The level of food safety knowledge in food establishments in three European countries

Food Control 63 (2016) 187e194

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The level of food safety knowledge in food establishments in three European countries Nada Smigic a, *, Ilija Djekic a, Margarida Liz Martins b, c, Ada Rocha b, c, Nikoleta Sidiropoulou d, Eleni P. Kalogianni d a

Food Safety and Quality Management Department, University of Belgrade, Faculty of Agriculture, Belgrade, Serbia Faculty of Nutrition and Food Sciences, University of Porto, Porto, Portugal LAQV@REQUIMTE, Porto, Portugal d Department of Food Technology, Alexander Technological Educational Institution of Thessaloniki, Thessaloniki, Greece b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 July 2015 Received in revised form 9 November 2015 Accepted 12 November 2015 Available online 18 November 2015

This study was performed with the aim to investigate and compare the level of food safety knowledge among food handlers in three different countries, Serbia, Greece and Portugal, in different food establishments, namely restaurants, take-away places and catering companies. Total of 377 food handlers were involved in this study with 115 food handlers from Serbia (30.5%), 180 food handlers from Greece (47.7%) and 82 food handlers from Portugal (21.8%). For each participant, the knowledge score (KS) was calculated by dividing the sum of correct answers by the total number of questions. The average KS for all participants was 70.5%, with best overall KS that was obtained for Portuguese food handlers (72.6%), followed by Serbian (71.3%), whereas Greek food handlers showed lower scores (69.1%, p < 0.05). The biggest knowledge gaps that have been identified in relation to temperature control, source of contamination of foods and food-stuffs and high-risk foods can be used as a foundation for further improvements in food safety trainings. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Food safety knowledge Food handlers Restaurants Take-away Catering

1. Introduction The number of food-borne outbreaks worldwide remains at a very high level, despite the various studies performed in the field of food safety followed by a number of preventive and control measures that were recommended and implemented in the food industry, the catering sector and food service (Havelaar et al., 2010). During 2013, the European Food Safety Authority and the European Centre for Disease Prevention and Control reported 5196 foodborne and water-borne outbreaks with 43,183 human cases, 5946 hospitalisations and 11 deaths in the European Union (EU). Among these, 22.2% of outbreaks were associated and/or occurred in restaurants, cafes, pubs, bars and hotels (EFSA & ECDC, 2015). According to the report of Serbian National Institute of Public Health, there were 114 food-borne outbreaks with 948 human cases and no deaths in Serbia during 2013 (NIPHS, 2014). Although this report does not give an information on the number of outbreaks that occurred in restaurants, pubs or cafes, media often reported cases

* Corresponding author. E-mail address: [email protected] (N. Smigic). http://dx.doi.org/10.1016/j.foodcont.2015.11.017 0956-7135/© 2015 Elsevier Ltd. All rights reserved.

connected with the consumption of food in take-away places or food prepared in catering services (Radovic, Kekovic, & Agic, 2014). This underlines the need for the investigation of the level of food safety knowledge and knowledge gaps among food handlers in order to design appropriate educational and training programmes. Food handlers have direct contact with food and they play a very important role in the prevention of food contamination. From the research conducted so far, many different factors, such as inadequate cooking, improper time/temperature control and cross contamination have been implicated in food-borne outbreaks. The contribution of infected food handlers on these cases is difficult to establish, although their role in transmission of food-borne pathogens to the public during food preparation is well known and main cause lies in the lack of adequate food safety knowledge (Greig, Todd, Bartleson, & Michaels, 2007). They may crosscontaminate raw and processed products, ready-to-eat (RTE) foodstuffs and therefore they may introduce food-borne pathogens such as hepatitis A virus, noroviruses, Salmonella, Staphylococcus aureus, Listeria monocytogenes, Escherichia coli O157H7 or Campylobacter jejuni into the food chain (Bolocan et al., 2015; Chai et al., 2008; Osaili et al., 2014; Tang et al., 2011; Todd, Greig,

