The level of food safety knowledge among meat handlers

Abstract

Purpose

- The purpose of this paper was to evaluate food safety knowledge of among meat handlers in Serbian meat establishments along the meat chain, i.e. in slaughterhouses, meat processing plants and retail stores.

Design/methodology/approach

- A structured, self-administrative questionnaire was designed and used to assess the level of food safety knowledge among handlers in different meat establishments. In total, of 352 meat handlers were involved in this study, with 110 handlers from slaughterhouses (31 per cent), 125 handlers from meat processing plants (36 per cent) and 116 handlers from retail stores (33 per cent). For each participant, the knowledge score was calculated by dividing the sum of correct answers by the total number of correct responses. Additionally, knowledge gaps among meat handlers were identified for each question across the three types of establishments (slaughterhouses, meat processing plants and retail stores).

Findings

- The average knowledge score for all participants was 64 per cent, whereas handlers from slaughterhouses and meat processing plants obtained significantly better scores (65 per cent and 66 per cent, respectively) than handlers from retail (60 per cent,p < 0.05). The knowledge score among all meat handlers was significantly associated with the age, education and previous food safety trainings. Results indicated that 57.9 per cent meat handlers could identify that bacteria will readily multiply at 25 °C, but they do not understand the manifestation of bacterial growth and incidence in food, as only 5.5 per cent of all meat handlers knew that food contaminated with food poisoning bacteria cannot be recognized by visual, olfactory or taste checks.

Originality/value

- This is the first research aimed to investigate the food safety knowledge among meat handlers in Serbia and also the first research performed to determine food safety knowledge among workers operating in different phases of the meat chain, namely meat handlers from slaughterhouses, meat processing plants and retail stores.

1. Introduction

Food-borne diseases, are caused by biological, chemical and physical hazards, which can contaminate food at several points during production and preparation process. Although the research in this field have been very intensive during the last decades, and many preventive and control measures have been already applied in the food industry, the burden of food-borne diseases remain at unacceptably high level (Havelaar et al. , 2010).

The surveillance of food-borne diseases in Serbia is a part of the Communicable Disease Information System. A national Communication Centre for surveillance, based on the European Centre for Disease Prevention and Control, is established within the Serbian National Institute of Public Health. According to its latest report, there were 114 food-borne outbreaks with 948 human cases and no deaths in the year 2013. Among these, 65.79 per cent of all food-borne outbreaks were associated with Salmonella (NIPHS, 2014). One of the biggest food-borne outbreak in 2013 occurred in the city of Smederevo, during the popular tourist manifestation "Smederevo's autumn". The epidemic of diarrhoea and gastroenteritis were announced, as 310 patients, including 220 children and 90 adults requested medical help within two days. The suspected food was grilled meat that was served at the event, although the official source of infection was never confirmed (Radovic et al. , 2014). Additionally, during 2013 and 2014, two important food-borne outbreaks also occurred, one among the workers in Serbian car factory and another among children in six Belgrade schools. The suspected vehicle in both cases was minced meat served in spaghetti, without an official announcement.

Food handlers have a very important role in the prevention of food poisoning as they may introduce pathogens within the entire food chain. They may cross-contaminate raw and processed, ready-to-eat foodstuffs and are often carriers of some specific food-borne pathogens such as hepatitis A virus, noroviruses, Salmonella , Staphylococcus aureus (Todd et al. , 2008). Good hygiene, both personal and during food handling practices, is the major preventive action for pathogen transmission from food handling personnel to final consumer. According to Todd et al. (2007), the most frequently reported food handlers' errors which resulted in subsequent outbreaks, were food handling by an infected person or by a person carrying a food-borne pathogen, bare-hand contact with food, improper washing hands and insufficient cleaning of processing or preparation equipment (Nørrung and Buncic, 2008). One example of mistaken actions in the butcher shop resulted in Lanarkshire outbreak of E. coli O157, as meat handlers used biodegradable instead of bactericidal cleaners and allowed spread of pathogen (Pennington, 2014).

