge was 2.39 times higher with compared to those with a poor level knowledge (AOR = 2.39, 95% CI 1.38, 4.12). Food handlers are expected to have substantial knowledge and skills for handling foods hygienically [ 12 ]. This might be due to those food handlers who had a good level knowledge might have a higher chance of good food handling practice. This finding was supported studies conducted in Gondar town, and Malaysia [ 5 , 15 ]. Marital status was another significantly associated factor with food safety practices. Single food handlers had lower probability of good food safety practices compared with divorced handlers. This is supported with the study done in Gondar town and Dangila town [ 19 ].

Food safety practice was significantly associated with supervision by health professionals. The probability of having good food safety practice was higher among food handlers supervised by health professionals as compared with non-supervised. This finding was supported by the study conducted in Arba Minch [ 21 ]. This might be due to supervisors give advice for food handlers, the owners and to the managers. A routine medical checkup was also another factor significantly associated with good food handling practice. The probability of having good food safety practice among food handlers engaged with routine medical checkup was higher than food handlers not engaged in routine medical checkup. This could be the health care workers gave advice for food handlers during examination. This finding is in line with studies conducted in Arba Minch and Dessie towns [ 20 , 21 ]. This study revealed that there was poor food handling practice among food handlers. Marital status, food safety training, supervision by health professionals, routine medical checkup, and level of knowledge of food handlers were significantly associated with good food handling practice. Owners, managers and local health professionals should enhance the level of knowledge of food handlers, provide food hygiene, safety training, undertake periodic supervision, and routine medical checkup.

Limitations

This study was not without limitations. Some of the limitations include inherent weakness of cross-sectional study to establish a cause–effect relationship, social desirability bias and recall bias.

Availability of data and materials

We will make data available upon request the primary author.

Abbreviations

World Health Organization

adjusted odds ratio

confidence interval

crude odds ratio

Statistical Package for Social Sciences

Ethiopian Birr

Institutional Review Board

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Acknowledgements

The authors are grateful to all study participants, data collectors, food establishment owners and the University of Gondar for their willingness and support to the success of this study.

The authors of this study have received no funds from anywhere but the University of Gondar has covered questionnaire duplication fees.

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JA took part in the research development proposal, data collection tools, entered data into Epi-info, analyse and interpret the data, and write various parts of the research report. MG and HD advised from the starting to the end. All authors read and approved the final manuscript.

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Correspondence to Jember Azanaw .

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We got ethical clearance from the Institutional Review Board (IRB/47/2010) of the Institution of Public Health, University of Gondar. Written informed consent was obtained from each study participants. The consent of the city administrator, the manager of the food and drinking establishments, and the respondents took part willingly. We kept the confidentiality of the respondents and for the food and drinking establishments by asking the participants not to write their names on the questionnaires and codes to conceal the identity of the food and drinking establishments. We used the collected data for this research purpose only. We forwarded health educations to the study participants by data collectors and the principal investigator at the end of the data collection.

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Azanaw, J., Gebrehiwot, M. & Dagne, H. Factors associated with food safety practices among food handlers: facility-based cross-sectional study. BMC Res Notes 12 , 683 (2019). https://doi.org/10.1186/s13104-019-4702-5

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Received : 10 August 2019

Accepted : 04 October 2019

Published : 22 October 2019

DOI : https://doi.org/10.1186/s13104-019-4702-5

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• Food safety
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• Food establishment
• Food-borne diseases

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Food Safety Research Priorities & Studies

The Food Safety and Inspection Service (FSIS) has developed a listing of the top food safety research areas of interest. FSIS has also identified key data gaps and laboratory methods that are needed to fulfill our mission.

While FSIS is not a research funding organization, it recognizes the importance of keeping abreast of the latest scientific endeavors as well as its role in promoting research in areas important to the FSIS mission. This listing supports the three goals of the FSIS Strategic Plan :

• Prevent Foodborne Illness and Protect Public Health
• Modernize Inspection Systems, Policies, and the Use of Scientific Approaches
• Achieve Operational Excellence

These priorities are presented as suggestions for researchers interested in pursuing food safety objectives that are relevant to FSIS regulated products. This list of research areas of interest may be useful to researchers who are preparing grants for submission to agencies that fund food safety research (e.g., USDA National Institute of Food and Agriculture ( http://www.nifa.usda.gov ), National Institutes of Health ( https://www.nih.gov/ ), Grants.gov ( http://www.grants.gov ), or researchers with resources to conduct such research.

While FSIS is extremely interested in these research areas, this interest does not imply that the data and/or technologies generated by this research will be endorsed by FSIS.