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Bartleson, & Michaels, 2008). The most often reported food handlers' errors which resulted in subsequent outbreaks, were handling of food by an infected person or by a person carrying a food-borne pathogen, bare-hand contact with food, improper hands washing practices and insufficient cleaning of processing or preparation equipment (Nørrung & Buncic, 2008; Todd, Greig, Bartleson, & Michaels, 2007). Personal hygiene and good hygiene practices present the major preventive actions for pathogen transmission from food handling personnel to the final consumer. Therefore adequate training and effective transfer of knowledge in behaviour changes may help in improving food handling practices on site and reducing the resulting negative effects of contamination on health and economy. Along with training, other factors such as age, education or work experience may affect the level of food safety knowledge (Angelillo, Viggiani, Rizzo, & Bianco, 2000; Jev
snik, Hlebec, & Raspor, 2008; Panchal, Bonhote, & Dworkin, 2013; Pichler, Ziegler, Aldrian, & Allerberger, 2014). European legislation on food hygiene requires and emphasize the need for food safety trainings in all EU countries. All food business operators are required to ensure that all their staff engaged in food handling activities are suitably trained and/or instructed in food hygiene, as stated in the European Regulation (EC) No 852/2004. The necessary food safety skills may be obtained through formally organised training courses or through internal trainings and self-study. In Greece, the Hellenic Food Safety Authority provides minimum acceptable context of food safety trainings, and approves organizations that may provide training. The context of the training follows requirements given in the EU Regulation (EU, 2004), while details are given by ministerial order No. 14708, which was adopted in 2007. In Portugal, the catering companies are responsible to organize and train their own employees and on food safety and the control is leased to private food safety companies. Official control is performed by the Portuguese Food Safety and Economic Authority. Employees from other food service establishments, such as take-away places and restaurants do not attend training courses in regular basis. Regarding Serbia, food safety system is widely reorganized to comply with European legislation (Smigic, Rajkovic, Djekic, & Tomic, 2015). The requirements for mandatory trainings on personal hygiene and food hygiene is given within Food safety law (Serbia, 2009), while rules for organisation of these trainings are given in a separate legal act (Serbia, 2010). Although the Ordinance was adopted and put in force in 2010, its full implementation has experienced some constraints, since the responsibility for the trainings is under the jurisdiction of the Ministry of Health with limited number of employees being available to provide trainings in different food establishments, including take away places, restaurants and catering services. The knowledge on food safety issues and level of practical training on hygienic handling of food are very important to protect the consumers health (Gomes, Lemos, Silva, Hora, & Cruz, 2014). This is of particular significance for the production and direct distribution of food to the final consumer, as it is in restaurants, takeaway and catering services. In previous years, different studies have been performed in order to investigate the level of food safety knowledge among handlers that work in restaurants and catering services (Bas¸, S¸afak Ersun, & Kıvanç, 2006; Jev
snik et al., 2008; Panchal, Carli, & Dworkin, 2014; Panchal et al., 2013; Pichler et al., 2014; Sun, Wang, & Huang, 2012). Nevertheless, a lack of information persists related to food safety knowledge among food handlers employed in food service sector in Serbia and Greece, with limited studies coming from Portugal. Therefore, the first aim of this study was to investigate and compare the level of food safety knowledge among food handlers in three different countries, Serbia, Greece and Portugal, in different food establishments,

namely restaurants, take-away places and catering companies. The second aim of the study was to identify the major gaps in the knowledge among food handlers in order to improve food training material. 2. Material and methods 2.1. Characteristics of food handlers This survey was conducted during the period between JuneeDecember 2014. A total of 377 food handlers from different food establishments were included in this survey. These workers were employed by restaurants, take-away and catering establishments. Restaurants' main activity is to serve complete and varied menus. Caterings are food establishments that prepare food in a stationary kitchen and then transport food to different sites. Takeaway places' main activity is to serve fast food, pastry, soft drinks and/or juices. Independently owned food establishments were selected randomly to represent all three types of establishments. Data was collected by visiting various food establishments in the three countries, during different shifts to avoid sampling bias. Managers of food establishments were asked to give interviewers permission to access the establishments and distribute the questionnaires to workers/food handlers. In order to answer the questions, the questionnaire was distributed to staff present at the time of visit. The categories of food handlers that participated in this survey is shown on Table 1. A self-administrative questionnaire was used and face-to-face interview was performed to ensure the accuracy of the answers and completeness of the questionnaire. The purpose of the study and instructions for completing the questionnaire were initially explained to food handlers by the interviewer. One author from each country trained and recruited students of master studies from the three universities to perform interviews. All students had appropriate food safety knowledge as a result of their previous studies. In total seven interviewers were used, three from Portugal, three from Serbia and one from Greece. Questionnaires were translated from English language to Greek, Portuguese and Serbian languages. 2.2. Questionnaire The questionnaire was prepared from previously performed studies (Gomes-Neves, Cardoso, Araújo, & Correia da Costa, 2011; Jev
snik et al., 2008; Walker, Pritchard, & Forsythe, 2003). It was designed to obtain information about food handlers' knowledge related to cross-contamination, cooling, cooking, cleaning and food poisoning, with a total number of 30 questions. Additionally, questionnaire included questions related to the demographic characteristics of food handlers (gender, age, education level, experience in foodservice operations, experience at the current work place, participation in food safety trainings) and food establishments (type of food establishments and number of employees). Three types of questions were used in the questionnaire, giving the possibility to answer either true/false, yes/no or multiple choice questions. Additionally, food handlers had the possibility to answer “I don't know” for each question, to minimize the possibility to select the correct answer randomly. 2.3. Data analysis For each food handler that participated in this study, the knowledge score (KS) was calculated by dividing the sum of correct answers by the total number of questions. KSs were analysed using an independent sample t-test (for two groups, such as gender) or

N. Smigic et al. / Food Control 63 (2016) 187e194

189

Table 1 Characteristics of food handlers and knowledge scores. Overall (n ¼ 377) N (%)