The most of handlers' implicated outbreaks came from food service facilities, such as restaurants and cafeterias, followed by catered events, schools and day care centres, processing facilities, homes and community events (Todd et al. , 2007). It is of note that fewer outbreaks occurred in big processing plants, most probably due to more stringent controls which are usually in place, either introduced voluntarily by management or by food control agencies that closely regulate the foodstuffs due to the potentially widespread distribution of products (Todd et al. , 2007). On the contrary, small food processing plants face more difficulties in the effective implementation of any food safety system. Often, small food producers are more vulnerable to contamination, especially if there is a lack of in-house knowledge and understanding of good manufacturing practices and the spread of diseases (Walker et al. , 2003). Although we are witnesses of global hand hygiene campaigns, with decades of employee personal hygiene trainings, millions of posters and talks by managers encouraging employees to properly wash their hand, personal hygiene remains one of the major problems in good hygiene practice (Pellegrino et al. , 2015; Sofos and Geornaras, 2010). Therefore, the knowledge on food safety issues and level of practical training on hygienic handling of food are very important to protect the health of the consumers (Gomes et al. , 2014). This is of particular significance for the production and distribution of highly perishable foodstuffs, such as meat and meat products.

Several studies have been conducted in previous years to investigate the level of food safety knowledge among food handlers working in restaurants and catering (Bas et al. , 2006; Jevsnik et al. , 2008; Panchal et al. , 2013, 2014; Pichler et al. , 2014; Sun et al. , 2012), hospital food service (Tokuç et al. , 2009), small businesses (Gomes-Neves et al. , 2007; Walker et al. , 2003), production of sauerkraut (Jevsnik et al. , 2008), meat processing plants (Ansari-Lari et al. , 2010; Gomes-Neves et al. , 2011; Jianu and Golet, 2014) and seafood production (Zanin et al. , 2015). The aim of this study was to investigate the level of food safety knowledge among food handlers in Serbian meat industry, in different stages of the meat chain, i.e. in slaughterhouses, meat processing plants and retail stores.

2. Material and methods

2.1. Selection of meat handlers

This study was conducted in the period April-December 2014 in 41 different Serbian meat establishments (25 companies with < 10 employees, 12 companies with 10-25 employees and four companies with > 25 employees) It involved 352 meat handlers. Initially, managers or food technologists in different meat establishments were contacted by phone and invited to take part in this survey.

The purpose of the study and instructions for completing the questionnaire were initially explained to the managers or food technologies in person in the companies that agreed to participate in the study. Due to the fear of the workers in respect to potential work consequences in the case of incorrect answers, questionnaires were distributed to the meat handlers during breaks and clear instructions for filling the questionnaires were given, emphasizing the aspects of anonymity and confidentiality. The completed questionnaires have been collected in person after the break, assuring that all questionnaires have been collected.

2.2. Questionnaire

A structured, self-administrative questionnaire was designed and adopted from previously performed studies (Gomes-Neves et al. , 2011; Jevsnik et al. , 2008; Walker et al. , 2003). The first part of the questionnaire was composed of demographic characteristics of the workers (gender, age, education level, experience in the food sector, experience at the current working place and food safety training) and meat establishment (number of workers and type of meat establishment). In the food safety knowledge part, there were 52 questions divided in four sections covering cross-contamination (ten), temperature regime (eight), food handling and health problems (12), hand hygiene (seven) and knowledge about food products and food-borne diseases (15). Different types of questions were used in the questionnaire, giving them the possibility to answer either between true/false, between yes/no or between multiple choice answers. Additionally, meat handlers had the possibility to circle "I don't know" for each question, to minimize the possibility to select the correct answer randomly.

2.3. Data analysis

For each participant in the study, the knowledge score was calculated by dividing the sum of correct answers by the total number of correct responses. Knowledge scores were analysed using an independent sample t -test (for two groups, such as gender) or analysis of variance (ANOVA) with post hoc Tukey test (for more than two groups, such as age, level of education, experience in food sector or food safety training (SPSS Statistics 17.0)). To identify knowledge gaps among meat handlers, [chi] 2 test was used to compare the percentage of correct responses to each question across the three types of meat establishments (slaughterhouses, meat processing plants and retail stores). Values with a p < 0.05 were considered statistically significant.