This list represents FSIS' current assessment of priority research that will help further its public health mission; the list will be updated biannually. We encourage researchers to contact Dr. Isabel Walls by e-mail ( [email protected] ) or at (202) 924-1420 and Dr. John Hicks by e-mail ( [email protected] ) or at (301) 504-0840 with questions. We also welcome information about research on related topics not currently listed here.

Research Priorities

Chemicals of potential concern, screening/detection methods.

• Develop or improve rapid methods for screening chemical compounds in FSIS regulated products
• Develop models to estimate chemical residue concentrations in beef, pork, and chicken tissues

Chemical Characterization

• Determine the magnitude and significance of migration of chemicals (e.g., endocrine disruptors) from packaging into FSIS regulated products

Intervention Strategies

• Identify and/or develop and evaluate the effectiveness of pre- and post-harvest interventions to reduce levels of chemical hazards in FSIS regulated products

Biological Hazards

Screening/detection/enumeration methods.

• Identify and evaluate improved sampling methods to ensure statistically relevant samples are collected in the most appropriate manner
• Develop or refine technologies to reduce pathogen detection time, including improved sample preparation methods
• Develop or refine technologies to detect multiple pathogens from a single sample of an FSIS regulated product
• Develop or refine testing methods for quantifying pathogens in meat, poultry, and egg products

Pathogen Characterization

• Develop bioinformatic methods for identifying epidemiologically meaningful patterns in whole genome sequence data
• Develop or refine technologies for virulence/ pathogenicity characterization of pathogens
• Improve our understanding of antimicrobial resistance in pathogens in poultry and cattle
• Develop or refine cooking and cooling models for pathogens in foods
• Determine the contribution of endogenous extra-intestinal sources of pathogens (e.g., lymph nodes) to contamination of FSIS-regulated products
• Evolution and Ecology of Foodborne Pathogens
• Identify and/or develop and evaluate the effectiveness of pre- and post-harvest interventions to reduce levels of pathogens in FSIS regulated products
• Evaluate the impact of regulatory initiatives on food contamination
• Identify consumer or retail practices which compromise the safety of FSIS regulated products
• Generate data to develop public education and outreach to improve food-handling practices

Animal Welfare

• Identify or develop approaches to facilitate humane handling of FSIS regulated livestock

Label Verification

• Develop improved techniques for species identity in raw and processed products

FSIS has identified the following data gaps, where data are needed to inform FSIS policy and guidance documents.  Collecting these data will benefit small and very small producers of meat, poultry, and egg products.

FSIS Data Gaps

1. A study is underway at USDA's Agriculture Research Service in support of this project.

Laboratory Detection Methods

FSIS has identified studies that pertain to validating and optimizing new laboratory methods, that may be adopted in the FSIS laboratory system after the basic research has been completed.

Research Studies

The Food Safety and Inspection Service (FSIS) has developed a list of the top food safety research areas of interest. Below are a list of specific research studies associated with our food safety research priorities. 

1. Preharvest Interventions

2. postharvest, 3. consumer/retail, related resources.

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ORIGINAL RESEARCH article

This article is part of the research topic.

Consumer Behavior around Food Safety and Quality in the Context of Technological Innovation

The Impact of Agricultural Insurance on Consumer Food Safety: Empirical Evidence from Provincial-Level Data in China Provisionally Accepted

• 1 Wuhan University, China
• 2 Wuhan College, China

The final, formatted version of the article will be published soon.

In the exploration of the efficacy of agricultural subsidy policies, agricultural insurance, as a key element of this policy system, has garnered widespread attention for its potential impact on consumer food safety. This paper delves into the influence of agricultural insurance on the safety of food consumed by individuals, based on provincial panel data in China from 2011 to 2021. The findings indicate that agricultural insurance significantly reduces the incidence of foodborne disease and enhances food safety. Mediating effect tests reveal that agricultural insurance effectively boosts food safety through two key pathways: promoting innovation in agricultural technology and reducing environmental pollution. Moreover, the analysis of moderating effects highlights that increased consumer confidence positively enhances the impact of agricultural insurance. Heterogeneity tests further show that in the provinces with higher levels of agricultural development and stronger government support for agriculture, the role of agricultural insurance in improving food safety is more pronounced. This research not only empirically verifies the effectiveness of agricultural insurance in enhancing food safety but also provides robust theoretical support and practical guidance for the precise formulation and effective implementation of agricultural subsidy policies, particularly agricultural insurance policies, offering significant reference value for policy-makers.

Keywords: Agricultural subsidies, Agricultural insurance, Food Safety, Agricultural Technological Innovation, Environmental Pollution, Consumer confidence

Received: 27 Feb 2024; Accepted: 15 Apr 2024.

Copyright: © 2024 Ruan, Yin and Zhang. 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) or licensor 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: Mx. Peiheng Ruan, Wuhan University, Wuhan, 430072, Hubei Province, China

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