KSx

Withiny p-value

Age

Education

Total work experience in food sector

Work experience at the current placae

Food safety training courses

Current food establishment

Number of employees at current food establishment

Male

173 (45.9%) Female 204 (54.1%) <24 55 (16.4%) 25e34 88 (26.2%) 35e44 83 (24.7%) 45e54 55 (16.4%) >55 55 (16.4%) 54 Elementary school (16.1%) High school 156 (46.4%) College 68 (20.2%) University 58 degree (17.3%) <2 years 86 (25.6%) 2-8 years 127 (37.8%) 8-16 years 61 (18.2%) >16 years 62 (18.5%) <2 years 173 (51.5%) 2-8 years 104 (31.0%) 8-16 years 31 (9.2%) >16 years 28 (8.3%) Yes, organised by 80 Ministry (23.8%) Yes, organised by 173 others (51.5%) No 83 (24.7%) Restaurant 122 (36.3%) Fast food 107 (31.8%) Catering 107 (31.8%) 10 employees 145 (43.2%) 10- 25 100 employees (29.8%) 25 employees 91 (27.1%)

70.0

0.535

70.6 70.0

ab

71.1

ab

0.023*

70.6ab 71.9b 67.6 69.7

a

0.287

71.2 69.4 69.8 69.8

0.786

70.5 70.9 70.1 69.8

0.353

71.1 71.5 69.3 71.2

0.286

69.7 70.8 70.8

0.389

70.0 70.6 70.6 69.9 70.5

N (%)

0.787

40 (34.8%) 75 (65.2%) 16 (13.9%) 31 (27.0%) 32 (27.8%) 22 (19.1%) 14 (12.2%) 4 (3.5%) 88 (76.5%) 17 (14.8%) 6 (5.2%) 45 (39.1%) 30 (26.1%) 20 (17.4%) 20 (17.4%) 79 (68.7%) 16 (13.9%) 11 (9.6%) 9 (7.8%) 18 (15.7%) 56 (48.7%) 41 (35.7%) 30 (26.1%) 31 (27.0%) 54 (47.0%) 56 (48.7%) 11 (9.6%) 48 (41.7%)

70.0A 72.1A 68.6

a

70.0

abA

73.6bA 70.4ab 73.3

b

70.1

0.088

106 (58.9%) 74 (41.1%) 0.048* 35 (19.4%) 58 (32.2%) 34 (18.9%) 20 (11.1%) 33 (18.3%) 0.319 5 (2.8%)

68.6 73.3 71.0

0.314

72.4A AB

69.0 71.6

0.163

72.6

AB

70.9

AB

66.0 68.7A 72.2

AB

71.1 69.0a 69.0

aA

73.3

bA

68.9aA 68.8a 74.6

bA

KS

0.170

43 (23.9%) 61 (33.9%) 71 (39.4%) 38 (21.1%) 84 (46.7%) 31 (17.2%) 27 (15.0%) 97 (53.9%) 60 (33.3%) 9 (5.0%)

68.7A 0.416 69.6B 69.6 0.840 A

69.0

68.2B 69.1 70.1 67.2 0.047 69.5A 67.1 70.7 70.9 0.359 68.8B A

68.6 67.8

69.5 0.814 A

69.0

A

67.5

14 68.0 (7.8%) 62 68.0A 0.163 (34.4%) 118 69.0A (65.6%) 0 (0.0%) 0.0

0.001* 60 (33.3%) 60 (33.3%) 60 (33.3%) 0.000* 67 (37.2%) 83 (46.1%) 30 (16.7%)

Portugal (n ¼ 82)

Within p- N (%) value

180 69.1B (47.7%)

71.7A

72.5

Greece (n ¼ 180)

Within N (%) pvalue

KS

115 71.3A (30.5%)

377 70.5 (100%) Gender

Serbia (n ¼ 115)

68.7 0.193 A

68.1

B

70.5

68.3A 0.092 70.4 B

67.3

Withinz p-value

KS

82 72.6A (21.8%) 27 (32.9%) 55 (67.1%) 11 (13.4%) 16 (19.5%) 27 (32.9%) 16 (19.5%) 12 (14.6%) 45 (54.9%) 32 (39.0%) 3 (3.7%) 2 (2.4%) 14 (17.1%) 30 (36.6%) 19 (23.2%) 19 (23.2%) 22 (26.8%) 41 (50.0%) 11 (13.4%) 8 (9.8%) 15 (18.3%) 25 (30.5%) 42 (51.2%) 32 (39.0%) 16 (19.5%) 34 (41.5%) 38 (46.3%) 22 (26.8%) 22 (26.8%)