3. Results and discussion

3.1. Sample characteristics

Total number of 352 meat handlers were involved in this study, with 110 handlers from slaughterhouses (31 per cent), 125 handlers from meat processing plants (36 per cent) and 116 handlers from retail stores (33 per cent), with almost equal number of male and female participants, being 49 per cent and 51 per cent, respectively (Table I). The mean age of all participants was 39 years, with the youngest participant being 19 years old, and the oldest 65 years old. The majority of participants 255 (73 per cent) had high school degree, while 47 (14 per cent) of all participants had only elementary school. In total 22 meat handlers had the university degree (6 per cent) and they were mainly employed in slaughterhouses and meat processing plants. Regarding work experience in the food sector, 114 (33 per cent) of participants had between two and eight years of work experience, 91 (27 per cent) had between eight and 16 years and > 16 years of work experience had 100 participants (29 per cent). In total 47 workers (14 per cent) had participated in the food safety training organized by the Ministry of Agriculture, Forestry and Water Management, while 185 (57 per cent) had participated in the training organized by other institutions. It is of note that 94 (29 per cent) participants had no training related to food safety at all with 50 of them being employed in the retail sector, although this is a mandatory requirement according to Food Safety law (Serbia, 2009, 2010).

3.2. Knowledge scores within different meat establishments

Overall, the knowledge score for all participants in this study was 64 per cent, whereas the workers from slaughterhouses and meat processing plants obtained significantly better scores (65 per cent and 66 per cent, respectively) than the workers from the retail sector (60 per cent, p < 0.05) (Table I).

3.2.1. Knowledge scores for all meat handlers

The knowledge score among all meat handlers was significantly associated with the age (p =0.030), education (p < 0.001) and participation in the food safety training (p < 0.001) (Table I). The participants that were < 24 years old in total scored 59 per cent, whereas older participants had better scores, with those aged between 45 and 54 having the highest obtained knowledge scores of 66 per cent. As expected, the participants with the lowest education (only primary school) scored the lowest values (59 per cent), and the highest educated participants (holding university degree) scored the highest values (76 per cent). This is in line with results previously published (Angelillo et al. , 2001; Ansari-Lari et al. , 2010; Jianu and Golet, 2014), in which positive correlation was seen between the level of knowledge and education. As expected, previous participation in different food safety trainings (either organized by ministry or other institutions) significantly influenced food safety knowledge output, as participants who had undergone some food safety training got 65 per cent, compared to those who had no training at all, with knowledge scores of 59 per cent (p < 0.001). These results are in accordance with previous findings reported elsewhere (Bas et al. , 2006; Gomes-Neves et al. , 2011; Pichler et al. , 2014).

3.2.2. Knowledge scores for meat handlers in slaughterhouses

The results obtained within the group of meat handlers working in the slaughterhouses indicated that the correct answers were significantly related to the education (p < 0.001) and workers' previous participation in the food safety trainings (p < 0.001) (Table I). Meat handlers with elementary education scored lower (56 per cent) than those with the university degree (77 per cent). It is of note that the size of the slaughterhouses also had significant influence on the knowledge scores (p < 0.001), as workers from the enterprises with > 25 employees showed higher scores (70 per cent) compared to small enterprises with < 10 employees (53 per cent). This is expected as small companies have less workers that might be focused on specific aspects of food safety, and have limited in-house knowledge related to good hygiene practices and spread of food-borne diseases (Jianu and Chis, 2012; Pérez-Rodríguez et al. , 2010; Ramalho et al. , 2015; Walker et al. , 2003).

3.2.3. Knowledge scores for meat handlers in meat processing plants

The results obtained from the handlers in meat processing plants indicated that the knowledge scores were only associated at the significant level with education (p < 0.001), whereas other characteristics had no significant influence on the obtained scores (gender, age, work experience, participation in the food safety training or the number of employees in the meat processing plants, p > 0.05) (Table I).

3.2.4. Knowledge scores for meat handlers in retail stores

Analysis of the knowledge scores of meat handlers from retail stores confirmed significances related to the age (p =0.011). Similar with the slaughterhouses, the size of retail stores had significant influence on the knowledge scores (p < 0.001). Nevertheless, the obtained differences were completely opposite compared to handlers from slaughterhouses, as handlers from retail stores with > 25 employees showed significantly lower scores (56 per cent) compared to those from retail stores with < 10 employees (67 per cent). These results are somehow surprising, as it was expected that the greater the company the more attention is paid on training, but also on monitoring of good hygiene practices, that might result in better knowledge among workers. It is not known whether these results have been a consequence of rapid staff turnover in big retail stores.