Between p-value

0.000*

72.6B 0.972

0.050*

72.7A

0.016*

69.7

0.094

0.855

B

0.010*

73.6A

0.002*

72.2

0.468

72.2

0.38

74.5

71.4

0.134

0.302

74.0B

0.039*

74.2

0.189

78.4

0.218

69.5a

0.007*

72.6abA 76.1

0.010*

bB

0.008*

71.6ab 71.5

0.763

0.099 0.123

0.086

73.0

B

0.018*

75.6

B

0.018*

70.0

0.704

73.5B 0.514 73.3

B

0.048* 0.008*

71.9

0.603

71.7

0.345

0.135

74.3

B

0.007*

72.8

AB

0.033*

73.3B 0.783

0.016*

72.5

0.278

73.4

A

0.000*

*Statistical significance p < 0.05. x Knowledge score, relative percentage which is based on valid values. y Differences within the characteristics of food handlers. z Differences between food handlers in Serbia, Greece and Portugal. Items denoted with the same small letter are not significantly different within the group and items denoted with the same capital letter are not significantly different between the groups.

analysis of variance (ANOVA) with post-hoc Duncan test (for more than two groups, such as age, level of education, experience in food sector or participation in food safety training.

Additionally, data were analysed to identify knowledge gaps among food handlers and for that purposes chi-square test was used to compare the percentage of correct responses to each

190

N. Smigic et al. / Food Control 63 (2016) 187e194

question across the countries (Serbia, Greece and Portugal). Values with a p < 0.05 were considered statistically significant. All statistical processing was performed using Microsoft Excel 2010 and SPSS Statistics 17.0. 3. Results 3.1. Sample characteristics Total of 377 food handlers were involved in this study. Among them, 115 were food handlers from Serbia (30.5%), 180 food handlers were from Greece (47.7%) and 82 food handlers were from Portugal (21.8%). The number of male and female participants were 45.9 and 54.1%, respectively (Table 1). The majority of food handlers (52.6%) involved in this study aged between 24 and 45 years, whereas the similar share was found for other age groups (approx. 15%). The mean age of all participants was 36 years, with the youngest participant being 18 years old and the oldest 71 years old. The total of 57.5% of all participants had finished elementary and high school, whereas 42.5% had either college or university degree, those mainly working in Greek food establishments. Regarding work experience in the food sector, 144 (38.2%) of all participants had between 2 and 8 years of work experience, 97 (25.7%) <2 years and 70 (18.6%) had between 8 and 16 years of work experience. The total of 294 (78%) food handlers had participated in some food safety trainings, organized by either governmental institution responsible for food safety issues or various training providers. It is of note that 83 (22%) participants had no training related to food safety at all and half of them are employed in Serbian and the other half in Portuguese food establishments. All Greek participants had previously participated in some kind of food safety training. Food handlers involved in this study were employed in restaurants (32.4%), take-away (28.4%) and catering companies (39.3%). Finally, 42.7% of all participants were employed in food establishments with <10 employees, 30.8% in establishments with 10e25 employees and 26.5% in establishments with >25 employees, as presented on Table 1. 3.2. Knowledge scores The overall KS for all food handlers who participated in this study was 70.5%. The best overall KS was obtained by Portuguese food handlers (72.6%), followed by the Serbian (71.3%), whereas Greek food handlers showed lower scores (69.1%, p < 0.05). This order of KS and significant differences were also seen for individual group of participants (males, females, different age groups, different education groups, etc.) as presented on Table 1. Overall, the knowledge score among all food handlers involved in this study was significantly associated with the age of participants, education, type of food establishments and number of employees (p < 0.05) (Table 1). The youngest participants aged <24 years had the lowest KS, although no statistical significant difference among different age groups was found. Our results indicated that food handlers holding college degree had the lowest knowledge scores (69.4%) which was different from those with elementary, high school or university (69.7, 71.2 or 69.8%, respectively, p < 0.05). Additionally, the overall knowledge scores showed that there is no effect of previous participation in the food safety training (either organized by governmental or other training providers) (p > 0.05). Food handlers from the enterprises with >25 employees had average scores of 70.5%, medium (10e25 employees) had 69.9% and small enterprises (<10 employees) 70.6%. In order to evaluate whether the reason for these results are related to different countries that were involved in this study, we have separately analysed KS within each country. The results

within the group of food handlers from Serbia indicated that the number of correct answers was significantly related to workers' age (p < 0.05), the type and the size of food establishment where they were working in (p < 0.05, Table 1). Serbian food handlers that worked in catering service showed average KS of 73.3%, that was higher than those working in restaurants and take-away places with an average KS of 69.0 (p < 0.05). Additionally, the size of Serbian food establishments also had a significant influence on KS (p < 0.05), as workers from the enterprises with >25 employees scored higher values (74.5%) compared to medium (10e25 employees) and small enterprises (<10 employees) (69.8 and 68.9%, respectively). The overall KS among Greek food handlers was 69.1% and none of investigated characteristics had a significant influence on the obtained KS (gender, age, work experience or the number of employees in the food establishment, p > 0.05) (Table 1). The Portuguese food handlers showed overall high KS of 72.6%, which is significantly related only to the work experience in the food sector (p < 0.001). The workers employed in the food sector between 8 and 16 years seems to have better knowledge (76.1%), compared to those being in food sector for only 2 years (69.5%). 3.3. Knowledge gaps The most often identified factors contributing to food-borne outbreaks included inadequate temperature control, infected food handlers and bare hand food manipulation, contaminated raw ingredients, cross-contamination and inadequate heat treatment during food preparation (Bryan, 1988; Rooney et al., 2004; Todd et al., 2007). The level of food handlers' knowledge and gaps related to these critical food safety issues were further investigated. 3.3.1. Temperature control We have observed that merely 66.4% of all food handlers knew that bacteria readily multiply at room temperature (25  C) and therefore keeping food products at this temperature might lead to microbial growth in food products. In addition, only 53.7% of all food handlers identified that microbial growth is stopped at the temperatures below 18  C, and that bacteria remain viable and may grow after defrosting in favourable conditions. When asked what is the required temperature inside the refrigerator, 81.9% of all food handlers correctly answered that the temperature should be below 8  C. Nonetheless, knowledge is still very limited in this area, as only 40.5% of them answered that given temperature of 13  C is not adequate for cold storage of food. Chilling of cooked foods should be performed as fast as possible to prevent microbial proliferation and/or toxins production. One of the possible approaches is to separate cooked food in small portions, to fasten up chilling process. Our results indicated that 60% of participants were aware of this good practice. The total of 69.5% and 69.4% of Portuguese and Serbians, respectively, was aware of this, while significantly lower percentage (50.6%) was seen for Greek participants (p < 0.05). If the cooked RTE food has to be served hot, it must be held at 63  C in suitable temperature control equipment. Almost half of Serbian food handlers (49.0%) responded correctly when asked what is the minimal allowed temperature for keeping thermally treated warm food, while 41.5 and 41.2% of Greek and Portuguese gave correct answer, respectively (p < 0.05). The total of 20.5% of correct answers was found when participants were asked about the importance to measure internal temperature during thermal food preparation. Only 6.7 and 9.4% of Serbians and Greeks, respectively, realized that the reason for measuring internal temperatures is related to killing harmful pathogens, while 68.1% of Portuguese correctly answered this question (p < 0.001).

N. Smigic et al. / Food Control 63 (2016) 187e194

3.3.2. Cross contamination Our results showed that 92.0% of all food handlers knew that raw and cooked food should be stored separately to prevent bacterial transfer. Even though >90.0% of participants knew the reason for separate storage of raw and RTE food, it seems that they did not completely understand what division and separate storage means in practice, as only 73.0% of them was aware that raw meat should be stored in the refrigerator below bean salad (RTE food), to avoid cross contamination. Almost 40% of Serbian, 30% of Greek and 5% of Portuguese handlers operating in the food service did not answer this question correctly (p < 0.05). A great number of respondents knew that food handlers (91.0%), raw food (85.1%) and insects (82.8%) can be the vehicle for transferring food-borne pathogens to food (Table 2). Nevertheless, 15.0% of Greek participants was not aware that food handlers themselves can be potential cause and transferring route for food contamination, which was significantly different from Serbian and Portuguese food handlers (p < 0.05). Among all food handlers, 90.2% knew the right procedure for washing cutting boards, while only 68.3% knew how to properly wash cutting knives after raw meat preparation. The smallest percentage of correct answers was seen in the group of Portuguese food handlers (34.6%) and that was significantly lower when compared to Serbian and Greek participants (85.1 and 72.8%, respectively, p < 0.05). Total of 82.6% of all food handlers knew that vegetables splashed with raw chicken juice should not be rinsed and used for sandwich preparation, but discarded, as poultry meat presents one of the most significant routes for the transmission of food-borne pathogens, such as Campylobacter and Salmonella in domestic and , 1990; Elizabeth, Christopher, catering kitchens (Boer & Hahne Jenny, & Tom, 2004). Additionally, 95.6% of all food handlers correctly answer that picking ice with bare hands is not allowed by good manufacturing practices in the kitchen. 3.3.3. Food handling and health problems/personal hygiene It seems that food handlers from the three European countries, were not able to distinguish different health problems and the possibilities to transmit pathogens to food they were working with. On one side they correctly indicated that it is not allowed to handle food when having health problems (Table 2), such as vomiting (93.7%), wounds on hands (93.4%), cuts (89.8%), cold (88.6%) diarrhoea (80.9%) or raised fever (71.3%). Nevertheless, our results indicated that almost 30.5% of all food handlers were not aware that hypertension, in spite of being a very serious illness, is not connected with food-borne pathogens and therefore people suffering from hypertension are allowed to work in food production and service. There was significantly greater percentage of food handlers from Portugal (95%) that correctly answer this question, compared to handlers from Greece and Serbia (60.4 and 63.3%, respectively, p < 0.05). Almost half of all food handlers involved in this study was not aware of the fact that a protective mask serves as a barrier/ protection of spreading microbial pathogens (Table 2). Again, Portuguese food handlers showed significantly better performance than Greeks or Serbians on this question (p < 0.05). Nevertheless, when participants were asked if they can handle food when suffering of diarrhoea, which is one of the most frequent symptoms of food-borne diseases, only 64.2% of Portuguese food handlers answered correctly, which was significantly lower than in the cases of the Greek or Serbian food handlers (81.8 and 87.8%, respectively, p < 0.05). Considering food handlers' knowledge on hand hygiene, most of them (average value above 90.0%) were aware of the requirement for washing hands after handling waste (98.4%), using toilette, handling raw food or blowing nose (97.0%) or eating and drinking