3.3. Identifying knowledge gaps

3.3.1. Cross contamination

The majority of meat handlers were aware of potential transmission routes and bacterial contamination of meat, as more than 80 per cent of all meat handlers gave correct answer (Table II). Nevertheless, retail workers seem to be more conscious of bacterial transmission via raw foods and insects compared to other two groups of workers (p < 0.05). It seems that Serbian meat handlers were not able to distinguish among different health problems and the possibility to transmit hazards to the food they were working with. On one side, they correctly indicated that it is not allowed to handle food when having health problems (Table II), such as wounds on hands (95.3 per cent), vomiting (92.2 per cent), cold (87.8 per cent), cuts (85.5 per cent), diarrhoea (84.1 per cent) or raised fever (77.4 per cent). This is in accordance with previously published results obtained among Portuguese and Slovenian food handlers (Gomes-Neves et al. , 2011; Jevsnik et al. , 2008). On the other side, only 41.8 per cent of all meat handlers indicated that workers with hypertension are permitted to work in food production lines, as this serious health issue is not linked with microbial hazards. An opposite to this study, Jevsnik et al. (2008) reported that 85.7 per cent of all Slovenian food handlers knew that hypertension is not an obstacle important for food safety issues. Serbian meat handlers were not aware of the fact that protective mask serves as a barrier/protection of spreading microbial hazards, as only 34 per cent indicated that working with food wearing protective mask and coughing is allowed. These results are in accordance with previous findings obtained among food handlers in Slovenia (Jevsnik et al. , 2008).

Most of Serbian meat handlers involved in this study knew that raw and ready to eat meats should not share the same place in cooling units (90.5), same cutting boards (89.3 per cent) or same scales (87.2 per cent). This is especially important for meat handlers working in the retail stores, as they are most frequently in contact with both raw and ready-to-eat meats, and possible cross contamination. Although relatively high percentage of handlers gave correct answer, it was lower than reported in the UK (Walker et al. , 2003).

3.3.2. Temperature regime

Almost half of all meat handlers were not aware of the basic requirements related to temperature control and its influence on the behaviour of microbial hazards. The total of 49.6 per cent of all meat handlers knew that microorganisms can grow in the cooling units, although very slow. This is lower compared to findings reported by Jevsnik et al. (2008), who reported that 63.4 per cent of Slovenian meat handlers knew this important fact about microbial behaviour. Additionally, 57.9 per cent of Serbian meat handlers were aware of the fact that microorganisms can multiply at room temperature (25°C) and 50 per cent knew that microbial growth is stopped at temperatures below -18°C, but the bacteria remain viable and may grow, after defrosting, in favourable conditions. The legal requirements for the temperature control in cooling units (4-7oC), working environments ([< or =, slant]12oC) and inside red meat ([< or =, slant]7oC) (Serbia, 2011) have not been adequately accepted and acknowledged by the meat handlers, as they showed low percentage of knowledge in this area (22, 33 and 34.6 per cent, respectively). As expected meat handlers from the slaughterhouses and meat processing plants scored significantly better in comparison to retail, when asked about the temperature that is needed for the knife sterilization (p < 0.001). Knives are primarily contaminated through direct contact with surfaces that are heavily contaminated with bacteria, such as skin of slaughtered animals or intestinal contents. Therefore, to reduce bacterial load, all knives/tools that are used within the slaughter line, in the chillers and in the dressing and deboning area, must be cleaned and disinfected as soon as possible, using water bath with temperature of water being at least 82°C, as they might be possible source of contamination (Goulter et al. , 2008; Nørrung and Buncic, 2008). Gomes-Neves et al. (2011) previously reported that a greater percentage of Portuguese meat handlers (64.6 per cent) knew correct temperature of knife sterilization, compared to the findings in this study.

3.3.3. Hand hygiene

Considering meat handlers' knowledge on hand hygiene, almost all of them (above 90 per cent) were aware of the critical role of sanitary measures that should be taken in the work place such as a the need for washing hands after using toilette (99.1 per cent), handling garbage (97.7 per cent), touching money (97.1 per cent), blowing nose (96.8 per cent), handling raw foods (94.2 per cent) or eating and drinking (92.2 per cent). The reason for this might be that hand hygiene is the most often monitored operation and possible focus of previous trainings and communication between workers and food safety managers. Nevertheless, only 31.1 per cent of all meat handlers knew what is the minimal time needed for proper hand washing, as recommended by World Health Organisation (Jacob, 1989). Similar finding was determined in the survey performed among food handlers in catering and restaurants in Austria and Switzerland, when asked for minimal time needed for lathering soap during hand washing (Panchal et al. , 2013; Pichler et al. , 2014).