191

(90.4%). This outcome is most probably a consequence of the fact that hand hygiene is the most often monitored operation and possible focus of previous trainings and communication between food handlers and food safety managers. It is of note that at all times, significantly lower percentage of Greek food handlers correctly answer questions related to hand hygiene compared to the Serbian or Portuguese ones (Table 2). 3.3.4. Food products and related food-borne diseases Substantial food safety knowledge gaps were identified when food handlers were asked about food products and related foodborne diseases. Actually, only 36.3% of food handlers knew that smelling, tasting or visually checking food is not a appropriate to evaluate food safety. Our results showed that 45.8% of all food handlers could identify UHT milks as a sterile food. Nevertheless, it is of note that about the same percentage of all food handlers (45.0%) answered that pasteurized milk is a sterile food. Our results indicated that >70% of participants knew that food such as beef, eggs or poultry, when not properly cooked, can cause serious food-borne diseases. Among them, only 55.6% of Greek respondents knew that undercooked beef might be dangerous for the consumption, which was significantly lower than Serbians or Portuguese respondents (93.5 and 73.2%, respectively, p < 0.001). What seems to be very worrying is the fact that only 27.2% of food handlers knew that there is a serious microbial risk associated with cooked rice (Table 2), with Portuguese respondents showing significantly lower percentage (10.3%) of correct answer compared to Serbian or Greek (20.9 and 35.5%, respectively with p < 0.001). 4. Discussion The overall level of food safety knowledge among food handlers working in three European countries, namely Serbia, Portugal and Greece was determined in this study, by calculating knowledge scores (KS). The average KS for Portuguese food handlers was 72.6%, followed by Serbian, 71.3%, whereas Greek food handlers showed significantly lower scores (69.1%, p < 0.05). Several studies have reported lower KS values than KS obtained in this study. For example, in the study performed in catering company which manufactures and distributes meals to the canteens of schools, kindergartens and nursing homes in Portugal (Martins, Hogg, & Otero, 2012), the average percentage of correct answer was 56.5%, while Gomes-Neves, Araújo, Ramos, and Cardoso (2007) reported the average score of 62.9% for Portuguese food handlers employed in small businesses. On the other hand, results from this study were lower than results reported for Austrian food handlers working in restaurants and catering companies, with KS being 76% (Pichler et al., 2014). The differences that were observed between our results and other studies may also be influenced by different method of data collection. Although statistically significant difference could be seen among participants from Portugal, Serbia and Greece, the importance of such difference is in certain level decreased when looking into the knowledge gaps among food handlers. For some questions the smallest percentage of correct answer was seen among Serbian food handlers, while for others this was on the side of Portuguese or Greek participants. Therefore, the way of evaluating the food safety knowledge should not only rely on determination of the average knowledge scores, as a percentage of correct answer among all asked questions. It is more important to identify the most critical area for improvements, after identification of deficiency and shortage in specific important area of food safety. By doing this, one will be able to make very concrete, specific and targeted training material, which should improve the current food safety knowledge.

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Table 2 Frequencies of correct answers to food safety knowledge questions in three countries. Question

Correct answers (%) Overall (n ¼ 377)

Cross-contamination The reason for storing raw and cooked food separately. Good practice of storing raw meat and bean salad in the same refrigerator. The possibility of storing raw meat anywhere in the refrigerator when tightly sealed in plastic film. Possible route of transferring food-borne pathogens: Food handlers, Raw food (raw meat, raw eggs, raw vegetables, etc.), Bread and bakery products, Insects. Vegetables for a salad splashed with a few drops of raw chicken juice can be rinsed with water and further used for food preparation. Good practice after using the cutting board for cutting raw foods. Good practice after using the knife for cutting raw meat. Good practice of putting ice cubes in glass: Using tongs, Using an ice scoop, Scooping ice into the ice cubes, Picking ice cubes with bare hands. Good practice of thawing food. Temperature regime Food handlers' reaction when food is delivered at inadequate (too high) temperature. Optimal temperature for bacterial multiplication. Bacterial behaviour at chilled temperatures. Required temperature inside refrigerator. Given temperature of 13 C is allowed for chilled storage of cold food. Good practice of portioning hot food in smaller portions when chilling. Maximum period for keeping cooked food at chilled 4  C. Minimal allowed temperature for keeping thermally processed warm food. Why it is important to measure internal temperature during thermal food preparation? Maximal tolerable temperature during oil or fats heating. Good practice and frequencies of changing oil or fats used for heating. If fish has been stored at temperature that is too warm, but then it is properly cooked to the correct internal temperature, it becomes safe to eat. Food handling and health problems May handle food when: …having a diarrhoea …having hypertension …having a cold …having a toothache …coughing and wearing protective mask …having raised temperature …vomiting …I had cut myself …wearing nail polish …I am upset …having wounds on my hands Good practice when handler had an open cut on his finger and working on ready to eat food preparation. Hand hygiene Washing hands is mandatory after… …handling raw foods …using the toilet …touching money …handling garbage …blowing nose …eating or drinking Food and food-borne diseases Identification of food contaminated with food-borne pathogens. Identification of cooked food that might cause food-borne disease. Identification of food that might cause food-borne disease if not properly cooked. Beef Eggs Carrots Poultry Identification of sterilized food. Foodstuffs frequently implicated in Salmonella food poisoning: Eggs Dairy Fish Chicken meat Potato puree Common symptoms of food-borne diseases. *Statistical significance p < 0.05.