3.3.4. Knowledge about food products and food-borne diseases

Although, 57.9 per cent of workers correctly identified that bacteria will readily multiply at 25°C, with 41.7 per cent of retail workers and 68 per cent of meat processing plant workers answering this question correctly (p < 0.001), they do not understand the manifestation of bacterial growth and incidence in food. Our results indicated that the greatest gap and concerns in food safety knowledge was related to the identification of contaminated food. Only 5.5 per cent of all meat handlers knew that food contaminated with food poisoning bacteria cannot be recognized by visual, olfactory or taste checks (Table II). This is the lowest percentage of correct answer among all previous studies performed in the UK (Walker et al. , 2003), Slovenia (Jevsnik et al. , 2008) or Portugal (Gomes-Neves et al. , 2007; Gomes-Neves et al. , 2011), in which more than 40 per cent of food handlers knew the correct answer related to possible identification of contaminated food. The grossly contaminated and spoiled food can be easily detected by discoloration, odour or other degradation, while most types of food-borne microbial contamination leave no obvious clue, either visual, olfactory or tactile. In order to detect and recognise microbial cells in food, one needs to perform microbiological analyses. It is of note that only 0.9 per cent of meat handlers from retail stores answered this question correctly, and it is evident that those workers incorrectly rely on physical attributes as indicators of safe food, during their everyday performance.

The most of the respondents gave correct answer when asked about the possibility to transfer specific diseases such as diarrhoea via food ( > 60 per cent), whereas only 32 per cent of all handlers knew that abortion in pregnant women and mental disorders of newborns may be a consequence of food-borne diseases. This is of special importance for meat handlers operating in retail stores, as ready-to-eat meat products might contain Listeria monocytogenes , and this could potentially lead to spontaneous abortion in pregnant women. In line with this, the knowledge of the study population about microbiological food hazards very relevant for animal food products, such as Salmonella and Escherichia coli O157:H7 was generally low (Table II). Similar was found earlier in the studies performed in Iran (Ansari-Lari et al. , 2010), Turkey (Tokuç et al. , 2009) and Portugal (Gomes-Neves et al. , 2007; Gomes-Neves et al. , 2011). The best results were determined for the association between Salmonella and eggs (87 per cent of correct answers), probably due to the often publicly shown and emphasised food-borne outbreaks in previous years (Altekruse et al. , 1996; Angelillo et al. , 2000).

4. Conclusion

This survey provides very important information on the level of food safety knowledge among Serbian meat handlers and difference/gaps in the knowledge among workers from different roles within the meat chain (slaughtering, processing and retail). This is of special importance, as these results might serve as a base for further improvement in the knowledge and training/educational material and emphasize the need for continuous food safety training among meat workers. It is crucial for all meat handlers to receive adequate and focused food safety training that will cover most important factors that contribute to food-borne outbreaks (cross contamination, time/temperature abuse during storage of ingredients or products, insufficient heat treatment and meat handlers' hands being one of crucial vectors for microorganisms). It is often assumed that the training leads to knowledge based changes in attitudes and practices on site. Nevertheless, several authors questioned if these trainings will result in assumed food handling changes (Bas et al. , 2006). Reasons for this might be found in the fact that the food handlers are often recruited from lower socio-economical class and subsequently with lower initial education, rapid staff turnover and poor motivation due to the low payment and condense job assignments (Soon et al. , 2012). Pellegrino et al. (2015) discussed several motivational models for improving hand hygiene. Clayton et al. (2002) indicated that trained food handlers had identified many barriers to implement obtained food handling information, such as lack of time, lack of staff and a lack of resources. Additionally, food handlers often underestimate themselves and the risk of their own role in the safety of meat and meat products. Therefore, it is not only the food safety knowledge that should be obtained through the risk-based food safety training, but also the change of company culture arising from the management in meat establishments. Additionally, food safety managers should be proactive and dedicated in both supervising meat handlers activities and on-site correcting/training of handlers in order to improve and advance food and handlers hygiene.

Table I Characteristics of meat handlers and knowledge scores

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Table II Frequencies of correct answers to food safety knowledge questions of all meat handlers in Serbian meat industry

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Fixed Table I

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Fixed Table II

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Fixed Table III

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Appendix

Fixed Table I

Fixed Table II

Fixed Table III

Corresponding author

Dr Nada Smigic can be contacted at: [email protected]

References

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Further reading

Greig, J.D., Todd, E.C.D., Bartleson, C.A. and Michaels, B.S. ( 2007 ), " Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 1. Description of the problem, methods, and agents involved ",Journal of Food Protection , Vol. 70 No. 7, pp. 1752 - 1761 .