Serbia (n ¼ 115)

Greece (n ¼ 180)

Portugal (n ¼ 82)

pvalue

92.2 73 50.7

88.8 60.4 59.1

92.2 71.2 48.3

96.3 94.9 44.2

0.181 0.000* 0.090

91 85.1 64.9 82.8 82.6

100 88.3 45.2 90.5 75.5

83.9 81.7 80.6 74.4 85

95.1 88.9 47.5 92.5 86.3

0.000* 0.188 0.000* 0.000* 0.08

90.2 68.3

90.4 85.1

89.4 72.8

91.5 34.6

0.091 0.000*

91.7 81.8 89.5 96.8 18.2

99.1 95.6 55.6 91.1 13.9

87.2 71.7 96.1 97.8 20.0

91.5 88.9 82.1 100 19.8

0.002* 0.000* 0.000* 0.004* 0.000*

52 66.4 53.7 81.9 40.5 60 90.5 43.9 20.5 51.9 49.9 66.7

32.2 67.3 47.7 79.5 32.3 69.4 93.5 49 6.7 55.6 47.4 71

56.1 66.5 52.8 80 49.4 50.6 85 41.5 9.4 36.1 60.6 65

71.3 64.9 63.8 89.7 29.9 69.5 98.8 41.2 68.1 85.3 29.1 65

0.000* 0.000* 0.000* 0.000* 0.002* 0.001* 0.000* 0.000* 0.000* 0.000* 0.000* 0.557

80.9 69.5 88.6 73.9 53 71.3 93.7 89.8 91.3 69.6 93.4 87.9

81.8 60.4 91.7 63.1 41.9 73.6 92.2 85.6 88.8 65.7 92.5 91.6

87.8 63.3 92.2 71.7 48.9 74.4 93.9 93.3 90.6 59.4 97.2 85

64.2 95 76.3 92.6 76.5 61.3 95.1 87.5 96.3 97.5 86.3 90.1

0.000* 0.000* 0.000* 0.000* 0.000* 0.078 0.716 0.084 0.172 0.000* 0.004* 0.222

97.6 97.9 95.2 98.4 97.3 90.4

99.1 100 99.1 100 99.1 97.4

95.6 95.6 91.7 96.7 95 83.3

100 100 97.6 100 100 96.3

0.041* 0.011* 0.008* 0.036* 0.024* 0.000*

36.3 27.2

20.9 25.5

48.9 35.9

28.9 10.3

0.000* 0.000*

70.5 82.3 91.7 95.6 45.8

93.5 93.4 77.3 98.1 48.5

55.6 72.2 95.6 96.1 43.3

73.2 90.1 98.8 91.5 48.6

0.000* 0.000* 0.000* 0.079 0.000*

85.8 47.4 57.6 85.7 82.4 90.8

97.1 70.6 45.8 93.6 72.7 89.2

75.6 31.7 68.3 90 96.1 90

93.9 58.4 43.6 67.1 59.5 94.8

0.000* 0.000* 0.000* 0.000* 0.000* 0.017*

N. Smigic et al. / Food Control 63 (2016) 187e194

Thus, we have also determined major gaps in food safety knowledge. Results indicated that there is a lack of adequate knowledge related to adequate temperature for cooking, storing or holding food. Temperature is one of the most important factors in controlling microbial growth and survival in foods. At the same time, temperature abuse and inadequate temperature control is one of the most often identified factors contributing to food-borne outbreaks (Bryan, 1988; Rooney et al., 2004; Todd et al., 2007). Although majority of food handlers knew what is the required temperature inside the refrigerator, only 40.5% of them answered that given temperature of 13  C is not adequate for storing cold food. It seems that participants still do not completely understand cold storage and its influence on microbial activities, as more than half of food handlers still think that 13  C is appropriate temperature for cold storage. Food-borne pathogens might be directly transferred from raw food to RTE food, but also indirectly from raw food to kitchen surfaces, food handlers or utensils and further to RTE food. Additionally, pathogens might survive for prolonged period of time on food contact materials, cloths and hands, which may lead to increased risk due to cross contamination. The proper washing practices of kitchen facilities and utensils performed with hot water, detergents and disinfectants is one of the essential preventive measures to avoid bacterial transfer and cross contamination (Ravishankar, Zhu, & Jaroni, 2010). Although this is well known and these practices were often recommended, it is still not understood by all food handlers in this study. Our results indicated that 90.2% of all food handlers knew the right procedure for washing cutting boards, while only 68.3% knew how to properly wash cutting knives after raw meat preparation. Substantial food safety knowledge gaps were identified when food handlers were asked about food products and related foodborne diseases. Actually, only 36.3% of food handlers knew that smelling, tasting or visually checking food is not a guarantee that food is safe. This is one of the most concerning knowledge gaps determined not only in this study is in line with previous findings by other authors (Gomes-Neves et al., 2007; Gomes-Neves et al., 2011; Jev
snik et al., 2008; Martins et al., 2012; Pichler et al., 2014; Walker et al., 2003). Besides heavily contaminated and spoiled food that can be easily detected by discolouration, odour or other changes, most types of food-borne microbial contamination leave no obvious clue, either visual, olfactory or tactile. Results of microbiological analyses are needed to detect and recognise microbial pathogens present on food. It is very important that food handlers were able to identify high risk food products that might allow pathogenic survival or even multiplication. As the food-borne pathogens such as E. coli O157:H7, Salmonella or Campylobacter can be easily transmitted from animals' gut to animal food products, they might cause a serious illness, if further transmitted to humans due to improper cooking and preparation procedure (Kassenborg et al., 2004; Tauxe, 1997; Zhao et al., 2001). Therefore, food handlers must be aware that undercooked animal food products present a serious threat for humans. What seems to be a very important finding is the fact that almost 22% of food handlers employed mainly in Serbia and Portugal had no food safety training at all (Veiros, Proença, Santos, Kent-Smith, & Rocha, 2009), although participation in food safety training is a mandatory legal requirement according EU Regulation 178/2002 (EU, 2002) and Serbian Food safety law (Serbia, 2009). That further means that all knowledge showed by food handlers in this study is only related to common food safety knowledge obtained either during formal education, colleagues or via different media, TV, internet or newspapers. On the other side, 78% of food handlers had participated in some food safety training, organised

193

by either governmental or non-governmental institutions. Even though it is assumed that they had passed training and accepted given information related to food handling practices and food safety issues, they did not perform significantly better than nontrained participants. Despite this, the most appropriate way to fill-in identified gaps and to acquire adequate knowledge is to create training and educational material with the focus on the most critical issues where the greatest knowledge gaps have been identified, such as temperature control, source of contamination of foods and food-stuffs and high-risk foods. Training programs should not be performed only to satisfy legal requirements and to provide basic and general information. They should serve as a major tool to communicate with food handlers, by simple and targeted explanation related to specific identified issues. Furthermore, knowledge maintenance and behavioural changes among food handlers should be monitored, with targeted and focused refreshments trainings that can be designed and implemented. As Clayton, Griffith, Price, and Peters, (2002) indicated, trained food handlers identified several barriers in implementation of knowledge skills, such as lack of time, lack of staff and a lack of resources. Thus effectiveness of the training increases when combined with some type of behavioural interventions such as showing case studies of poisoned victims to incorporate the emotion of fear into individuals, especially those with children (Soon, Baines, & Seaman, 2012), as well as motivational programs (Pellegrino, Crandall, O'Bryan, & Seo, 2015). In addition, food handlers often underestimate themselves and the risk of their own role in the safety of food. 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 food establishments. Food safety managers should be proactive and dedicated in supervising food handlers' activities and on-site correcting/training of handlers in order to improve and advance food and hygiene. According to Hofstede et al.(Hofstede, Hofstede, & Minkov, 2010), the three European countries involved in this study have one cultural dimension in common e the high power distance index. This means that workers expect to be told what to do, regardless of their knowledge. In companies there is one manager who takes complete responsibility, including the level of food safety. This may be one of the reasons for some incorrect answers related to hygiene practices as a result of workers knowledge overruled by their bosses understanding of food safety. This cultural aspect should not be omitted when food safety trainings are organised and their implementation and behaviour changes followed up. Food safety trainings should not provide only basic information on food hygiene. They should be deployed as targeted and simplified explanation of specific issues, such as time and temperature and cross contamination. Additionally, the in-depth comprehension and application of the acquired knowledge is needed and still must be improved. As indicated by our results food handler's attendance to training on food safety does not always imply effective behaviour changes, pointing to the need for improving either training materials and contents as well as training methodologies. On the job training may be a potential strategy to overcome this issue. 5. Conclusion Findings in this study provide very important information on the level of food safety knowledge and major knowledge gaps among food handlers in three European countries, including temperature control, food products and related food-borne diseases and cross contamination. Qualified staffs are key to success and innovative food knowledge strategies should offer a wide spectrum

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